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Convergence and divergence in gne expression profiles induced by leaf senescence and 27 senescence-promoting hormonal, pathological and environmental stress treatments
Abstract
In addition to age and developmental progress, leaf senescence and senescence-associated genes (SAGs) can be induced by other factors such as plant hormones, pathogen infection and environmental stresses. The relationship is not clear, however, between these induced senescence processes and developmental leaf senescence, and to what extent these senescence-promoting signals mimic age and developmental senescence in terms of gene expression profiles. By analysing microarray expression data from 27 different treatments (that are known to promote senescence) and comparing them with that from developmental leaf senescence, we were able to show that at early stages of treatments, different hormones and stresses showed limited similarity in the induction of gene expression to that of developmental leaf senescence. Once the senescence process is initiated, as evidenced by visible yellowing, generally after a prolonged period of treatments, a great proportion of SAGs of developmental leaf senescence are shared by gene expression profiles in response to different treatments. This indicates that although different signals that lead to initiation of senescence may do so through distinct signal transduction pathways, senescence processes induced either developmentally or by different senescence-promoting treatments may share common execution events.
... Previous studies have found that although the initiation signals of leaf senescence are different, plant leaves show similar morphological, physiological, biochemical and transcriptional changes, which are the consequence of the similar signal transduction systems both in age-dependent and stress-induced leaf senescence (Guo et al., 2004;Guo and Gan, 2005). Meanwhile, many senescence associated genes (SAGs) are involved in both age-dependent senescence and stress-induced senescence (van der Graaff et al., 2006;Guo and Gan, 2012), therefore, the underlying regulatory mechanisms may overlap . Protein kinases, such as RPK1 and SnRK1, are also involved in both age-dependent senescence and stress-induced senescence Cho et al., 2012;Kim et al., 2017;Koo et al., 2017). ...
... There are about 80 MAPKKKs, 10 MAPKKs, and 20 MAPKs in Arabidopsis, some of which being involved in several signaling networks having an integrative function in the plants response to their environment (Chardin et al., 2017;Jagodzik et al., 2018). A variety of transcriptome analysis revealed a large number of MAPKs kinases with altered expression patterns during leaf senescence (Buchanan-Wollaston et al., 2003;Guo et al., 2004;Breeze et al., 2011;Guo and Gan, 2012). An Arabidopsis MAPKKK, MEKK1 (MAP kinase or ERK kinase kinase 1) affects leaf senescence by binding with an important senescence transcription factor WRKY53 (Miao et al., 2007), while the MEKK1-MKK1/2-MPK4 cascade negatively regulates innate immune responses (Gao et al., 2008;Kong et al., 2012); Another Arabidopsis MAPKKK kinase, EDR1 (enhanced disease resistance 1), plays a negative role in powdery mildew resistance and ethylene induced leaf senescence (Tang and Innes, 2002); the rice MAPKKK, SLES (spotted leaf sheath) is involved in disease resistance and leaf senescence by regulating the dynamic balance of ROS (Lee et al., 2018). ...
... Many kinase-associated mutants and/or transgenic plants were detected earlier/delayed leaf senescence phenotype and these materials played roles to find new components and their regulatory networks involved in the leaf senescence process (Li Z. et al., 2020). A large number of SAGs have been found by differential expression techniques in different plants (Guo et al., 2004;Buchanan-Wollaston et al., 2005;Breeze et al., 2011;Guo and Gan, 2012), and some SAGs were protein kinases, which play roles in signal transduction during leaf senescence. The researchers have found lots of SAPs (senescence associated proteins) through proteomics approaches and combined the information of metabolites change by metabolomics during leaf senescence, however, no protein kinase was detected as SAPs because of their low abundance in nature (Hebeler et al., 2008;Watanabe et al., 2013;Balazadeh et al., 2014;Moschen et al., 2016;Wei et al., 2016). ...
Leaf senescence is an evolutionarily acquired process and it is critical for plant fitness. During senescence, macromolecules and nutrients are disassembled and relocated to actively growing organs. Plant leaf senescence process can be triggered by developmental cues and environmental factors, proper regulation of this process is essential to improve crop yield. Protein kinases are enzymes that modify their substrates activities by changing the conformation, stability, and localization of those proteins, to play a crucial role in the leaf senescence process. Impressive progress has been made in understanding the role of different protein kinases in leaf senescence recently. This review focuses on the recent progresses in plant leaf senescence-related kinases. We summarize the current understanding of the function of kinases on senescence signal perception and transduction, to help us better understand how the orderly senescence degeneration process is regulated by kinases, and how the kinase functions in the intricate integration of environmental signals and leaf age information.
... Ethylene, jasmonic acid (JA), salicylic acid (SA), abscisic acid (ABA), and strigolactones (SLs) promote leaf senescence, while cytokinins (CKs), gibberellic acid (GA), and auxin delay leaf senescence Amasino 1995, 1997;Lim et al. 2007;Miao and Zentgraf 2007;Li et al. 2013;Zhang et al. 2013). Multiple environmental factors, including abiotic stresses such as drought, salt, DNA damage, high or low temperature, darkness and nutrient deficiency, and biotic stresses such as pathogen infection and phloem-feeding insects are also critical in regulating senescence (Lim et al. 2007; Guo and Gan 2012;Sade et al. 2018). Recent studies reveal that DNA damage, caused by endogenous insults or exogenous genotoxic stresses, might be one of the main determinants of leaf senescence Zhang et al. 2020c). ...
... For plants, stress-induced premature senescence may not be a passive choice, but is an evolutionary fitness strategy, which speeds up the reproduction of the next generation under unfavorable living conditions (Sade et al. 2018). However, each factor does not work independently, but has mutual promotion or inhibition (Guo and Gan 2012). Environmental stress factors trigger the changes of endogenous hormones, and then affect leaf senescence through a complex regulatory network instead of a linear way. ...
... In contrast with the global upregulation of ATG genes, only a fraction of the proteasome subunit genes increases their expression during senescence (Guo and Gan 2012). In senescing leaves of oilseed rape, barley, and Arabidopsis, the proteasome is highly active (Poret et al. 2016;Velasco-Arroyo et al. 2016). ...
Leaf senescence, the last stage of leaf development, is a type of postmitotic senescence and is characterized by the functional transition from nutrient assimilation to nutrient remobilization which is essential for plants’ fitness. The initiation and progression of leaf senescence are regulated by a variety of internal and external factors such as age, phytohormones, and environmental stresses. Significant breakthroughs in dissecting the molecular mechanisms underpinning leaf senescence have benefited from the identification of senescence-altered mutants through forward genetic screening and functional assessment of hundreds of senescence-associated genes (SAGs) via reverse genetic research in model plant Arabidopsis thaliana as well as in crop plants. Leaf senescence involves highly complex genetic programs that are tightly tuned by multiple layers of regulation, including chromatin and transcription regulation, post-transcriptional, translational and post-translational regulation. Due to the significant impact of leaf senescence on photosynthesis, nutrient remobilization, stress responses, and productivity, much effort has been made in devising strategies based on known senescence regulatory mechanisms to manipulate the initiation and progression of leaf senescence, aiming for higher yield, better quality, or improved horticultural performance in crop plants. This review aims to provide an overview of leaf senescence and discuss recent advances in multi-dimensional regulation of leaf senescence from genetic and molecular network perspectives. We also put forward the key issues that need to be addressed, including the nature of leaf age, functional stay-green trait, coordination between different regulatory pathways, source-sink relationship and nutrient remobilization, as well as translational researches on leaf senescence.
... In addition, plant hormones can integrate environmental signals into the process of plant development, thus altering leaf senescence (Lee and Masclaux-Daubresse 2021). Nevertheless, the effect of environmental factors on leaf senescence is not independent but involves mutual promotion or inhibition (Guo and Gan 2012). Thus, interactions between plant hormones, developmental processes and environmental factors may determine the onset of leaf senescence. ...
... Nutrient deficiency is an important environmental factor that induces leaf senescence, and deficiency of any nutrient can cause early leaf senescence (Sade et al. 2018;Guo and Gan 2012). N is an essential element for plant growth and development, and its deficiency tends to induce rapid leaf senescence (Park et al. 2018). ...
Although it is well established that nitrogen (N) deficiency induces leaf senescence, the molecular mechanism of N deficiency-induced leaf senescence remains largely unknown. Here, we show that an abscisic acid (ABA)-responsive NAC transcription factor (TF) is involved in N deficiency-induced leaf senescence. The overexpression of MdNAC4 led to increased ABA levels in apple calli by directly activating the transcription of the ABA biosynthesis gene MdNCED2 . In addition, MdNAC4 overexpression promoted N deficiency-induced leaf senescence. Further investigation showed that MdNAC4 directly bound the promoter of the senescence-associated gene (SAG) MdSAG39 and upregulated its expression. Interestingly, the function of MdNAC4 in promoting N deficiency-induced leaf senescence was enhanced in the presence of ABA. Furthermore, we identified an interaction between the ABA receptor protein MdPYL4 and the MdNAC4 protein. Moreover, MdPYL4 showed a function similar to that of MdNAC4 in ABA-mediated N deficiency-induced leaf senescence. These findings suggest that ABA plays a central role in N deficiency-induced leaf senescence and that MdPYL4 interacts with MdNAC4 to enhance the response of the latter to N deficiency, thus promoting N deficiency-induced leaf senescence. In conclusion, our results provide new insight into how MdNAC4 regulates N deficiency-induced leaf senescence.
Graphical Abstract
... In this study, IDL6 peptides were found to function in promoting age-dependent leaf senescence and senescence induced by darkness, ABA and ethylene treatments. Cross-talks between plant senescence and stress responses have been well recognized in earlier studies (Guo and Gan, 2012;Guo et al., 2021). IDL6 could be induced rapidly by various biotic and abiotic stresses, such as cold, salt, UV, P. syringae (Vie et al., 2015). ...
... The roles of phytohormones in leaf senescence have been well established (Guo and Gan, 2012). The transcriptome analysis in this study revealed multiple DEGs related to phytohormones in the idl6 mutant (Figures 6B,D). ...
Leaf senescence is a highly coordinated process and has a significant impact on agriculture. Plant peptides are known to act as important cell-to-cell communication signals that are involved in multiple biological processes such as development and stress responses. However, very limited number of peptides has been reported to be associated with leaf senescence. Here, we report the characterization of the INFLORESCENCE DEFICIENT IN ABSCISSION-LIKE6 (IDL6) peptide as a regulator of leaf senescence. The expression of IDL6 was up-regulated in senescing leaves. Exogenous application of synthetic IDL6 peptides accelerated the process of leaf senescence. The idl6 mutant plants showed delayed natural leaf senescence as well as senescence included by darkness, indicating a regulatory role of IDL6 peptides in leaf senescence. The role of IDL6 as a positive regulator of leaf senescence was further supported by the results of overexpression analysis and complementation test. Transcriptome analysis revealed differential expression of phytohormone-responsive genes in idl6 mutant plants. Further analysis indicated that altered expression of IDL6 led to changes in leaf senescence phenotypes induced by ABA and ethylene treatments. The results from this study suggest that the IDL6 peptide positively regulates leaf senescence in Arabidopsis thaliana.
... In the case of pathogen infection, immune responses are induced and interfere with age-induced senescence signals, which can, in some cases, lead to a precocious senescence [2]. Interestingly, large-scale analyses of gene expression in senescing leaves of A. thaliana revealed that defence-related genes represent a significant portion of the leaf senescence transcriptome [8]. Indeed, it has been shown that their respective signalling pathways greatly overlap and several senescence-associated genes (SAGs) are activated during both development and defence [8][9][10]. ...
... Interestingly, large-scale analyses of gene expression in senescing leaves of A. thaliana revealed that defence-related genes represent a significant portion of the leaf senescence transcriptome [8]. Indeed, it has been shown that their respective signalling pathways greatly overlap and several senescence-associated genes (SAGs) are activated during both development and defence [8][9][10]. A large fraction of the genes that operate at the nexus of development and defence encode proteins involved in hormonal signalling. ...
In annual plants, tight coordination of successive developmental events is of primary importance to optimize performance under fluctuating environmental conditions. The recent finding of the genetic interaction of WRKY53 , a key senescence-related gene with REVOLUTA , a master regulator of early leaf patterning, raises the question of how early and late developmental events are connected. Here, we investigated the developmental and metabolic consequences of an alteration of the REVOLUTA and WRKY53 gene expression, from seedling to fruiting. Our results show that REVOLUTA critically controls late developmental phases and reproduction while inversely WRKY53 determines vegetative growth at early developmental stages. We further show that these regulators of distinct developmental phases frequently, but not continuously, interact throughout ontogeny and demonstrated that their genetic interaction is mediated by the salicylic acid (SA). Moreover, we showed that REVOLUTA and WRKY53 are keys regulatory nodes of development and plant immunity thought their role in SA metabolic pathways, which also highlights the role of REV in pathogen defence. Together, our findings demonstrate how late and early developmental events are tightly intertwined by molecular hubs. These hubs interact with each other throughout ontogeny, and participate in the interplay between plant development and immunity.
... As a very intricate and exquisite physiological process, senescence is a necessary stage in the natural development of plants and is controlled by a series of internal factors (Guo and Gan, 2012). It is also affected by a variety of environmental factors including pathogen infection (Guo and Gan, 2005). ...
... Plant hormones also act a key role in controlling the progression of leaf senescence. ABA, ET, JA, and SA are considered as senescence promotors, while auxins, CKs, and GAs are senescence suppressors (Guo and Gan, 2012;Estornell et al., 2013). For example, the SA and ABA-related genes in A. thaliana were significantly upregulated in normal leaves as compared with the senescing ones (van der Graaff et al., 2006;Breeze et al., 2011); the transcriptome analysis of the calyx abscission zone of Huanglongbing-diseased sweet orange revealed that ET and JA signaling are involved in regulating the fruit abscission (Zhao et al., 2019). ...
Colletotrichum fructicola infects pear leaves, resulting in two major symptoms: tiny black spots (TS) followed by severe early defoliation and big necrotic lesions (BnL) without apparent damage depending on the pathotypes. How the same fungal species causes different symptoms remains unclear. To understand the molecular mechanism underlying the resulting diseases and the diverse symptoms, two C. fructicola pathogenetic strains (PAFQ31 and PAFQ32 responsible for TS and BnL symptoms, respectively) were inoculated on Pyrus pyrifolia leaves and subjected to transcriptome sequencing at the quiescent stage (QS) and necrotrophic stage (NS), respectively. In planta, the genes involved in the salicylic acid (SA) signaling pathway were upregulated at the NS caused by the infection of each strain. In contrast, the ethylene (ET), abscisic acid (ABA), and jasmonic acid (JA) signaling pathways were specifically related to the TS symptoms caused by the infection of strain PAFQ31, corresponding to the yellowish and early defoliation symptoms triggered by the strain infection. Correspondingly, SA was accumulated in similar levels in the leaves infected by each strain at NS, but JA was significantly higher in the PAFQ31-infected as measured using high-performance liquid chromatography. Weighted gene co-expression network analysis also reveals specific genes, pathways, phytohormones, and transcription factors (TFs) associated with the PAFQ31-associated early defoliation. Taken together, these data suggest that specific metabolic pathways were regulated in P. pyrifolia in response to the infection of two C. fructicola pathotypes resulting in the diverse symptoms: JA, ET, and ABA accumulated in the PAFQ31-infected leaves, which negatively affected the chlorophyll metabolism and photosynthesis pathways while positively affecting the expression of senescence-associated TFs and genes, resulted in leaf yellowing and defoliation; whereas SA inhibited JA-induced gene expression in the PAFQ32-infected leaves, which led to hypersensitive response-like reaction and BnL symptoms.
... In addition, the involvement of DNA methylation in maintaining genome integrity by silencing TEs and repetitive sequences during senescence has been reported before [20,21]. Studies on Arabidopsis and barley have shown the release of TEs during leaf senescence [22,23]. He et al. [24] detected a retrotransposon, called "NMR19" (naturally occurring DNA methylation variation region 19), and its location in the genome, and found that the status of its methylation varies among different Arabidopsis thaliana ecotypes. ...
... However, the overlap between the signaling pathways of programmed and induced senescence is not well understood. Guo and Gan [22] studied the effect of 27 senescence-promoting stresses on the transcription of senescence genes and found that after long-term stress treatment, the signaling pathway during senescence progression overlaps between induced and programmed senescence; however, only small similarity was found at the beginning of stress treatment, suggesting that the initial stage of senescence is probably very specific. ...
Senescence is a major developmental transition in plants that requires a massive reprogramming of gene expression and includes various layers of regulations. Senescence is either an age-dependent or a stress-induced process, and is under the control of complex regulatory networks that interact with each other. It has been shown that besides genetic reprogramming, which is an important aspect of plant senescence, transcription factors and higher-level mechanisms, such as epigenetic and small RNA-mediated regulators, are also key factors of senescence-related genes. Epigenetic mechanisms are an important layer of this multilevel regulatory system that change the activity of transcription factors (TFs) and play an important role in modulating the expression of senescence-related gene. They include chromatin remodeling, DNA methylation, histone modification, and the RNA-mediated control of transcription factors and genes. This review provides an overview of the known epigenetic regulation of plant senescence, which has mostly been studied in the form of leaf senescence, and it also covers what has been reported about whole-plant senescence.
... Developmentally regulated senescence has been studied in leaves (Zhang and Gan 2012;Jiang et al. 2014), fruits ) and flowers Lü et al. 2014), and it has also been shown that environmental conditions, such as drought, darkness, high temperature and salinity, as well as pathogen challenge, can trigger organ senescence (Sade et al. 2018;Patharkar and Walker 2019). However, the mechanistic relationships between senescence that is developmentally programmed or that which is environmentally induced, or the nature of any shared signaling pathways, are not well understood (Guo and Gan 2012). ...
... As well as being developmentally controlled, the onset of senescence can also be induced by unfavorable environmental conditions, such as water deficit (Sade et al. 2018;Patharkar and Walker 2019;Guo and Gan 2012). In the context of senescence, expression profiling of A. thaliana TFs has revealed that a considerable number are induced during senescence and are also upregulated by various stresses, suggesting extensive overlap between senescence and stress responses (Chen et al. 2002;Li et al. 2018). ...
Petals and leaves share common evolutionary origins but have different phenotypic characteristics, such as the absence of stomata in the petals of most angiosperm species. Plant NAC transcription factor, NAP, is involved in ABA responses and regulates senescence-associated genes, and especially those that affect stomatal movement. However, the regulatory mechanisms and significance of NAP action in senescing astomatous petals is unclear. A major limiting factor is failure of flower opening and accelerated senescence. Our goal is to understand the finely regulatory mechanism of dehydration tolerance and aging in rose flowers. We functionally characterized RhNAP, an AtNAP-like transcription factor gene that is induced by dehydration and aging in astomatous rose petals. Cytokinins (CKs) are known to delay petal senescence and we found that a cytokinin oxidase/dehydrogenase gene 6 (RhCKX6) shares similar expression patterns with RhNAP. Silencing of RhNAP or RhCKX6 expression in rose petals by virus induced gene silencing markedly reduced petal dehydration tolerance and delayed petal senescence. Endogenous CK levels in RhNAP- or RhCKX6-silenced petals were significantly higher than those of the control. Moreover, RhCKX6 expression was reduced in RhNAP-silenced petals. This suggests that the expression of RhCKX6 is regulated by RhNAP. Yeast one-hybrid experiments and electrophoresis mobility shift assays showed that RhNAP binds to the RhCKX6 promoter in heterologous in vivo system and in vitro, respectively. Furthermore, the expression of putative signal transduction and downstream genes of ABA-signaling pathways were also reduced due to the repression of PP2C homolog genes by RhNAP in rose petals. Taken together, our study indicates that the RhNAP/RhCKX6 interaction represents a regulatory step enhancing dehydration tolerance in young rose petals and accelerating senescence in mature petals in a stomata-independent manner.
Supplementary Information
The online version contains supplementary material available at 10.1186/s43897-021-00016-7.
... Leaf senescence also occurs in an age-dependent manner under controlled growth conditions. Comparative analysis of transcriptomic changes in response to different senescenceinducing stress treatments and during developmental senescence has suggested that during the execution process of senescence, a significant proportion of gene expression changes are shared between stress-induced and natural senescence (Guo and Gan, 2012). In fact, leaf senescence is closely related to plant environmental stress tolerance. ...
... Leaf senescence is tightly linked to environmental adaptability, and the senescence process can be induced by multiple environmental stimuli (Guo and Gan, 2012;Sade et al., 2017). CLE14 expression in detached leaves was induced by ABA, JA, SA, NaCl, and drought treatments, whereas ACC, GR24, and IAA treatments did not cause a significant change in CLE14 transcript levels (Figure 2A and 2B). ...
Leaf senescence is an important developmental process in plants' life cycle and has a significant impact on agriculture. As an adaptive mechanism, when facing harsh environmental conditions, monocarpic plants often initiate leaf senescence early to ensure a complete life cycle. Upon initiation, the senescence process is fine-tuned through the coordination of both positive and negative regulators. Here we report a small secreted peptide, CLAVATA3/ESR-RELATED (CLE) 14, which functions in suppressing leaf senescence through regulating ROS homeostasis in Arabidopsis. Expression of the CLE14-encoding gene in leaves was significantly induced by age, high salinity, abscisic acid (ABA), salicylic acid (SA) and jasmonic acid (JA). CLE14 knock-out plants displayed accelerated progression of both natural and salinity-induced leaf senescence. On the other hand, increased CLE14 expression or treatments with synthetic CLE14 peptides delayed senescence. CLE14 peptide treatments also caused delay in ABA-induced senescence in detached leaves. Further analysis showed that CLE14 gain-of-function led to reduced ROS levels in leaves, where higher expression of ROS scavenging genes were detected. Moreover, CLE14 signaling resulted in transcriptional activation of JUB1, a NAC family transcription factor previously identified as a negative regulator of senescence. Notably, the function of CLE14 peptides was JUB1-dependent in delaying leaf senescence, reducing H2O2 level, and activating ROS scavenging genes. We propose that small peptide CLE14 serves as a novel "brake signal" in regulating age-dependent and stress-induced leaf senescence through JUB1-mediated ROS scavenging.
... The process of leaf senescence is precisely regulated directly or indirectly by internal signals such as developmental age, hormone level (Hensel et al. 1993;Koyama 2018) and external signals including extreme temperature, drought, injury, nutrient deficiency, pathogen infection, UV-B radiation, ozone oxidative stress (Lim et al. 2007;Guo and Gan 2012;Gregersen et al. 2013), while environmental stresses are generally integrated into the regulation of senescence by altering hormone levels in plants. In complex regulatory network during leaf senescence, the transcription factors (TFs) play an important role, for example, several NAC members have been revealed to serve crucial roles. ...
Leaf senescence, the last stage of leaf development, is essential for crop yield by promoting nutrition relocation from senescence leaves to new leaves and seeds. NAC (NAM/ATAF1/ATAF2/CUC2) proteins, one of the plant-specific transcription factors, widely distribute in plants and play important roles in plant growth and development. Here, we identified a new NAC member OsNAC103 and found that it plays critical roles in leaf senescence and plant architecture in rice. OsNAC103 mRNA levels were dramatically induced by leaf senescence as well as different phytohormones such as ABA, MeJA and ACC and abiotic stresses including dark, drought and high salinity. OsNAC103 acts as a transcription factor with nuclear localization signals at the N terminal and a transcriptional activation signal at the C terminal. Overexpression of OsNAC103 promoted leaf senescence while osnac103 mutants delayed leaf senescence under natural condition and dark-induced condition, meanwhile, senescence-associated genes (SAGs) were up-regulated in OsNAC103 overexpression (OsNAC103-OE) lines, indicating that OsNAC103 positively regulates leaf senescence in rice. Moreover, OsNAC103-OE lines exhibited loose plant architecture with larger tiller angles while tiller angles of osnac103 mutants decreased during the vegetative and reproductive growth stages due to the response of shoot gravitropism, suggesting that OsNAC103 can regulate the plant architecture in rice. Taken together, our results reveal that OsNAC103 plays crucial roles in the regulation of leaf senescence and plant architecture in rice.
... Interestingly, many stress-related genes might also be involved in plant senescence process. To date, extensive studies have revealed that a wide range of transcription factors, including WRKY and NAC, are involved in the regulation of age-dependent as well as stress-induced leaf senescence [40][41][42]. For example, WRKY54 and WRKY70 act synergistically as the negative regulators of leaf senescence in Arabidopsis, participating in a regulatory network integrating internal and environmental cues to regulate the onset and progression of leaf senescence [43]. ...
As the final stage of leaf development, leaf senescence is affected by a variety of internal and external signals including age and environmental stresses. Although significant progress has been made in elucidating the mechanisms of age-dependent leaf senescence, it is not clear how stress conditions induce a similar process. Here, we report the roles of a stress-responsive and senescence-induced gene, ERD7 (EARLY RESPONSIVE TO DEHYDRATION 7), in regulating both age-dependent and stress-induced leaf senescence in Arabidopsis. The results showed that the leaves of erd7 mutant exhibited a significant delay in both age-dependent and stress-induced senescence, while transgenic plants overexpressing the gene exhibited an obvious accelerated leaf senescence. Furthermore, based on the results of LC-MS/MS and PRM quantitative analyses, we selected two phosphorylation sites, Thr-225 and Ser-262, which have a higher abundance during senescence, and demonstrated that they play a key role in the function of ERD7 in regulating senescence. Transgenic plants overexpressing the phospho-mimetic mutant of the activation segment residues ERD7T225D and ERD7T262D exhibited a significantly early senescence, while the inactivation segment ERD7T225A and ERD7T262A displayed a delayed senescence. Moreover, we found that ERD7 regulates ROS accumulation by enhancing the expression of AtrbohD and AtrbohF, which is dependent on the critical residues, i.e., Thr-225 and Ser-262. Our findings suggest that ERD7 is a positive regulator of senescence, which might function as a crosstalk hub between age-dependent and stress-induced leaf senescence.
... Leaf senescence is the last and inevitable stage of leaf development, which directly affects crop yield and quality (Lim et al. 2007). The senescence process is not only genetically programmed but also induced by exogenous stress to ensure completion of the plant life cycle, successful reproduction and environmental adaptability (Guo and Gan 2012;Maillard et al. 2015;Have et al. 2017;Sade et al. 2018;Woo et al. 2019;Zhang et al. 2022). Therefore, an in-depth understanding of the regulatory mechanisms of leaf senescence is of great importance. ...
Characterization of the early leaf senescence mutant els3 and identification of its causal gene ELS3, which encodes an LRR-RLK protein in wheat.
Leaf senescence is an important agronomic trait that affects both crop yield and quality. However, few senescence-related genes in wheat have been cloned and functionally analyzed. Here, we report the characterization of the early leaf senescence mutant els3 and fine mapping of its causal gene ELS3 in wheat. Compared with wild-type Yanzhan4110 (YZ4110), the els3 mutant had a decreased chlorophyll content and a degraded chloroplast structure after the flowering stage. Further biochemical assays in flag leaves showed that the superoxide anion and hydrogen peroxide contents increased, while the activities of antioxidant enzymes, including catalase, superoxide dismutase and glutathione reductase, decreased gradually after the flowering stage in the els3 mutant. To clone the causal gene underlying the phenotype of leaf senescence, a genetic map was constructed using 10,133 individuals of F2:3 populations, and ELS3 was located in a 2.52 Mb region on chromosome 2DL containing 16 putative genes. Subsequent sequence analysis and gene annotation identified only one SNP (C to T) in the first exon of TraesCS2D02G332700, resulting in an amino acid substitution (Pro329Ser), and TraesCS2D02G332700 was preliminarily considered as the candidate gene of ELS3. ELS3 encodes a leucine-rich repeat receptor-like kinase (LRR-RLK) protein that is localized on the cell membrane. We also found that the transient expression of mutant TraesCS2D02G332700 can induce leaf senescence in N. benthamiana. Taken together, TraesCS2D02G332700 is likely to be the candidate gene of ELS3 and may have a function in regulating leaf senescence.
... CCGs, including NYC1, NYE1/SGR1, NYE2/SGR2, and PHEOPHORBIDE a OXYGENASE (PaO), play key roles in regulating chlorophyll breakdown [51]. Drought-induced leaf senescence happens gradually, and previous studies have shown that some genes are involved in senescence and also play crucial roles in stress response [52,53]. The overexpression of GhTZF1 enhanced drought tolerance and delayed drought-induced leaf senescence through regulating the expression of antioxidant genes and SAGs in transgenic Arabidopsis [54]. ...
Plants face various biotic and abiotic stress factors during their growth and development, among which, drought is a serious adverse factor that affects yield and quality in agriculture and forestry. Several transcription factors are involved in regulating plant responses to drought stress. In this study, the B-box (BBX) transcription factor CoBBX24 was cloned from Camellia oleifera. This gene encodes a 241-amino-acid polypeptide containing two B-box domains at the N-terminus. A phylogenetic analysis revealed that CoBBX24 and CsBBX24 from Camellia sinensis are in the same branch, with their amino acid sequences being identical by 96.96%. CoBBX24 was localized to the nucleus and acted as a transcriptional activator. The overexpression of CoBBX24 in Arabidopsis heightened its drought tolerance along with a relatively high survival rate, and the rate of water loss in the OX-CoBBX24 lines was observably lower than that of the wild-type. Compared to the wild-type, the root lengths of the OX-CoBBX24 lines were significantly inhibited with abscisic acid. Leaf senescence was delayed in the OX-CoBBX24 lines treated with abscisic acid. The expression of genes related to leaf senescence and chlorophyll breakdown (e.g., SAG12, SAG29, NYC1, NYE1, and NYE2) was downregulated in the OX-CoBBX24 lines. This study indicated that CoBBX24 positively regulates the drought tolerance in Arabidopsis through delayed leaf senescence.
... However, when plants are exposed to shade or complete darkness for an extended period, it triggers leaf senescence [37,[77][78][79][80][81]. Transcriptomic analysis has shown that gene expression changes induced by darkness closely resemble those observed during natural senescence [82][83][84][85]. In fact, more than 50% of the genes up-regulated during natural senescence are also up-regulated under dark treatment conditions [83]. ...
Leaf senescence is a natural phenomenon that occurs during the aging process of plants and is influenced by various internal and external factors. These factors encompass plant hormones, as well as environmental pressures such as inadequate nutrients, drought, darkness, high salinity, and extreme temperatures. Abiotic stresses accelerate leaf senescence, resulting in reduced photosynthetic efficiency, yield, and quality. Gaining a comprehensive understanding of the molecular mechanisms underlying leaf senescence in response to abiotic stresses is imperative to enhance the resilience and productivity of crops in unfavorable environments. In recent years, substantial advancements have been made in the study of leaf senescence, particularly regarding the identification of pivotal genes and transcription factors involved in this process. Nevertheless, challenges remain, including the necessity for further exploration of the intricate regulatory network governing leaf senescence and the development of effective strategies for manipulating genes in crops. This manuscript provides an overview of the molecular mechanisms that trigger leaf senescence under abiotic stresses, along with strategies to enhance stress tolerance and improve crop yield and quality by delaying leaf senescence. Furthermore, this review also highlighted the challenges associated with leaf senescence research and proposes potential solutions.
... Although beautiful autumn colours are widely appreciated by the public, senescence regulation at the molecular level is not well understood. Research efforts 1-3 , such as genetic approaches, transcriptomics, metabolomics and external applications of phytohormones have identified genes where mutations lead to premature or delayed senescence, senescence-associated genes (SAGs) that are up-or downregulated in senescing leaves, and metabolic signals such as reactive oxygen species (ROS) that are involved in the process [4][5][6][7][8] . Yet, there is no consensus on the senescence trigger, which metabolites, genes or post-translational mechanisms are the most important ones-across species-for the process, or which environmental factors could consistently explain why senescence starts at a certain time in trees in nature. ...
Deciduous trees exhibit a spectacular phenomenon of autumn senescence driven by the seasonality of their growth environment, yet there is no consensus which external or internal cues trigger it. Senescence starts at different times in European aspen (Populus tremula L.) genotypes grown in same location. By integrating omics studies, we demonstrate that aspen genotypes utilize similar transcriptional cascades and metabolic cues to initiate senescence, but at different times during autumn. The timing of autumn senescence initiation appeared to be controlled by two consecutive “switches”; 1) first the environmental variation induced the rewiring of the transcriptional network, stress signalling pathways and metabolic perturbations and 2) the start of senescence process was defined by the ability of the genotype to activate and sustain stress tolerance mechanisms mediated by salicylic acid. We propose that salicylic acid represses the onset of leaf senescence in stressful natural conditions, rather than promoting it as often observed in annual plants.
... At the biochemical level, intracellular macromolecules (including proteins, lipids, and carbohydrates) are degraded. At the molecular level, leaf senescence involves drastic changes in gene expression, including genes that are up-and down-regulated during aging (Buchanan-Wollaston et al., 2005;Guo and Gan, 2012). Senescence up-regulated genes, named SENESCENCE-ASSOCIATED GENES (SAGs), comprise genes encoding proteins involved in the execution of senescence, including transcription factors, proteases, and signal transduction components (Woo et al., 2019;Guo et al., 2021). ...
Receptor-like kinases (RLKs) are the most important class of cell surface receptors and play crucial roles in plant development and stress responses. However, few studies were reported about the biofunctions of RLK in leaf senescence. In the current study, we characterized a novel RLK-encoding gene senescence-related receptor kinase 1 (SENRK1), which was significantly down-regulated during leaf senescence. Notably, the loss-of-function senrk1 mutants displayed an early leaf senescence phenotype, while overexpression of SENRK1 significantly delayed leaf senescence, indicating that SENRK1 negatively regulates age-dependent leaf senescence in Arabidopsis. Furthermore, the senescence-promoting transcription factor WRKY53 is able to repress the expression of SENRK1. While the wrky53 mutant showed a delayed senescence phenotype as reported, the wrky53 senrk1-1 double mutant exhibited precocious leaf senescence, suggesting that SENRK1 functions downstream of WRKY53 in regulating age-dependent leaf senescence in Arabidopsis.
... By monitoring leaf yellowing in conjunction with taking chlorophyll content measurements, the progression of senescence can be evaluated and compared across different senescenceinducing conditions. Since the molecular responses that are important during early senescence differ among various senescence conditions, comparative transcriptome analyses should be conducted at similar and early stages of senescence (Guo and Gan, 2012). Furthermore, the early senescence stage is considered useful for identifying regulatory genes that can be used for genetic modification to regulate leaf senescence (Lim et al., 2007). ...
The lawn grass Zoysia japonica is widely cultivated for its ornamental and recreational value. However, its green period is subject to shortening, which significantly decreases the economic value of Z. japonica , especially for large cultivations. Leaf senescence is a crucial biological and developmental process that significantly influences the lifespan of plants. Moreover, manipulation of this process can improve the economic value of Z. japonica by extending its greening period. In this study, we conducted a comparative transcriptomic analysis using high-throughput RNA sequencing (RNA-seq) to investigate early senescence responses triggered by age, dark, and salt. Gene set enrichment analysis results indicated that while distinct biological processes were involved in each type of senescence response, common processes were also enriched across all senescence responses. The identification and validation of differentially expressed genes (DEGs) via RNA-seq and quantitative real-time PCR provided up- and down-regulated senescence markers for each senescence and putative senescence regulators that trigger common senescence pathways. Our findings revealed that the NAC, WRKY, bHLH, and ARF transcription factor (TF) groups are major senescence-associated TF families that may be required for the transcriptional regulation of DEGs during leaf senescence. In addition, we experimentally validated the senescence regulatory function of seven TFs including ZjNAP, ZjWRKY75, ZjARF2, ZjNAC1, ZjNAC083, ZjARF1 , and ZjPIL5 using a protoplast-based senescence assay. This study provides new insight into the molecular mechanisms underlying Z. japonica leaf senescence and identifies potential genetic resources for enhancing its economic value by prolonging its green period.
... The salicylic acid response pathway plays a role in the natural senescence of Arabidopsis leaves (Buchanan-Wollaston et al., 2005). On the other hand, our current knowledge, based also on the modern multi-omics approaches, indicates that the senescence process itself exhibits a certain pattern at the cellular and molecular levels regardless of the origin of its initial promoting factor (Gan and Amasino, 1997;Gan, 2003;Guo and Gan, 2012;reviewed in Kim et al., 2016). In other words, once leaf senescence has started, it always proceeds in a similar way. ...
Increasing crop productivity under optimal conditions and mitigating yield losses under stressful conditions is a major challenge in contemporary agriculture. We have recently identified an effective anti-senescence compound (MTU, [1-(2-methoxyethyl)-3-(1,2,3-thiadiazol-5yl)urea]) in in vitro studies. Here, we show that MTU delayed both age- and stress-induced senescence of wheat plants (Triticum aestivum L.) by enhancing the abundance of PSI supercomplex with LHCa antennae (PSI-LHCa) and promoting the cyclic electron flow (CEF) around PSI. We suppose that this rarely-observed phenomenon blocks the disintegration of photosynthetic apparatus and maintains its activity as was reflected by the faster growth rate of wheat in optimal conditions and under drought and heat stress. Our multiyear field trial analysis further shows that the treatment with 0.4 g ha-1 of MTU enhanced average grain yields of field-grown wheat and barley (Hordeum vulgare L.) by 5-8%. Interestingly, the analysis of gene expression and hormone profiling confirms that MTU acts without the involvement of cytokinins or other phytohormones. Moreover, MTU appears to be the only chemical reported to date to affect PSI stability and activity. Our results indicate a central role of PSI and CEF in the onset of senescence with implications in yield management at least for cereal species.
... The regulatory network of senescence associated genes is constantly updated, and many SAGs were found being involved in gene expression regulation, signal transduction, macromolecular degradation and other senescence processes (He et al., 2001;Gepstein et al., 2003;Buchanan-Wollaston et al., 2005;Guo and Gan, 2012). SAG113 belongs to the PP2C superfamily and plays an indispensable role in plant senescence. ...
Introduction
Alfalfa (Medicago sativa) is a kind of high quality leguminous forage species, which was widely cultivated in the world. Leaf senescence is an essential process in plant development and life cycle. Here, we reported the isolation and functional analysis of an alfalfa SENESCENCE-ASSOCIATED GENE113 (MsSAG113), which belongs to the PP2C family and mainly plays a role in promoting plant senescence.
Methods
In the study, Agrobacterium-mediated, gene expression analysis, next generation sequencing, DNA pull-down, yeast single hybridization and transient expression were used to identify the function of MsSAG113 gene.
Results
The MsSAG113 gene was isolated from alfalfa, and the transgenic plants were obtained by Agrobacterium-mediated method. Compared with the wildtype, transgenic plants showed premature senescence in leaves, especially when cultivated under dark conditions. Meanwhile, application of exogenous hormones ABA, SA, MeJA, obviously acclerated leaf senescence of transgenic plants. Furthermore, the detached leaves from transgenic plants turned yellow earlier with lower chlorophyll content. Transcriptome analysis identified a total of 1,392 differentially expressed genes (DEGs), involving 13 transcription factor families. Of which, 234 genes were related to phytohormone synthesis, metabolism and transduction. Pull-down assay and yeast one-hybrid assay confirmed that alfalfa zinc finger CCCH domain-containing protein 39 (MsC3H-39) could directly bind the upstream of MsSAG113 gene. In conclusion, the MsSAG113 gene plays a crucial role in promoting leaf senescence in alfalfa via participating in the hormone regulatory network.
Discussion
This provides an essential basis for further analysis on the regulatory network involving senescence-associated genes in alfalfa.
... Microgreens senesce fast after harvest and have usually a very small shelf life (1-2 days) at ambient temperature, due to the abrupt disruption of plant growth at a very early stage (Guo and Gan 2012;Xiao et al. 2015). ...
Natural bioactive compounds are molecules’ treasure trove for nutraceuticals, food additives, and functional foods, as they exhibit several structures and activities. Some of these chemicals, such as polyphenols, can be found in high concentrations in nature. However, others are present in such low concentrations that significant harvesting is vital to achieving sufficient quantities, and chemical synthesis is unprofitable due to their structural diversity and complexity. Because screening and synthesizing these compounds are complex, new technologies have been created. The most common approach is traditional liquid or solid–liquid extraction also termed solvent extraction, although modern approaches comprise supercritical and subcritical extractions, pressured liquid extraction, along with microwave and ultrasound-assisted extractions. Such technologies could give a novel technique for increasing the construction of bioactive and usage of such particular compounds as nutraceuticals or as ingredients in functional foods.KeywordsPressured liquid extractionBioactive componentsSolid–liquid extractionFunctional potential
... Microgreens senesce fast after harvest and have usually a very small shelf life (1-2 days) at ambient temperature, due to the abrupt disruption of plant growth at a very early stage (Guo and Gan 2012;Xiao et al. 2015). ...
One of the most critical uses in the food business is the encapsulation of food components. Bioactive components are being used in food applications due to growing consumer interest in natural ingredients. Encapsulation is a promising method for improving the stability of bioactive components while allowing for regulated release. This chapter presents an overview of various encapsulation procedures, viz. spray drying, freeze-drying, extrusion, emulsification, coacervation, cocrystallisation, supercritical fluid method, and different encapsulated bioactive compounds, which have been used to fortify food components and deliver them into various functional foods.
... Microgreens senesce fast after harvest and have usually a very small shelf life (1-2 days) at ambient temperature, due to the abrupt disruption of plant growth at a very early stage (Guo and Gan 2012;Xiao et al. 2015). ...
Microgreens are new specialty crops gaining popularity and increased attention nowadays. These are the juvenile and tender cotyledonary leafy greens having catchy appearance, tender texture, and strong flavor and provide full pack of healthful nutrients. They range in size from 1″ to 1 1/2″ including stem and leaves. Microgreens are considered to be beneficial for health and provide necessary nutrients to human body. Microgreens represent a new group of vegetables considered to be “functional foods” as they possess disease-preventing properties, in addition to their nutritional value. Microgreens have a short life cycle of 5–10 days which may go to few days more if they have not attained the desired height. Common examples of microgreens include red amaranth, green basil, cabbage, broccoli, cilantro, etc. Despite small size, microgreens have strong flavors including higher amounts of vitamins and minerals. Microgreens are rich in various phytochemicals as carotenoids, tocopherols, ascorbic acid, and phylloquinones. Microgreens are perishable and the problem results in case of their post-harvest storage and shelf life. The problems including rotting, foul odor, and premature degradation leads to shorter shelf life and hence, the spoilage of the product.
... Moreover, we found the enrichment of GO terms linked to cell-wall biogenesis and metabolism in RhCIPK6-silenced petals ( Figure 6). Previous studies showed that many cell-wall-degrading genes were regulated during senescence [15,63]. Petal abscission is also associated with pectin solubility in the cell wall [74]. ...
Cultivated roses have the largest global market share among ornamental crops. Postharvest release of ethylene is the main cause of accelerated senescence and decline in rose flower quality. To understand the molecular mechanism of ethylene-induced rose petal senescence, we analyzed the transcriptome of rose petals during natural senescence as well as with ethylene treatment. A large number of differentially expressed genes (DEGs) were observed between developmental senescence and the ethylene-induced process. We identified 1207 upregulated genes in the ethylene-induced senescence process, including 82 transcription factors and 48 protein kinases. Gene Ontology enrichment analysis showed that ethylene-induced senescence was closely related to stress, dehydration, and redox reactions. We identified a calcineurin B-like protein (CBL) interacting protein kinase (CIPK) family gene in Rosa hybrida, RhCIPK6, that was regulated by age and ethylene induction. Reducing RhCIPK6 expression through virus-induced gene silencing significantly delayed petal senescence, indicating that RhCIPK6 mediates petal senescence. In the RhCIPK6-silenced petals, several senescence associated genes (SAGs) and transcription factor genes were downregulated compared with controls. We also determined that RhCIPK6 directly binds calcineurin B-like protein 3 (RhCBL3). Our work thus offers new insights into the function of CIPKs in petal senescence and provides a genetic resource for extending rose vase life.
... During long periods, transgenic rapeseed maintains the high chlorophyll levels, which improves crop yield under water stress conditions (Kant et al., 2015). At the genetic level, plant responses to stresses differ significantly from aging procedures and are associated with accelerated aging process (Guo and Gan, 2011). Leaf senescence caused by environmental stress or intrinsic inheritance can reduce photosynthesis, lead to premature cell death, and cause the supply of anabolites to decrease before flowering, thus negatively regulating the final grain weight (Gregersen et al., 2008). ...
Leaf senescence, the final stage of leaf development, is one of the adaptive mechanisms formed by plants over a long period of evolution. Leaf senescence is accompanied by various changes in cell structure, physiological metabolism, and gene expressions. This process is controlled by a variety of internal and external factors. Meanwhile, the genes and plant hormones involved in leaf aging affect the quality, yield and stress resistance in horticultural plants. Leaf senescence mediated by plant hormones affected plant quality at both pre-harvest and post-harvest stages. Exogenous plant growth regulators or plant hormone inhibitors has been applied to delay leaf senescence. Modification of related gene expression by over-expression or antisense inhibition could delay or accelerate leaf senescence, and thus influence quality. Environmental factors such as light, temperature and water status also trigger or delay leaf senescence. Delaying leaf senescence could increase chloroplast lifespan and photosynthesis and thus improve source strength, leading to enhanced yield. Accelerating leaf senescence promotes nutrient redistribution from old leaves into young leaves, and may raise yield under certain circumstances. Many genes and transcriptional factors involved in leaf senescence are associated with responses to abiotic and biotic stresses. WRKY transcriptional factors play a vital role in this process and they could interact with JA signalling. This review summarized how genes, plant hormones and environmental factors affect the quality, yield. Besides, the regulation of leaf senescence holds great promise to improving the resistance to plant biotic and abiotic stresses.
... In fact, gene expression analyses have shown that several stress-responsive genes, including regulatory genes, are induced during progression of senescence (Breeze et al., 2011;Dong et al., 2021;Li et al., 2021). It is, therefore, believed that the molecular pathways of leaf senescence cross-talk with stress responsive pathways in plants (Guo and Gan, 2012). Our study revealed that several PR genes, conventionally associated with biotic stress, were differentially expressed in senescing coleoptiles, which is consistent with the previous studies where PR protein encoding genes were categorized as SAGs (Barth et al., 2004;Sillanpää et al., 2005). ...
Coleoptile is the small conical, short-lived, sheath-like organ that safeguards the first leaf and shoot apex in cereals. It is also the first leaf-like organ to senesce that provides nutrition to the developing shoot and is, therefore, believed to play a crucial role in seedling establishment in rice and other grasses. Though histochemical studies have helped in understanding the pattern of cell death in senescing rice coleoptiles, genome-wide expression changes during coleoptile senescence have not yet been explored. With an aim to investigate the gene regulation underlying the coleoptile senescence (CS), we performed a combinatorial whole genome expression analysis by sequencing transcriptome and miRNAome of senescing coleoptiles. Transcriptome analysis revealed extensive reprogramming of 3439 genes belonging to several categories, the most prominent of which encoded for transporters, transcription factors (TFs), signaling components, cell wall organization enzymes, redox homeostasis, stress response and hormone metabolism. Small RNA sequencing identified 41 known and 21 novel miRNAs that were differentially expressed during CS. Comparison of gene expression and miRNA profiles generated for CS with publicly available leaf senescence (LS) datasets revealed that the two aging programs are remarkably distinct at molecular level in rice. Integration of expression data of transcriptome and miRNAome identified high confidence 140 miRNA-mRNA pairs forming 42 modules, thereby demonstrating multi-tiered regulation of CS. The present study has generated a comprehensive resource of the molecular networks that enrich our understanding of the fundamental pathways regulating coleoptile senescence in rice.
... One central hallmark of plant senescence is the transcriptomewide reprogramming of gene expressions, including the induction of many senescence-associated genes (SAGs; Breeze et al, 2011;Buchanan-Wollaston et al, 2005;Guo et al, 2004;Guo & Gan, 2012;Guo & Gan, 2014;Kim et al, 2016;Liebsch & Keech, 2016;Lin & Wu, 2004;Woo et al, 2019;Woo et al, 2016). It is evident that a complex array of transcription factors (TFs) are involved in the transcriptional regulation of senescence. ...
One of the hallmarks of plant senescence is the global transcriptional reprogramming coordinated by a plethora of transcription factors (TFs). However, mechanisms underlying the interactions between different TFs in modulating senescence remain obscure. Previously, we discovered that plant ABS3 subfamily MATE transporter genes regulate senescence and senescence-associated transcriptional changes. In a genetic screen for mutants suppressing the accelerated senescence phenotype of the gain-of-function mutant abs3-1D, AUXIN RESPONSE FACTOR 2 (ARF2) and PHYTOCHROME-INTERACTING FACTOR 5 (PIF5) were identified as key TFs responsible for transcriptional regulation in the ABS3-mediated senescence pathway. ARF2 and PIF5 (as well as PIF4) interact directly and function interdependently to promote senescence, and they share common target genes such as key senescence promoting genes ORESARA 1 (ORE1) and STAY-GREEN 1 (SGR1) in the ABS3-mediated senescence pathway. In addition, we discovered reciprocal regulation between ABS3-subfamily MATEs and the ARF2 and PIF5/4 TFs. Taken together, our findings reveal a regulatory paradigm in which the ARF2-PIF5/4 functional module facilitates the transcriptional reprogramming in the ABS3-mediated senescence pathway.
... Leaf senescence is a genetically programmed cell suicide process that is accompanied by mobilization of nutrients released during cell attrition to active growing regions, seeds or trunks (Gan and Amasino, 1997;Guo et al., 2021). The regulation of senescence is rather complex, and it involves activation of thousands of senescence-associated genes (SAGs) and/or inactivation of many senescence-down-regulated genes (Guo et al., 2004;Guo and Gan, 2012). TFs have been shown to have critical roles in regulating SAG expression and leaf senescence. ...
Salicylic acid (SA) is an important plant hormone that regulates defense responses and leaf senescence. It is imperative to understand upstream factors that regulate genes of SA biosynthesis. SAG202/SARD1 is a key regulator for isochorismate synthase 1 (ICS1) induction and SA biosynthesis in defense responses. The regulatory mechanism of SA biosynthesis during leaf senescence is not well understood. Here we show that AtNAP, a senescence-specific NAC family transcription factor, directly regulates a senescence-associated gene named SAG202 as revealed in yeast one-hybrid and in planta assays. Inducible overexpreesion of AtNAP and SAG202 lead to high levels of SA and precocious senescence in leaves. Individual knockout mutants of sag202 and ics1 have markedly reduced SA levels and display a significantly delayed leaf senescence phenotype. Furthermore, SA positively feedback regulates AtNAP and SAG202. Our research has uncovered a unique positive feedback regulatory loop, SA-AtNAP-SAG202-ICS1-SA, that operates to control SA biosynthesis associated with leaf senescence but not defense response.
Supplementary Information
The online version contains supplementary material available at 10.1186/s43897-022-00036-x.
... Senescence phenotypic changes, such as color fading or wilting, are mediated by complex pathways, and the degradation of polymers or nucleic acids and protein biosynthesis can influence these pathways. Thousands of up-or down-regulated structural genes and transcription factors (TFs) have been reported to be implicated in plant senescence (Guo and Gan, 2012;Hong et al., 2013;Yamazaki et al., 2020). ...
Herbaceous peony is an important cut-flower plant cultivated worldwide, but its short vase life substantially restricts its economic value. It is well established that endogenous hormones regulate the senescence process, but their molecular mechanism in flower senescence remains unclear. Here, we isolated a MYB transcription factor gene, PlMYB308, from herbaceous peony flowers, based on transcriptome data. Quantitative real-time PCR analysis showed that PlMYB308 is strongly up-regulated in senescing petals, and its expression was induced by abscisic acid or ethylene and reduced by gibberellin in petals. Treatment with abscisic acid or ethylene accelerated herbaceous peony petal senescence, and gibberellin delayed the process. PlMYB308 silencing delayed peony flower senescence and dramatically increased gibberellin, but reduced ethylene and abscisic acid levels in petals. PlMYB308 ectopic overexpression in tobacco accelerated flower senescence and reduced gibberellin, but increased ethylene and abscisic acid accumulation. Correspondingly, five endogenous hormone biosynthetic genes showed variable expression levels in petals after PlMYB308 silencing or overexpression. A dual-luciferase assay and yeast one-hybrid analysis showed that PlMYB308 specifically binds the PlACO1 promoter. Moreover, treatment with ethylene and 1-MCP can accelerate PlMYB308 silencing-reduced senescence and delay PlMYB308- overexpression-induced senescence. We also found that PlACO1 silencing delayed senescence in herbaceous peony petals. Taken together, our results suggest that the PlMYB308-PlACO1 regulatory checkpoints positively mediate the production of ethylene, and thus contribute to senescence in herbaceous peony flowers.
... Premature senescence caused by environmental stressors can result in significant yield loss and quality reduction. Such stressors include darkness, drought, saline, and alkaline conditions (Guo and Gan, 2012;He et al., 2018;Guo et al., 2021). Saline-alkaline stress is a common abiotic stress that limits plant growth and development, and has become a serious problem restricting crop production as well as ecological environment construction (Zhu, 2016;Wei et al., 2021). ...
In plants, the leaf is an essential photosynthetic organ, and is the primary harvest in forage crops such as alfalfa (Medicago sativa). Premature leaf senescence caused by environmental stress can result in significant yield loss and quality reduction. Therefore, the stay-green trait is important for improving the economic value of forage crops. Alkaline stress can severely damage leaf cells and, consequently, cause leaf senescence. To understand the molecular regulatory mechanisms and identify vital senescence-associated genes under alkaline stress, we used high-throughput sequencing to study transcriptional changes in Medicago truncatula, a model plant for forage crops. We identified 2,165 differentially expressed genes, 985 of which were identical to those in the dark-induced leaf senescence group. Gene ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway enrichment analyses showed that the 985 genes were mainly enriched in nutrient cycling processes such as cellular amino acid metabolic processes and organic substance catabolic processes, indicating nutrient redistribution. The other 1,180 differentially expressed genes were significantly enriched in the oxidoreductase complex, aerobic respiration, and ion transport. Our analysis showed the two gene sets guiding the coupled physiological and biochemical alterations play different roles under alkaline stress with a coordinated and integrated way. Many transcription factor families were identified from these differentially expressed genes, including MYB, WRKY, bHLH, and NAC which have particular preference involved in stress resistance and regulation of senescence. Our results contribute to the exploration of the molecular regulatory mechanisms of leaf senescence in M. truncatula under alkaline stress and provide new candidate genes for future breeding to improve the biomass and quality of forage crops.
... Leaf senescence proceeds with age, but plants must coordinate the timing and speed of leaf senescence by integrating a range of internal and external signals (Buchanan-Wollaston et al., 2003;Woo et al., 2018). It is well documented that leaf senescence is modulated by diverse environmental stresses such as darkness, oxidative stress, salt stress, and drought, as well as by plant hormones such as ethylene, cytokinin, and abscisic acid (ABA) (Breeze et al., 2011;Guo and Gan, 2012). Thus far, intensive studies have been conducted to understand how plants coordinate leaf senescence in response to a repertoire of environmental stresses, yet more questions need to be answered to obtain a clear picture of the interplay between the regulatory programs of leaf senescence This article is protected by copyright. ...
Leaf senescence proceeds with age but is modulated by various environmental
stresses and hormones. Salt stress is one of the most well-known environmental
stresses that accelerate leaf senescence. However, the molecular mechanisms that
integrate salt stress signaling with leaf senescence programs remain elusive. In this
study, we characterized the role of ETHYLENE RESPONSIVE FACTOR34 (ERF34),
an Arabidopsis APETALA2 (AP2)/ERF family transcription factor, in leaf senescence.
ERF34 was differentially expressed under various leaf senescence-inducing
conditions, and negatively regulated leaf senescence induced by age, dark, and salt
stress. ERF34 also promoted salt stress tolerance at different stages of the plant life
cycle such as seed germination and vegetative growth. Transcriptome analysis
revealed that the overexpression of ERF34 increased the transcript levels of salt
stress-responsive genes including COLD-REGULATED15A (COR15A), EARLY
RESPONSIVE TO DEHYDRATION10 (ERD10), and RESPONSIVE TO
DESICCATION29A (RD29A). Moreover, ERF34 directly bound to ERD10 and
RD29A promoters and activated their expression. Our findings indicate that ERF34
plays a key role in the convergence of the salt stress response with the leaf senescence
programs, and is a potential candidate for crop improvement, particularly by
enhancing salt stress tolerance.
... Senescence is an organized process regulated by chlorophyll degradation, photosynthesis decline, lipid peroxidation, and protein deprivation (Smart, 1994). The initiation of leaf senescence is a developmentally programmed and apoptotic process that can be controlled through diverse signals, such as environmental factors (including light, nutrients, temperature, and osmotic stress), pathogen attack, and phytohormones (Lim et al., 2007a;Guo and Gan, 2012;Li et al., 2012). To date, several senescencerelated mutants and a variety of senescence-associated genes (SAGs), which accumulate during leaf senescence, have been isolated and characterized (Buchanan-Wollaston et al., 2003;Lim et al., 2007a;Li et al., 2012). ...
Multiple endogenous and environmental signals regulate the intricate and highly complex processes driving leaf senescence in plants. A number of genes have been identified in a variety of plant species, including Arabidopsis, which influence leaf senescence. Previously, we have shown that HOS15 is a multifunctional protein that regulates several physiological processes, including plant growth and development under adverse environmental conditions. HOS15 has also been reported to form a chromatin remodeling complex with PWR and HDA9 and to regulate the chromatin structure of numerous genes. However, unlike PWR and HDA9, the involvement of HOS15 in leaf senescence is yet to be identified. Here, we report that HOS15, together with PWR and HDA9, promotes leaf senescence via transcriptional regulation of SAG12/29, senescence marker genes, and CAB1/RCBS1A, photosynthesis-related genes. The expression of ORE1, SAG12, and SAG29 was downregulated in hos15-2 plants, whereas the expression of photosynthesis-related genes, CAB1 and RCBS1A, was upregulated. HOS15 also promoted senescence through dark stress, as its mutation led to a much greener phenotype than that of the WT. Phenotypes of double and triple mutants of HOS15 with PWR and HDA9 produced phenotypes similar to those of a single hos15-2. In line with this observation, the expression levels of NPX1, APG9, and WRKY57 were significantly elevated in hos15-2 and hos15/pwr, hos15/hda9, and hos15/pwr/hda9 mutants compared to those in the WT. Surprisingly, the total H3 acetylation level decreased in age-dependent manner and under dark stress in WT; however, it remained the same in hos15-2 plants regardless of dark stress, suggesting that dark-induced deacetylation requires functional HOS15. More interestingly, the promoters of APG9, NPX1, and WRKY57 were hyperacetylated in hos15-2 plants compared to those in WT plants. Our data reveal that HOS15 acts as a positive regulator and works in the same repressor complex with PWR and HDA9 to promote leaf senescence through aging and dark stress by repressing NPX1, APG9, and WRKY57 acetylation.
... In addition, as revealed by genomic, genetic, metabolomic, proteomic, and transcriptomic research, leaf senescence is dynamically regulated by numerous SAGs [37]. Furthermore, several transcription factors, including OsNAP [38], ORE1 [3], AtNAP2 [2,39], and WRKY53 [40], play important roles in regulating chlorophyll degradation-related genes and SAGs. In this study, the overexpression of SlJMJ4 in tomato plants resulted in the upregulated expression of a large number of senescence-related regulatory genes under dark conditions, including chlorophyll degradation-related genes (SlSGR1, SlNYC1, SlPPH, SlPAO, and SlRCCR), transcription factor genes (SlEIN3, SlNOR, SlORE1, SlNAP2, and SlWRKY53) and SAGs (SlSAG12/13/15/101/113) (Fig. 4). ...
Leaf senescence is a highly-programmed developmental process during the plant life cycle. ABA plays an important role in leaf senescence. However, the mechanism underlying ABA-mediated leaf senescence, particularly the upstream epigenetic regulatory network, remains largely unclear. Here, we identified that SlJMJ4, a Jumonji C (jmjC) domain-containing protein in tomato, specifically demethylates di- and tri-methylations of lysine 27 of histone H3 (H3K27) in vitro and in vivo. Overexpression of SlJMJ4 results in premature senescence phenotype and promotes dark- and ABA-induced leaf senescence in tomato. Under dark condition, SlJMJ4-promoted leaf senescence is associated with upregulated expression of transcription factors (SlORE1 and SlNAP2) and senescence-associated genes (SlSAG113, SlSAG12) via removal of H3K27me3. In responses to ABA, overexpression of SlJMJ4 increases its binding at the loci of SlORE1, SlNAP2, SlSAG113, SlSAG12, SlABI5 and SlNCED3 and decreases their H3K27me3 levels, and therefore activates their expression and mediates ABA-induced leaf senescence in tomato. Taken together, these results demonstrate that SlJMJ4 plays a positive role in leaf senescence in tomato and is implicated in ABA-induced leaf senescence by binding to many key genes related to ABA synthesis and signaling, transcription regulation and senescence and hence promoting their H3K27me3 demethylation.
... Similarly, in the present study, we hypothesized that different light regimes might influence the hormonal regulations between the two sides of the maize plant, impacting leaf senescence. For instance, phytohormones like ethylene, abscisic acid (ABA), and salicylic acid (SA) accelerate the senescence process in contrast accumulation of auxin, gibberellin, and cytokinin delay senescence (Guo & GAN, 2012;Jibran et al., 2013). Previously, increased accumulation of some plant hormones such as IAA and GA 3 under slight shading has been reported as growth promotion indicators (Han et al., 2018). ...
As an essential regulator of photosynthesis and hormone signaling, light plays a critical role in leaf senescence and yield gain in crops. Previously, numerous studies have shown that the narrow-wide-row planting pattern, especially under intercropping systems, is more beneficial for crops to enhance light interception, energy conversion, and yield improvement. However, the narrow-wide-row planting pattern inevitably leads to a heterogeneous light environment for crops (i. e., maize in maize-based intercropping systems) on both sides of the plant. The mechanism by which it affects leaf senescence and yield of maize under a narrow-wide-row planting pattern is still unclear. Therefore, in this study, we compared the leaf senescence and yield formation process of maize under homogeneous (normal light, NL and full shade, FS) and heterogeneous (partial light, PL) light conditions. Results revealed that partial light treatment influenced the homeostasis of growth and senescence hormones by regulating the expression of ZmPHYA and ZmPIF5. Compared to normal light and full shade treatments, partial light delayed leaf senescence by 3.6 and 5.9 days with 2.2 and 3.3 more green leaves and 1.1 and 1.4 fold nitrogen uptake, respectively. Partial light reduced oxidative stress by enhancing antioxidant enzyme activities of PS (shade side of partial light) leaves, which improved photosynthetic assimilation, balanced sucrose, and starch ultimately maintaining the similar maize yield to NL. Overall, these results are important for understanding the mechanism of leaf senescence in maize, especially under heterogeneous light environments, which maize experienced in maize-based intercropping systems. Furthermore, these findings are providing proof of getting a high yield of maize with less land in intercropping systems. Thus, we can conclude that maize-based intercropping systems can be used for obtaining high maize yields maintained under the current climate change scenario.
... Prolonged darkness causes phenotypes and transcriptome changes largely resembling those during natural senescence (7,21). Dark-induced senescence (DIS) is therefore used as a simple and efficient system to evaluate the effects of senescence regulators. ...
Significance
Leaf senescence is a critical process in plants and has a direct impact on many important agronomic traits. Despite decades of research, identity of the senescence signal and the molecular mechanism that perceives and transduces the signal remain elusive. Using dark-induced leaf senescence as the experimental system, we found that senescence induces rapid reciprocal regulation of plastocyanin, a copper-binding electron carrier in the photosynthetic electron transport chain, and the PCY-SAG14 pair of phytocyanins located on the endomembrane. We also found that PCY-SAG14, which is modulated by PIF3/4/5 and miR408, is both necessary and sufficient to promote senescence. These findings indicate that intracellular copper homeostasis mediated by the PCY-SAG14 module plays an important regulatory role in dark-induced leaf senescence.
... Plant senescence is the last stage of mature cell development, which aims to degrade cellular components and reuse them (Thomas et al., 2003;Jansson and Thomas, 2008). This stage is first dependent on the age and developmental progress, but is also regulated by diverse environmental factors such as temperature, darkness, pathogen infection, and nutrient deficiencies (Guo and Gan, 2012). In this regard, senescence is important for plants to adapt to different environments and survive under stress (Woo et al., 2019). ...
Senescence in plants is a complex trait, which is controlled by both genetic and environmental factors and can affect the yield and quality of cotton. However, the genetic basis of cotton senescence remains relatively unknown. In this study, we reported genome-wide association studies (GWAS) based on 185 accessions of upland cotton and 26,999 high-quality single-nucleotide polymorphisms (SNPs) to reveal the genetic basis of cotton senescence. To determine cotton senescence, we evaluated eight traits/indices. Our results revealed a high positive correlation (r>0.5) among SPAD value 20 days after topping (SPAD20d), relative difference of SPAD (RSPAD), nodes above white flower on topping day (NAWF0d), nodes above white flower 7 days after topping (NAWF7d), and number of open bolls on the upper four branches (NB), and genetic analysis revealed that all traits had medium or high heritability ranging from 0.53 to 0.86. Based on a multi-locus method (FASTmrMLM), a total of 63 stable and significant quantitative trait nucleotides (QTNs) were detected, which represented 50 genomic regions (GWAS risk loci) associated with cotton senescence. We observed three reliable loci located on chromosomes A02 (A02_105891088_107196428), D03 (D03_37952328_38393621) and D13 (D13_59408561_60730103) because of their high repeatability. One candidate gene (Ghir_D03G011060) was found in the locus D03_37952328_38393621, and its Arabidopsis thaliana homologous gene (AT5G23040) encodes a cell growth defect factor-like protein (CDF1), which might be involved in chlorophyll synthesis and cell death. Moreover, qRT-PCR showed that the transcript level of Ghir_D03G011060 was down-regulated in old cotton leaves, and virus-induced gene silencing (VIGS) indicated that silencing of Ghir_D03G011060 resulted in leaf chlorosis and promoted leaf senescence. In addition, two candidate genes (Ghir_A02G017660 and Ghir_D13G021720) were identified in loci A02_105891088_107196428 and D13_59408561_60730103, respectively. These results provide new insights into the genetic basis of cotton senescence and will serve as an important reference for the development and implementation of strategies to prevent premature senescence in cotton breeding programs.
... The loss of the potential UPP ubiquitin receptor RPN10 significantly delays senescence (Lin et al., 2011), and overexpression of RPN5a leads to premature senescence (Book et al., 2009). In contrast to the overall up-regulation of ATG genes, transcript levels of only a small part of the proteasome subunit genes were increased during leaf senescence (Guo and Gan, 2012). In the senescent leaf of rape and barley (Hordeum vulgare L.), the proteasome is very active (Poret et al., 2016;Velasco-Arroyo et al., 2016). ...
Leaf senescence is the last stage of leaf development and is an orderly biological process accompanied by degradation of macromolecules and nutrient recycling, which contributes to plant fitness. Forward genetic mutant screening and reverse genetic studies of senescence-associated genes (SAGs) have revealed that leaf senescence is a genetically regulated process, and the initiation and progression of leaf senescence are influenced by an array of internal and external factors. Recently, multi-omics techniques have revealed that leaf senescence is subjected to multiple layers of regulation, including chromatin, transcriptional and post-transcriptional, as well as translational and post-translational levels. Although impressive progress has been made in plant senescence research, especially the identification and functional analysis of a large number of SAGs in crop plants, we still have not unraveled the mystery of plant senescence, and there are some urgent scientific questions in this field, such as when plant senescence is initiated and how senescence signals are transmitted. This paper reviews recent advances in the multiple layers of regulation on leaf senescence, especially in post-transcriptional regulation such as alternative splicing.
... Plant senescence occurs under various conditions, such as reduced light availability, nutrition deficiency, abiotic stress and developmental change (Lim et al. 2007, Guo and Gan 2012, Liebsch and Keech 2016, Zhuo et al. 2020, and could be classified into natural senescence (i.e. age-dependent), starvationinduced senescence (e.g. ...
Introduction
Jasmonate (JA)-induced plant senescence has been mainly studied with a dark/starvation-promoted system using detached leaves; yet, the induction of whole-plant senescence by JA remains largely unclear. This work reports the finding of a JA-induced whole-plant senescence of tobacco under light/non-starvation conditions and the investigation of underlying regulations. Methyl jasmonate (MeJA) treatment induces the whole-plant senescence of tobacco in a light-intensity–dependent manner, which is suppressed by silencing of NtCOI1 that encodes the receptor protein of JA-Ile (the bioactive derivative of JA). MeJA treatment could induce the senescence-specific cysteine protease gene SAG12 and another cysteine protease gene SAG-L1 to high expression levels in the detached leaf patches under dark conditions but failed to induce their expression in tobacco whole plants under light conditions. Furthermore, MeJA attenuates the RuBisCo activase (RCA) level in the detached leaves but has no effect on this protein in the whole plant under light conditions. A genome-wide transcriptional assay also supports the presence of a differential regulatory pattern of senescence-related genes during MeJA-induced whole-plant senescence under non-starvation conditions and results in the finding of a chlorophylase activity increase in this process. We also observed that the MeJA-induced senescence of tobacco whole plants is reversible, which is accompanied by a structural change of chloroplasts. This work provides novel insights into JA-induced plant senescence under non-starvation conditions and is helpful to dissect the JA-synchronized process of whole-plant senescence.
Bamboo cultivation, particularly Moso bamboo ( Phyllostachys edulis ), holds significant economic importance in various regions worldwide. Bamboo shoot degradation (BSD) severely affects productivity and economic viability. However, despite its agricultural consequences, the molecular mechanisms underlying BSD remain unclear. Consequently, we explored the dynamic changes of BSD through anatomy, physiology and the transcriptome. Our findings reveal ruptured protoxylem cells, reduced cell wall thickness and the accumulation of sucrose and reactive oxygen species (ROS) during BSD. Transcriptomic analysis underscored the importance of genes related to plant hormone signal transduction, sugar metabolism and ROS homoeostasis in this process. Furthermore, BSD appears to be driven by the coexpression regulatory network of senescence‐associated gene transcription factors (SAG‐TFs), specifically PeSAG39 , PeWRKY22 and PeWRKY75 , primarily located in the protoxylem of vascular bundles. Yeast one‐hybrid and dual‐luciferase assays demonstrated that PeWRKY22 and PeWRKY75 activate PeSAG39 expression by binding to its promoter. This study advanced our understanding of the molecular regulatory mechanisms governing BSD, offering a valuable reference for enhancing Moso bamboo forest productivity.
Phosphorus (P) is a crucial macronutrient for plant growth, development, and reproduction. The effects of low P (LP) stress on leaf senescence and the role of PHR1 in LP‐induced leaf senescence are still unknown. Here, we report that PHR1 plays a crucial role in LP‐induced leaf senescence, showing delayed leaf senescence in phr1 mutant and accelerated leaf senescence in 35S:PHR1 transgenic Arabidopsis under LP stress. The transcriptional profiles indicate that 763 differentially expressed SAGs (DE‐SAGs) were upregulated and 134 DE‐SAGs were downregulated by LP stress. Of the 405 DE‐SAGs regulated by PHR1, 27 DE‐SAGs were involved in P metabolism and transport. PHR1 could bind to the promoters of six DE‐SAGs ( RNS1 , PAP17 , SAG113 , NPC5 , PLDζ2 , and Pht1;5 ), and modulate them in LP‐induced senescing leaves. The analysis of RNA content, phospholipase activity, acid phosphatase activity, total P and phosphate content also revealed that PHR1 promotes P liberation from senescing leaves and transport to young tissues under LP stress. Our results indicated that PHR1 is one of the crucial modulators for P recycling and redistribution under LP stress, and the drastic decline of P level is at least one of the causes of early senescence in P‐deficient leaves.
Leaf growth initiates in the peripheral region of the meristem at the apex of the stem, eventually forming flat structures. Leaves are pivotal organs in plants, serving as the primary sites for photosynthesis, respiration, and transpiration. Their development is intricately governed by complex regulatory networks. Leaf development encompasses five processes: the leaf primordium initiation, the leaf polarity establishment, leaf size expansion, shaping of leaf, and leaf senescence. The leaf primordia starts from the side of the growth cone at the apex of the stem. Under the precise regulation of a series of genes, the leaf primordia establishes adaxial-abaxial axes, proximal-distal axes and medio-lateral axes polarity, guides the primordia cells to divide and differentiate in a specific direction, and finally develops into leaves of a certain shape and size. Leaf senescence is a kind of programmed cell death that occurs in plants, and as it is the last stage of leaf development. Each of these processes is meticulously coordinated through the intricate interplay among transcriptional regulatory factors, microRNAs, and plant hormones. This review is dedicated to examining the regulatory influences of major regulatory factors and plant hormones on these five developmental aspects of leaves.
In plants, leaf senescence is regulated by several factors, including age and carbon starvation. The molecular mechanism of age-regulated developmental leaf senescence differs from that of carbon starvation-induced senescence. Salicylic acid (SA) and Nonexpressor of pathogenesis-related genes 1 (NPR1) play important roles in promoting developmental leaf senescence. However, the relationship between SA signaling and carbon starvation-induced leaf senescence is not currently well understood. Here, we used Arabidopsis thaliana as material and found that carbon starvation-induced leaf senescence was accelerated in the SA dihydroxylase mutants s3hs5h compared to the Columbia ecotype (Col). Exogenous SA treatment significantly promoted carbon starvation-induced leaf senescence, especially in NPR1-GFP. Increasing the endogenous SA and overexpression of NPR1 inhibited carbon starvation-induced autophagy. However, mutation of NPR1 delayed carbon starvation-induced leaf senescence, increased autophagosome production and accelerated autophagic degradation of the Neighbor of BRCA1 gene 1 (NBR1). In conclusion, SA promotes carbon starvation-induced leaf senescence by inhibiting autophagy via NPR1.
Flower senescence is genetically regulated and developmentally controlled. The phytohormone ethylene induces flower senescence in rose (Rosa hybrida), but the underlying signaling network is not well understood. Given that calcium regulates senescence in animals and plants, we explored the role of calcium in petal senescence. Here, we report that the expression of calcineurin B-like protein 4 (RhCBL4), which encodes a calcium receptor, is induced by senescence and ethylene signaling in rose petals. RhCBL4 interacts with CBL-interacting protein kinase 3 (RhCIPK3), and both positively regulate petal senescence. Furthermore, we determined that RhCIPK3 interacts with the jasmonic acid response repressor jasmonate ZIM-domain 5 (RhJAZ5). RhCIPK3 phosphorylates RhJAZ5 and promotes its degradation in the presence of ethylene. Our results reveal that the RhCBL4-RhCIPK3-RhJAZ5 module mediates ethylene-regulated petal senescence. These findings provide insights into flower senescence, which may facilitate innovations in postharvest technology for extending rose flower longevity.
Drought stress inducing pollen sterility can reduce crop yield worldwide. The regulatory crosstalk associated with the effects of drought on pollen formation at the cellular level has not been explored in detail so far. In this study, we performed morphological and cytoembryological analysis of anther perturbations and examined pollen development in two spring barley genotypes that differ in earliness and drought tolerance. The Syrian breeding line CamB (drought-tolerant) and the European cultivar Lubuski (drought-sensitive) were used as experimental materials to analyze the drought-induced changes in yield performance, chlorophyll fluorescence kinetics, the pollen grain micromorphology and ultrastructure during critical stages of plant development. In addition, fluctuations in HvGAMYB expression were studied, as this transcription factor is closely associated with the development of the anther. In the experiments, the studied plants were affected by drought, as was confirmed by the analyses of yield performance and chlorophyll fluorescence kinetics. However, contrary to our expectations, the pollen development of plants grown under specific conditions was not severely affected. The results also suggest that growth modification, as well as the perturbation in light distribution, can affect the HvGAMYB expression. This study demonstrated that the duration of the vegetation period can influence plant drought responses and, as a consequence, the processes associated with pollen development as every growth modification changes the dynamics of drought effects as well as the duration of plant exposition to drought.
The papain-like cysteine proteases (PLCPs) family contains many proteolytic enzymes involved in plant growth and development, leaf senescence, immunity, and stress responses. However, little is known about these enzymes in pepper. We identified 35 PLCPs, which were divided into nine subfamilies based on evolution phylogeny, including four RD21 (responsive to desiccation 21), two CEP (cysteine endopeptidase), two XCP (xylem cysteine peptidase), three XBCP3 (xylem bark cysteine peptidase 3), one THI, ten SAG12 (senescence-associated gene 12), three RD19 (responsive to desiccation 19), one ALP (aleurain-like protease) and eight CTB (cathepsin B-like). The identities of PLCPs were revealed by analyzing conserved motifs, domains and gene structures. An analysis of the putative promoter regions (2 kb upstream regions of the start codon) revealed the enrichment of plant growth, environmental stress and phytohormone signaling cis-elements. Expression profiling revealed diverse patterns of CaPLCPs family members over various tissues. Transcriptional profiling showed a distinct pattern of expression under abiotic stress. Silencing CaCP34 promoted leaf senescence induced by salt and osmotic stress. In contrast, CaCP34 overexpression enhanced the tolerance of pepper to leaf senescence induced by salt and osmotic stress. Taken together, these results demonstrate that the CaPLCPs have various roles in developmental senescence and resistance in pepper.
NAC proteins constitute one of the largest transcription factor families and are involved in regulation of plant development and stress responses. Our previous transcriptome analyses of tobacco revealed a significant increase in the expression of NtNAC028 during leaf yellowing. In this study, we found that NtNAC028 was rapidly upregulated in response to high salinity, dehydration, and abscisic acid (ABA) stresses, suggesting a vital role of this gene in abiotic stress response. NtNAC028 loss-of-function tobacco plants generated via CRISPR-Cas9 showed delayed leaf senescence and increased tolerance to drought and salt stresses. Meanwhile NtNAC028 overexpression led to precocious leaf senescence and hypersensitivity to abiotic stresses in Arabidopsis, indicating that NtNAC028 functions as a positive regulator of natural leaf senescence and a negative regulator of stress tolerance. Furthermore, NtNAC028-overexpressing Arabidopsis plants showed lower antioxidant enzyme activities, higher reactive oxygen species (ROS), and H2O2 accumulation under high salinity, resulted in more severe oxidative damage after salt stress treatments. On the other hand, NtNAC028 mutation in tobacco resulted in upregulated expression of ROS-scavenging and abiotic stress-related genes, higher antioxidant enzyme activities, and enhanced tolerance against abiotic stresses, suggesting that NtNAC028 might act as a vital regulator for plant stress response likely by mediating ROS scavenging ability. Collectively, our results indicated that the NtNAC028 plays a key regulatory role in leaf senescence and response to multiple abiotic stresses.
Incident light is a central modulator of plant growth and development. However, there are still open questions surrounding wavelength-specific plant proteomic responses. Here we applied tandem mass tag based quantitative proteomics technology to acquire an in-depth view of proteome changes in Arabidopsis thaliana response to narrow wavelength blue (B; 450 nm), amber (A; 595 nm), or red (R; 650 nm) light treatments. A total of 16,707 proteins were identified with 9120 proteins quantified across all three light treatments in three biological replicates. This enabled examination of changes in the abundance for proteins with low abundance and important regulatory roles including transcription factors and hormone signaling. Importantly, 18% (1631 proteins) of the A. thaliana proteome is differentially abundant in response to narrow wavelength lights, and changes in proteome correlate well with different morphologies exhibited by plants. To showcase the usefulness of this resource, data were placed in the context of more than thirty published datasets, providing orthogonal validation and further insights into light-specific biological pathways, including Systemic Acquired Resistance and Shade Avoidance Syndrome. This high-resolution resource for A. thaliana provides baseline data and a tool for defining molecular mechanisms that control fundamental aspects of plant response to changing light conditions, with implications in plant development and adaptation.
Significance
Understanding of molecular mechanisms involved in wavelength-specific response of plant is question of widespread interest both to basic researchers and to those interested in applying such knowledge to the engineering of novel proteins, as well as targeted lighting systems. Here we sought to generate a high-resolution labeling proteomic profile of plant leaves, based on exposure to specific narrow-wavelength lights. Although changes in plant physiology in response to light spectral composition is well documented, there is limited knowledge on the roles of specific light wavelengths and their impact. Most previous studies have utilized relatively broad wavebands in their experiments. These multi-wavelengths lights function in a complex signaling network, which provide major challenges in inference of wavelength-specific molecular processes that underly the plant response. Besides, most studies have compared the effect of blue and red wavelengths comparing with FL, as control. As FL light consists the mixed spectra composition of both red and blue as well as numerous other wavelengths, comparing undeniably results in inconsistent and overlapping responses that will hamper effects to elucidate the plant response to specific wavelengths [1, 2]. Monitoring plant proteome response to specific wavelengths and further compare the changes to one another, rather than comparing plants proteome to FL, is thus necessary to gain the clear insights to specific underlying biological pathways and their effect consequences in plant response. Here, we employed narrow wavelength LED lights in our design to eliminate the potential overlap in molecular responses by ensuring non-overlapping wavelengths in the light treatments. We further applied TMT-labeling technology to gain a high-resolution view on the associates of proteome changes. Our proteomics data provides an in-depth coverage suitable for system-wide analyses, providing deep insights on plant physiological processes particularly because of the tremendous increase in the amount of identified proteins which outreach the other biological data.
Melatonin (MT) functions in removing reactive oxygen species (ROS) and delaying plant senescence, thereby acting as an antioxidant; however, the molecular mechanism underlying the specific action of MT is unclear. Here in, we used the mutant plants carrying the MT decomposition gene melatonin 3‐hydroxylase (SlM3H) in tomato to elucidate the specific mechanism of action of MT. SlM3H‐OE accelerated senescence by decreasing the content of endogenous MT in plants. SlM3H is a senescence‐related gene that positively regulates aging. MT inhibited the expression of the senescence‐related gene SlCV to scavenge ROS, induced stable chloroplast structure, and delayed leaf senescence. Simultaneously, MT weakened the interaction between SlCV and SlPsbO/SlCAT3, reduced ROS production in photosystem II (PS II), and promoted ROS elimination. In conclusion, MT regulates ROS homeostasis and delays leaf aging in tomato plants through SlCV expression modulation. This article is protected by copyright. All rights reserved.
In annual plants, tight coordination of successive developmental events is of primary importance to optimize performance under fluctuating environmental conditions. The recent finding of the genetic interaction of WRKY53 , a key senescence-related gene with REVOLUTA , a master regulator of early leaf patterning, raises the question of how early and late developmental events are connected. Here, we investigated the developmental and metabolic consequences of an alteration of the REVOLUTA and WRKY53 gene expression, from seedling to fruiting . Our results show that REVOLUTA critically controls late developmental phases and reproduction while inversely WRKY53 determines vegetative growth at early developmental stages. We further show that these regulators of distinct developmental phases frequently, but not continuously, interact throughout ontogeny and demonstrated that their genetic interaction is mediated by the salicylic acid (SA). Moreover, we showed that REVOLUTA and WRKY53 are keys regulatory nodes of development and plant immunity thought their role in SA metabolic pathways, which also highlights the role of REV in pathogen defence. Together, our findings demonstrate how late and early developmental events are tightly intertwined by molecular hubs. These hubs interact with each other throughout ontogeny, and participate to the interplay between plant development and immunity.
Leaf senescence is a pivotal progress in the last stage of plant life cycle and influenced by various external and endogenous cues. A series of reports have indicated the involvement of WRKY transcription factor in regulating leaf senescence, whereas the molecular mechanisms and signaling pathways remain largely unclear. Here, we provide evidence demonstrating that WRKY71 acts as a positive regulator of leaf senescence in Arabidopsis. WRKY71-1D, an over-expressor of WRKY71, exhibited early leaf senescence, while wrky71-1, the WRKY71 loss-of-function mutant, displayed delayed leaf senescence. Accordingly, a set of senescence-associated genes (SAGs) were substantially elevated in WRKY71-1D but markedly decreased in wrky71-1. Chromatin immunoprecipitation assay indicated that WRKY71 can directly bind to the promoters of SAG13 and SAG201. Transcriptome analysis suggested that WRKY71 might mediate multiple cues to accelerate leaf senescence, such as abiotic stresses, dark and ethylene. WRKY71 was ethylene inducible, and the ethylene precursor ACC treatment enhanced the leaf senescence of WRKY71-1D, but caused only a marginal delay in the leaf senescence of wrky71-1. In vitro and in vivo assays demonstrated that WRKY71 can directly regulate ETHYLENE INSENSITIVE2 (EIN2) and ORESARA1 (ORE1), genes of ethylene signaling pathway. Consistently, leaf senescence of WRKY71-1D was obviously retarded in the ein2-5 and nac2-1 mutants. Moreover, WRKY71 was also proved to interact with ACS2 in vitro and in vivo. AgNO3 and aminoethoxyvinylglycine (AVG) treatment, and acs2-1 could greatly arrest the leaf senescence of WRKY71-1D. In conclusion, our data revealed that WRKY71 mediates ethylene signaling and synthesis to hasten leaf senescence in Arabidopsis.
In the present study, we evaluate the protective effect of nitric oxide (NO) against the senescence of rice leaves promoted by hydrogen peroxide (H 2O2). Senescence of rice leaves was determined by decreases in protein content. H2O2 treatment resulted in (1) increases in leaf H2O2 content, (2) induction of leaf senescence, (3) increases in lipid peroxidation, (4) decreases in ascorbic acid (AsA) and reduced form glutathione (GSH) contents, and (5) increases in antioxidative enzyme activities (ascorbate peroxidase, glutathione reductase, and peroxidase). NO donors [N-tert-butyl-α-phenylnitrone (PBN), sodium nitroprusside, 3-morpholinosydonimine, and AsA + NaNO2] were effective in reducing H2O2-induced leaf senescence. PBN prevented H2O2-increased H2O2 content, H2O2-induced lipid peroxidation, H 2O2-decreased AsA and GSH contents, and H 2O2-increased antioxidative enzyme activities. The protective effect of PBN on H2O2-promoted senescence, H2O2-increased H2O2 content and lipid peroxidation, H2O2-decreased AsA and GSH contents, and H2O2-increased antioxidative enzyme activities was reversed by 2-(4-carboxy-2-phenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3- oxide, a NO-specific scavenger, suggesting that the protective effect of PBN is attributable to the NO released. Reduction of H2O2-induced senescence by NO in rice leaves is most likely mediated through its ability to scavenge H2O2.
Drought is one of the major factors limiting the yield of wheat (Triticum aestivum L.) particularly during grain filling. Under terminal drought condition, remobilization of pre-stored carbohydrates in wheat stem to grain has a major contribution in yield. To determine the molecular mechanism of stem reserve utilization under drought condition, we compared stem proteome patterns of two contrasting wheat landraces (N49 and N14) under a progressive post-anthesis drought stress, during which period N49 peduncle showed remarkably higher stem reserves remobilization efficiency compared to N14. Out of 830 protein spots reproducibly detected and analyzed on two-dimensional electrophoresis gels, 135 spots showed significant changes in at least one landrace. The highest number of differentially expressed proteins was observed in landrace N49 at 20days after anthesis when active remobilization of dry matter was observed, suggesting a possible involvement of these proteins in effective stem reserve remobilization of N49. The identification of 82 of differentially expressed proteins using mass spectrometry revealed a coordinated expression of proteins involved in leaf senescence, oxidative stress defense, signal transduction, metabolisms and photosynthesis which might enable N49 to efficiently remobilized its stem reserves compared to N14. The up-regulation of several senescence-associated proteins and breakdown of photosynthetic proteins in N49 might reflect the fact that N49 increased carbon remobilization from the stem to the grains by enhancing senescence. Furthermore, the up-regulation of several oxidative stress defense proteins in N49 might suggest a more effective protection against oxidative stress during senescence in order to protect stem cells from premature cell death. Our results suggest that wheat plant might response to soil drying by efficiently remobilize assimilates from stem to grain through coordinated gene expression.
Leaf senescence is an essential developmental process that impacts dramatically on crop yields and involves altered regulation of thousands of genes and many metabolic and signaling pathways, resulting in major changes in the leaf. The regulation of senescence is complex, and although senescence regulatory genes have been characterized, there is little information on how these function in the global control of the process. We used microarray analysis to obtain a high-resolution time-course profile of gene expression during development of a single leaf over a 3-week period to senescence. A complex experimental design approach and a combination of methods were used to extract high-quality replicated data and to identify differentially expressed genes. The multiple time points enable the use of highly informative clustering to reveal distinct time points at which signaling and metabolic pathways change. Analysis of motif enrichment, as well as comparison of transcription factor (TF) families showing altered expression over the time course, identify clear groups of TFs active at different stages of leaf development and senescence. These data enable connection of metabolic processes, signaling pathways, and specific TF activity, which will underpin the development of network models to elucidate the process of senescence.
Arabidopsis WRKY proteins are plant-specific transcription factors, encoded by a large gene family, which contain the highly conserved amino acid sequence WRKYGQK and the zinc-finger-like motifs, Cys(2)His(2) or Cys(2)HisCys. They can recognize and bind the TTGAC(C/T) W-box ciselements found in the promoters of target genes, and are involved in the regulation of gene expression during pathogen defense, wounding, trichome development, and senescence. Here we investigated the physiological function of the Arabidopsis WRKY22 transcription factor during dark-induced senescence. WRKY22 transcription was suppressed by light and promoted by darkness. In addition, AtWRKY22 expression was markedly induced by H(2)O(2). These results indicated that AtWRKY22 was involved in signal pathways in response to abiotic stress. Dark-treated AtWRKY22 over-expression and knockout lines showed accelerated and delayed senescence phenotypes, respectively, and senescence-associated genes exhibited increased and decreased expression levels. Mutual regulation existed between AtWRKY22 and AtWRKY6, AtWRKY53, and AtWRKY70, respectively. Moreover, AtWRKY22 could influence their relative expression levels by feedback regulation or by other, as yet unknown mechanisms in response to dark. These results prove that AtWRKY22 participates in the dark-induced senescence signal transduction pathway.
Leaf senescence, as the last stage of leaf development, is regulated by diverse developmental and environmental factors. Jasmonates (JAs) have been shown to induce leaf senescence in several plant species; however, the molecular mechanism for JA-induced leaf senescence remains unknown. In this study, proteomic, genetic, and physiological approaches were used to reveal the molecular basis of JA-induced leaf senescence in Arabidopsis (Arabidopsis thaliana). We identified 35 coronatine-insensitive 1 (COI1)-dependent JA-regulated proteins using two-dimensional difference gel electrophoresis in Arabidopsis. Among these 35 proteins, Rubisco activase (RCA) was a COI1-dependent JA-repressed protein. We found that RCA was down-regulated at the levels of transcript and protein abundance by JA in a COI1-dependent manner. We further found that loss of RCA led to typical senescence-associated features and that the COI1-dependent JA repression of RCA played an important role in JA-induced leaf senescence.
Factors that influence the longevity and senescence of photosynthetic tissues of Arabidopsis were investigated. To determine the influence of reproductive development on the timing of somatic tissue senescence, the longevity of rosette leaves of the Landsberg erecta strain and of isogenic mutant lines in which flowering is delayed (co-2) or sterile flowers are produced (ms1-1) were compared. No difference in the timing of senescence of individual leaves was observed between these lines, indicating that somatic tissue longevity is not governed by reproductive development in this species. To examine the role of differential gene expression in the process of leaf senescence, cDNA clones representing genes that are differentially expressed in senescing tissues were isolated. Sequence analysis of one such clone indicated homology to previously cloned cysteine proteinases, which is consistent with a role for the product of this gene in nitrogen salvage. RNA gel blot analysis revealed that increased expression of senescence-associated genes is preceded by declines in photosynthesis and in the expression of photosynthesis-associated genes. A model is presented in which it is postulated that leaf senescence is triggered by age-related declines in photosynthetic processes.
Disease resistance is associated with a plant defense response that involves an integrated set of signal transduction pathways. Changes in the expression patterns of 2,375 selected genes were examined simultaneously by cDNA microarray analysis in Arabidopsis thaliana after inoculation with an incompatible fungal pathogen Alternaria brassicicola or treatment with the defense-related signaling molecules salicylic acid (SA), methyl jasmonate (MJ), or ethylene. Substantial changes (up- and down-regulation) in the steady-state abundance of 705 mRNAs were observed in response to one or more of the treatments, including known and putative defense-related genes and 106 genes with no previously described function or homology. In leaf tissue inoculated with A. brassicicola, the abundance of 168 mRNAs was increased more than 2.5-fold, whereas that of 39 mRNAs was reduced. Similarly, the abundance of 192, 221, and 55 mRNAs was highly (>2.5-fold) increased after treatment with SA, MJ, and ethylene, respectively. Data analysis revealed a surprising level of coordinated defense responses, including 169 mRNAs regulated by multiple treatments/defense pathways. The largest number of genes coinduced (one of four induced genes) and corepressed was found after treatments with SA and MJ. In addition, 50% of the genes induced by ethylene treatment were also induced by MJ treatment. These results indicated the existence of a substantial network of regulatory interactions and coordination occurring during plant defense among the different defense signaling pathways, notably between the salicylate and jasmonate pathways that were previously thought to act in an antagonistic fashion.
Like most monocarpic plants, longevity of Arabidopsis thaliana plants is controlled by the reproductive structures; however, they appear to work differently from most dicots studied. Neither male- and female-sterility mutations (ms1-1 and bell1, respectively) nor surgical removal of the stems with inflorescences (bolts) at various stages significantly increased the longevity of individual rosette leaves, yet the mutants and treated plants lived 20-50 d longer, measured by the death of the last rosette and/or the last cauline leaf. A series of growth mutations (clv2-4, clv3-2, det3, vam1 enh, and dark green) also increased plant longevity by 20-30 d but did not delay the overall development of the plants. The mutations prolonged plant life through the production of new leaves and stems with inflorescences (bolts) rather than by extending leaf longevity. In growing stems, the newly-formed leaves may induce senescence in the older leaves; however, removal of the younger leaves did not significantly increase the life of the older leaves on the compressed stems of Arabidopsis. Since plants that produce more bolts also live longer, the reproductive load (dry weight) of the bolts did not seem to drive leaf or whole plant senescence here. The developing reproductive structures caused the death of the plant by preventing regeneration of leaves and bolts, which are green and presumably photosynthetic. They also exerted a correlative control (repression) on the development of additional reproductive structures.
We have compared the time course of leaf senescence in pea (Pisum sativum L. cv Messire) plants subjected to a mild water deficit to that of monocarpic senescence in leaves of three different ages in well-watered plants and to that of plants in which leaf senescence was delayed by flower excision. The mild water deficit (with photosynthesis rate maintained at appreciable levels) sped up senescence by 15 d (200°Cd), whereas flower excision delayed it by 17 d (270°Cd) compared with leaves of the same age in well-watered plants. The range of life spans in leaves of different ages in control plants was 25 d (340°Cd). In all cases, the first detected event was an increase in the mRNA encoding a cysteine-proteinase homologous to Arabidopsis SAG2. This happened while the photosynthesis rate and the chlorophyll and protein contents were still high. The 2-fold variability in life span of the studied leaves was closely linked to the duration from leaf unfolding to the beginning of accumulation of this mRNA. In contrast, the duration of the subsequent phases was essentially conserved in all studied cases, except in plants with excised flowers, where the degradation processes were slower. These results suggest that senescence in water-deficient plants was triggered by an early signal occurring while leaf photosynthesis was still active, followed by a program similar to that of monocarpic senescence. They also suggest that reproductive development plays a crucial role in the triggering of senescence.
A homozygous, dominant, C2H4-resistant line of Arabidopsis thaliana (L.) Heynh (cv. Columbia; er) was selected from ethylmethylsulfonate-mutagenized seed, and used to test the role of C2H4 and other growth regulators in senescence of mature leaves. Chlorophyll (Chl) loss from disks excised from leaves of er was much slower than that from wild-type (WT) disks, whether they were held in the light or in the dark. C2H4 accelerated Chl loss from WT disks but had no effect on the yellowing of mutant disks. C2H4 biosynthesis was higher in disks from the mutant plants, particularly in the light. In the dark, treatment with the cytokinin, 6-benzyladenine (BA), reduced Chl loss from wild-type disks, but had no effect on mutant disks. In the light, BA treatment stimulated chlorophyll breakdown in both wild type and mutant disks. Treatment with abscisic acid (ABA) stimulated chlorophyll loss in wild-type and mutant disks, whether they were held in the light or the dark. C2H4 production was stimulated in ABA-treated disks, but they still yellowed even when C2H4 production was inhibited by application of aminooxyacetic acid (AOA). These data indicate that C2H4 is only one of the factors involved in leaf senescence, and that the promotion of senescence by ABA is not mediated through its stimulation of C2H4 production.
The expression patterns of senescence-related genes were determined during ozone (O3) exposure in Arabidopsis. Rosettes were treated with 0.15 μL L⁻¹ O3 for 6 h d⁻¹ for 14 d. O3-treated leaves began to yellow after 10 d of exposure, whereas yellowing was not apparent in control leaves until d 14. Transcript levels for eight of 12 senescence related genes characterized showed induction by O3. SAG13(senescence-associated gene), SAG21, ERD1(early responsive to dehydration), and BCB (blue copper-binding protein) were induced within 2 to 4 d of O3 treatment; SAG18, SAG20, and ACS6 (ACC synthase) were induced within 4 to 6 d; and CCH (copper chaperone) was induced within 6 to 8 d. In contrast, levels of photosynthetic gene transcripts,rbcS (small subunit of Rubisco) and cab(chlorophyll a/b-binding protein), declined after 6 d. Other markers of natural senescence, SAG12,SAG19, MT1 (metallothionein), andAtgsr2 (glutamine synthetase), did not show enhanced transcript accumulation. When SAG12promoter-GUS (β-glucuronidase) andSAG13 promoter-GUS transgenic plants were treated with O3, GUS activity was induced in SAG13-GUS plants after 2 d but was not detected in SAG12-GUS plants.SAG13 promoter-driven GUS activity was located throughout O3-treated leaves, whereas control leaves generally showed activity along the margins. The acceleration of leaf senescence induced by O3 is a regulated event involving many genes associated with natural senescence.
Numerous studies have shown that transcription factors are important in regulating plant responses to environmental stress. However, specific functions for most of the genes encoding transcription factors are unclear. In this study, we used mRNA profiles generated from microarray experiments to deduce the functions of genes encoding known and putative Arabidopsis transcription factors. The mRNA levels of 402 distinct transcription factor genes were examined at different developmental stages and under various stress conditions. Transcription factors potentially controlling downstream gene expression in stress signal transduction pathways were identified by observed activation and repression of the genes after certain stress treatments. The mRNA levels of a number of previously characterized transcription factor genes were changed significantly in connection with other regulatory pathways, suggesting their multifunctional nature. The expression of 74 transcription factor genes responsive to bacterial pathogen infection was reduced or abolished in mutants that have defects in salicylic acid, jasmonic acid, or ethylene signaling. This observation indicates that the regulation of these genes is mediated at least partly by these plant hormones and suggests that the transcription factor genes are involved in the regulation of additional downstream responses mediated by these hormones. Among the 43 transcription factor genes that are induced during senescence, 28 of them also are induced by stress treatment, suggesting extensive overlap responses to these stresses. Statistical analysis of the promoter regions of the genes responsive to cold stress indicated unambiguous enrichment of known conserved transcription factor binding sites for the responses. A highly conserved novel promoter motif was identified in genes responding to a broad set of pathogen infection treatments. This observation strongly suggests that the corresponding transcription factors play general and crucial roles in the coordinated regulation of these specific regulons. Although further validation is needed, these correlative results provide a vast amount of information that can guide hypothesis-driven research to elucidate the molecular mechanisms involved in transcriptional regulation and signaling networks in plants.
In their Perspective, Lithgow and Kirkwood postulate that evolutionary theory predicts that the process of aging is not subject
to selection in the same way as other physiological processes such as development. They then describe the genetics of aging
in the worm Caenorhabditis elegans and how what we know about the functions of the genes that have been identified as controlling life-span support this notion.
A homozygous, dominant, C2H4-resistant line of Arabidopsis thaliana (L.) Heynh (cv. Columbia; er) was selected from ethylmethylsulfonate-mutagenized seed, and used to test the role of C2H4 and other growth regulators in senescence of mature leaves. Chlorophyll (Chl) loss from disks excised from leaves of er was much slower than that from wild-type (WT) disks, whether they were held in the light or in the dark. C2H4 accelerated Che loss from WT disks but had no effect on the yellowing of mutant disks. C2H4 biosynthesis was higher in disks from the mutant plants, particularly in the light. In the dark, treatment with the cytokinin, 6-benzyladenine (BA), reduced Chl loss from wild-type disks, but had no effect on mutant disks. In the light, BA treatment stimulated chlorophyll breakdown in both wild type and mutant disks. Treatment with abscisic acid (ABA) stimulated chlorophyll loss in wild-type and mutant disks, whether they were held in the light or the dark. C2H4 production was stimulated in ABA-treated disks, but they still yellowed even when C2H4 production was inhibited by application of aminooxyacetic acid (AOA). These data indicate that C2H4 is only one of the factors involved in leaf senescence, and that the promotion of senescence by ABA is not mediated through its stimulation of C2H4 production.
O3 significantly reduces photosynthesis, growth, and yield and causes foliar injury and senescence. Here, integrated transcriptomics, proteomics and metabolomics approaches were applied to investigate the molecular responses of O3 in the leaves of 2-week-old rice seedlings exposed to 0.2 ppm O3 for a period of 24 h. Transcript profiling of rice genes was performed in leaves exposed for 1, 12, and 24 h using rice DNA microarray chip. This systematic survey showed that O3 triggers a chain reaction of altered gene, protein and metabolite expressions involved in multiple cellular processes in rice.
Chlorophyll degradation in Cucumis leaf discs was measured at different temperatures between 1 and 25°C in the light and in darkness, and in the presence or absence of sucrose. Two different processes of chlorophyll degradation could be distinguished, a light-requiring process operating at 1 and 5°C and another, light and sucrose enhanced degradation process which was evident at 25°C. Degradation of leaf pigments at low temperatures was of a photo-oxidative nature since there was no degradation in the dark. The chlorophyll a/b ratio was decreased, carotene was degraded at a faster rate than chlorophyll, and 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU) and triphenyltetrazolium chloride (TTC) which prevent photo-oxidation, protected against chlorophyll degradation. The light and sucrose enhanced chlorophyll degradation at 25°C was of an enzymatic nature since it occurred in the dark as well as in the light. The chlorophyll a/b ratio was not affected, and carotene and chlorophyll degradation occurred at the same rate. Since DCMU completely inhibited the light enhancement at 25°C and experimentation in a low oxygen atmosphere also protected chlorophyll against the effect of light and sugar application, it is suggested that the enhancement of chlorophyll degradation by light and sucrose at 25°C may be due to increased sugar uptake of the chloroplasts and consequently excessive starch formation in the organelles.
• To prevent premature cell death and to allow efficient nutrient mobilization from senescing leaves, the photosynthetic apparatus has to be dismantled systematically. This requires temporal, spatial and metabolic regulation of photosynthetic function and photoprotection.• Conventional pulse-modulated fluorometry and chlorophyll fluorescence imaging were used to study age- and nutrient-dependent senescence patterns in Arabidopsis thaliana.• Nonphotochemical quenching (NPQ) rose during leaf maturation, indicating increased energy dissipation. During later stages of senescence, overall plant NPQ declined, but NPQ remained high in the base of rosette leaves. Other fluorescence parameters also showed spatial patterns, for example minimum fluorescence (F0) was temporarily increased in the tips of inner rosette leaves from where high F0 spread to the base, in a zone preceding cell death. Senescence-dependent changes in chlorophyll fluorescence characteristics were accelerated by growth on glucose-containing medium in combination with low, but not with high, nitrogen supply.• Our experiments revealed distinct spatial patterns of photosynthetic and photoprotective processes in senescing leaves and induction of these processes by high sugar-to-nitrogen ratios.
The metallothionein gene,LSC54, shows increased expression during leaf senescence inBrassica napusandArabidopsis thaliana. A number of abiotic and biotic stresses have been shown to induce senescence-like symptoms in plants and, to investigate this further, the promoter of theLSC54gene was cloned and fused to the GUS gene and transformed intoArabidopsis. The promoter was highly induced during leaf senescence and also in response to wounding; histochemical analysis indicated that this induction was localised to a few cells close to the wound site. The transgenicArabidopsistissue was infected with compatible and incompatible isolates of both the fungal biotroph,Peronospora parasiticaand the bacterial necrotroph,Pseudomonas syringae.Incompatible isolates induced rapid cell death (the hypersensitive response) at the site of infection and, with both pathogens, early, localised expression of the GUS gene was observed. In contrast, relatively slow induction of the GUS gene was seen in the compatible interaction and this was correlated with the appearance of senescence-like symptoms in the biotrophic interaction and cell death by necrosis that occurred in response to the necrotrophic pathogen. These results suggest that there are common steps in the signalling pathways that lead to cell death in the hypersensitive response, pathogen induced necrosis and senescence.
Leaf senescence is a hiphly-controlled sequence of events comprising the final stage of development. Cells remain viable during the process and new gene expression is required. There is some similarity between senescence in plants and programmed cell death in animals. In this review, different classes of senescence-related genes are defined and progress towards isolating such genes is reported. A range of internal and external factors which appear to cause leaf senescence is considered and various models for the mechanism of senescence- initiation are described. The current understanding of senescence at the wrganelle and molecular levels is presented. Finally, same ideas are mooted as to why senescence occurs and why it should be studied further.
We have analyzed macromolecular changes that are associated with natural leaf senescence in Arabidopsis thaliana. The loss of chlorophyll that is characteristic of leaf senescence is accompanied by a specific pattern of decline of total RNA and protein levels. We have constructed two cDNA libraries representing mRNAs from Arabidopsis leaves at different senescence stages. Six cDNA clones corresponding to mRNAs that substantially increase in abundance during senescence were isolated. The levels of these mRNAs remain elevated into the late stages of senescence when most of the chlorophyll and protein of the leaf has been degraded. Sis cDNA clones that correspond to mRNAs that exhibit contrasting behavior were also identified: the levels of these mRNAs decrease to undetectable levels during senescence. The changes in the levels of these specific mRNAs during the course of senescence are presented. The results indicate that major changes in gene expression occur in Arabidopsis leaves during the process of senescence.
Genes that are expressed during leaf senescence in Brassica napus were identified by the isolation of representative cDNA clones. DNA sequence and deduced protein sequence from two senescence-related cDNAs, LSC94 and LSC222, representing genes that are expressed early in leaf senescence before any yellowing of the leaves is visible, showed similarities to genes for pathogenesis-related (PR) proteins: a PR-1a-like protein and a class IV chitinase, respectively. The LSC94 and LSC222 genes showed differential regulation with respect to each other; an increase in expression was detected at different times during development of healthy leaves. Expression of both genes was induced by salicylic acid treatment. These findings suggest that some PR genes, as well as being induced by pathogen infection, may have alternative functions during plant development, for example in the process of leaf senescence.
Senescence occurs ubiquitously in living organisms. At the cellular level, a cell’s life history consists of two processes:
mitotic division and post-mitotic life pattern (6). A mother cell or germ-like cell can undergo a finite number of divisions
to produce daughter cells. When the cell ceases dividing, this cell is said to undergo mitotic senescence. In literature concerning
yeast and mammalian cells in culture, this type of senescence is often referred to as replicative senescence or replicative
aging. Although the mitotically senescent cell can no longer divide, it may live for a certain period before its ultimate
attrition/death; the functional degenerative process of the cell is called post-mitotic senescence. The degeneration of a
neuron and the dying and peeling of a skin cell represent mitotic senescence in nature. Plants exhibit both mitotic and post-mitotic
senescence.
Botrytis cinerea is a non-specific necrotrophic pathogen that attacks more than 200 plant species. In contrast to biotrophs, the necrotrophs obtain their nutrients by first killing the host cells. Many studies have shown that infection of plants by necrosis-causing pathogens induces a systemic acquired resistance (SAR), which provides protection against successive infections by a range of pathogenic organisms. We analyzed the role of SAR in B.cinerea infection of Arabidopsis. We show that although B.cinerea induced necrotic lesions and camalexin biosynthesis, it did not induce SAR-mediated protection against virulent strains of Pseudomonas syringae, or against subsequent B.cinerea infections. Induction of SAR with avirulent P.syringae or by chemical treatment with salicylic acid (SA) or benzothiadiazole also failed to inhibit B.cinerea growth, although removal of basal SA accumulation by expression of a bacterial salicylate hydroxylase (NahG) gene or by infiltration of 2-aminoindan-2-phosphonic acid, an inhibitor of phenylpropanoid pathway, increased B.cinerea disease symptoms. In addition, we show that B.cinerea induced expression of genes associated with SAR, general stress and ethylene/jasmonate-mediated defense pathways. Thus, B.cinerea does not induce SAR nor is it affected by SAR, making it a rare example of a necrogenic pathogen that does not cause SAR.
Leaf senescence is a complex developmental process during which essential nutrients are recycled. In order to unravel the biochemical pathways and regulatory mechanisms that underlie this process, it would be valuable to examine the transcriptome associated with leaf senescence. Accordingly, an Arabidopsis thaliana leaf senescence cDNA library with approximately 104 recombinant clones was subjected to large-scale single-pass sequencing. Approximately 6200 expressed sequence tags (ESTs) were obtained, corresponding to 2491 unique genes. These included 134 genes encoding transcription factors and 182 genes whose products are components of signal transduction pathways, such as the mitogen-activated protein kinase (MAPK) cascades. A total of 116 of these genes are predicted to be involved in protein turnover, including 75 genes associated with the ubiquitin–proteasome pathway and 35 proteinases. Many of the genes are predicted to encode transporters for ions, amino acids and sugars, consistent with the substantial nutrient recycling during leaf senescence. In addition, this study revealed ESTs for 98 annotated genes for which ESTs did not previously exist and 46 novel transcribed units that have not previously been annotated in the Arabidopsis genome. Approximately one-third of the 2491 genes are predicted to encode proteins with unknown functions. The genes are distributed evenly on the five chromosomes.
Abstract Leaf senescence is a complex developmental process during which essential nutrients are recycled. In order to unravel the biochemical pathways and regulatory mechanisms that underlie this process, it would be valuable to examine the transcriptome associated with leaf senescence. Accordingly, an Arabidopsis thaliana leaf senescence cDNA library with approximately 104 recombinant clones was subjected to large-scale single-pass sequencing. Approximately 6200 expressed sequence tags (ESTs) were obtained, corresponding to 2491 unique genes. These included 134 genes encoding transcription factors and 182 genes whose products are components of signal transduction pathways, such as the mitogen-activated protein kinase (MAPK) cascades. A total of 116 of these genes are predicted to be involved in protein turnover, including 75 genes associated with the ubiquitin–proteasome pathway and 35 proteinases. Many of the genes are predicted to encode transporters for ions, amino acids and sugars, consistent with the substantial nutrient recycling during leaf senescence. In addition, this study revealed ESTs for 98 annotated genes for which ESTs did not previously exist and 46 novel transcribed units that have not previously been annotated in the Arabidopsis genome. Approximately one-third of the 2491 genes are predicted to encode proteins with unknown functions. The genes are distributed evenly on the five chromosomes.
It is known that a senescing leaf loses water faster than a non-senescing leaf and that ABA has an important role in promoting leaf senescence. However, questions such as why water loss is faster, how water loss is regulated, and how ABA functions in leaf senescence are not well understood. Here we report on the identification and functional analysis of a leaf senescence associated gene called SAG113. The RNA blot and GUS reporter analyses all show that SAG113 is expressed in senescing leaves and is induced by ABA in Arabidopsis. The SAG113 expression levels are significantly reduced in aba2 and abi4 mutants. A GFP fusion protein analysis revealed that SAG113 protein is localized in the Golgi apparatus. SAG113 encodes a protein phosphatase that belongs to the PP2C family and is able to functionally complement a yeast PP2C-deficient mutant TM126 (ptc1Δ). Leaf senescence is delayed in the SAG113 knockout mutant compared with that in the wild type, stomatal movement in the senescing leaves of SAG113 knockouts is more sensitive to ABA than that of the wild type, and the rate of water loss in senescing leaves of SAG113 knockouts is significantly reduced. In contrast, inducible over-expression of SAG113 results in a lower sensitivity of stomatal movement to ABA treatment, more rapid water loss, and precocious leaf senescence. No other aspects of growth and development, including seed germination, were observed. These findings suggest that SAG113, a negative regulator of ABA signal transduction, is specifically involved in the control of water loss during leaf senescence.
Sugars are important signals in the regulation of plant metabolism and development. During stress and in senescing leaves, sugars often accumulate. In addition, both sugar accumulation and stress can induce leaf senescence. Infection by bacterial and fungal pathogens and attack by herbivores and gall-forming insects may influence leaf senescence via modulation of the sugar status, either by directly affecting primary carbon metabolism or by regulating steady state levels of plant hormones. Many types of biotic interactions involve the induction of extracellular invertase as the key enzyme of an apoplasmic phloem unloading pathway, resulting in a source-sink transition and an increased hexose/sucrose ratio. Induction of the levels of the phytohormones ethylene and jasmonate in biotic interactions results in accelerated senescence, whereas an increase in plant- or pathogen-derived cytokinins delays senescence and results in the formation of green islands within senescing leaves. Interactions between sugar and hormone signalling also play a role in response to abiotic stress. For example, interactions between sugar and abscisic acid (ABA) signalling may be responsible for the induction of senescence during drought stress. Cold treatment, on the other hand, can result in delayed senescence, despite sugar and ABA accumulation. Moreover, natural variation can be found in senescence regulation by sugars and in response to stress: in response to drought stress, both drought escape and dehydration avoidance strategies have been described in different Arabidopsis accessions. The regulation of senescence by sugars may be key to these different strategies in response to stress.
The plant hormone ethylene affects myriad developmental processes ranging from seed germination to organ senescence, and plays a crucial role in plant resistance to environmental stresses. The C-repeat/dehydration-responsive element binding factor genes (CBF1-3) are transcriptional activators involved in plant low-temperatures responses; their overexpression enhances frost tolerance, but also has various pleiotropic effects on growth and development, mainly growth retardation and delay of flowering and senescence. We found that overexpression of CBF2 in Arabidopsis suppressed leaf tissue responsiveness to ethylene as compared with wild-type plants, as manifested in significantly delayed senescence and chlorophyll degradation. In wild-type plants, exposure to ethylene at 0.1 microl.l(-1) for 48 h caused 50% reduction in chlorophyll levels as compared to leaves held in air alone, whereas CBF2-overexpressing plants required an ethylene concentration of 10.0 microl.l(-1) to cause the same effect. Furthermore, continuous exposure to ethylene at 1.0 microl.l(-1) reduced chlorophyll content in wild-type leaves by 50% after 42 h but took 72 h in CBF2-overexpressing plants. Transcript profiling of ethylene receptors and signal transduction genes in leaves of wild-type and CBF2-overexpressing plants, by means of the Affymetrix ATH1 genome array, revealed only minor differences in gene expression patterns - insufficient to explain the observed responsiveness differences. Nevertheless, we found that overexpression of CBF2 significantly increased transcript levels of 17 ABA biosynthetic and responsive genes and, thus, may have affected leaf responsiveness to ethylene via contrasting interactions with other hormones, mainly ABA. Overall, the current findings suggest that overexpression of the CBF2 transcriptional activator in Arabidopsis may, at least in part, contribute to the observed delay of leaf senescence and enhanced plant fitness by suppressing leaf responsiveness to stress-regulated ethylene.
Senescence and programmed cell death are important features for plant development. By allowing nutrient recycling and reallocation all along plant life, senescence contributes to the plant survival and the developmental program. This review first presents the concept of senescence in the global whole-plant life story, with an emphasis on the control exerted by flowering. It then focuses on leaf-senescence and its control by hormones, nutrients and development. The role of autophagy and of the Target of Rapamycin (TOR) kinase as potential regulators integrating environmental and endogenous signals, which control cell proliferation, reprogramming and nutrient management, is finally considered.
The onset and progression of senescence are under genetic and environmental control. The Arabidopsis thaliana NAC transcription factor ANAC092 (also called AtNAC2 and ORE1) has recently been shown to control age-dependent senescence, but its mode of action has not been analysed yet. To explore the regulatory network administered by ANAC092 we performed microarray-based expression profiling using estradiol-inducible ANAC092 overexpression lines. Approximately 46% of the 170 genes up-regulated upon ANAC092 induction are known senescence-associated genes, suggesting that the NAC factor exerts its role in senescence through a regulatory network that includes many of the genes previously reported to be senescence regulated. We selected 39 candidate genes and confirmed their time-dependent response to enhanced ANAC092 expression by quantitative RT-PCR. We also found that the majority of them (24 genes) are up-regulated by salt stress, a major promoter of plant senescence, in a manner similar to that of ANAC092, which itself is salt responsive. Furthermore, 24 genes like ANAC092 turned out to be stage-dependently expressed during seed growth with low expression at early and elevated expression at late stages of seed development. Disruption of ANAC092 increased the rate of seed germination under saline conditions, whereas the opposite occurred in respective overexpression plants. We also detected a delay of salinity-induced chlorophyll loss in detached anac092-1 mutant leaves. Promoter-reporter (GUS) studies revealed transcriptional control of ANAC092 expression during leaf and flower ageing and in response to salt stress. We conclude that ANAC092 exerts its functions during senescence and seed germination through partly overlapping target gene sets.
Gene expression responses of paper birch (Betula papyrifera) leaves to elevated concentrations of CO(2) and O(3) were studied with microarray analyses from three time points during the summer of 2004 at Aspen FACE. Microarray data were analyzed with clustering techniques, self-organizing maps, K-means clustering and Sammon's mappings, to detect similar gene expression patterns within sampling times and treatments. Most of the alterations in gene expression were caused by O(3), alone or in combination with CO(2). O(3) induced defensive reactions to oxidative stress and earlier leaf senescence, seen as decreased expression of photosynthesis- and carbon fixation-related genes, and increased expression of senescence-associated genes. The effects of elevated CO(2) reflected surplus of carbon that was directed to synthesis of secondary compounds. The combined CO(2)+O(3) treatment resulted in differential gene expression than with individual gas treatments or in changes similar to O(3) treatment, indicating that CO(2) cannot totally alleviate the harmful effects of O(3).
Senescence of plant organs is a genetically controlled process that regulates cell death to facilitate nutrient recovery and recycling, and frequently precedes, or is concomitant with, ripening of reproductive structures. In Arabidopsis thaliana, the seeds are contained within a silique, which is itself a photosynthetic organ in the early stages of development and undergoes a programme of senescence prior to dehiscence. A transcriptional analysis of the silique wall was undertaken to identify changes in gene expression during senescence and to correlate these events with ultrastructural changes. The study revealed that the most highly up-regulated genes in senescing silique wall tissues encoded seed storage proteins, and the significance of this finding is discussed. Global transcription profiles of senescing siliques were compared with those from senescing Arabidopsis leaf or petal tissues using microarray datasets and metabolic pathway analysis software (MapMan). In all three tissues, members of NAC and WRKY transcription factor families were up-regulated, but components of the shikimate and cell-wall biosynthetic pathways were down-regulated during senescence. Expression of genes encoding ethylene biosynthesis and action showed more similarity between senescing siliques and petals than between senescing siliques and leaves. Genes involved in autophagy were highly expressed in the late stages of death of all plant tissues studied, but not always during the preceding remobilization phase of senescence. Analyses showed that, during senescence, silique wall tissues exhibited more transcriptional features in common with petals than with leaves. The shared and distinct regulatory events associated with senescence in the three organs are evaluated and discussed.
Senescence of barley (Hordeum vulgare L. cv. Carina) primary foliage leaves was induced by transfer of the plants into darkness for 2 d. Under these conditions senescence was characterized by a light-reversible decline in the efficiency of photosystem II, and in chlorophyll and protein contents. To isolate senescence-associated genes a differential display of cDNA fragments amplified from reversely transcribed RNA was employed. By this method, gene expression in leaves of control plants collected at the onset of the dark period was compared with gene expression in senescing leaves collected at the end of the extended dark period. The expression of the genes represented by various differentially displayed cDNA fragments was examined by Northern blot hybridizations with RNA derived from primary foliage leaves before and after induction of senescence by darkness. In order to test whether these genes with enhanced expression during dark-induced senescence also show enhanced expression during natural senescence, Northern blot hybridizations were carried out with RNA samples prepared from flag leaves of barley plants during maturation and senescence under field conditions. Five of the cDNA fragments representing transcripts associated with dark-induced senescence, as well as with natural senescence, were selected as probes for screening a cDNA library from senescent flag leaves. With one probe a larger cDNA including a complete open reading frame with homology to the sequence of a known proteinase inhibitor was found. Another cDNA isolated by this means showed high sequence similarity with a gene coding for a 4-hydroxyphenylpyruvate dioxygenase. The other three larger cDNA clones isolated by this procedure so far do not show significant homologies with known sequences.
The expression of several Arabidopsis thaliana senescence-associated genes (SAGs) in attached and/or detached leaves was compared in response to age, dehydration, darkness, abscisic acid, cytokinin, and ethylene treatments. Most of the SAGs responded to most of the treatments in a similar fashion. Detachment in darkness and ethylene were the strongest inducers of both SAGs and visible yellowing. Detachment in light was also a strong inducer of SAGs, but not of visible yellowing. The other treatments varied more in their effects on individual SAGs. Responses were examined in both older and younger leaves, and generally were much stronger in the older ones. Individual SAGs differed from the norms in different ways, however, suggesting that their gene products play a role in overlapping but not identical circumstances. Some SAGs responded quickly to treatments, which may indicate a direct response. Others responded more slowly, which may indicate an indirect response via treatment-induced senescence. Four new SAGs were isolated as part of this work, one of which shows strong similarity to late embryogenesis-abundant (Lea) genes.
Four cDNA clones, named pSEN2, pSEN3, pSEN4, and pSEN5, for mRNAs induced during leaf senescence in Arabidopsis thaliana were characterized. The clones were isolated from a cDNA library of detached leaves incubated in darkness for 2 days to accelerate senescence, first by differential screening and then by examining expression of the primarily screened clones during age-dependent leaf senescence. Transcript levels detected by these cDNA clones, thus, were up-regulated in an age-dependent manner and during dark-induced leaf senescence. In contrast, when leaf senescence was induced by ethylene, ABA or methyljasmonate, the transcript level detected by the clones was differentially regulated depending on the senescence-inducing hormones. The transcript level for pSEN4 increased during senescence induced by all three hormones, while the transcript detected by the pSEN2 clone did not increase during senescence induced by ethylene. The transcript level for pSEN5 was increased upon ABA-induced senescence but decreased during ethylene-induced senescence. The pSEN3 clone detected multiple transcripts that are differentially regulated by these factors. The results show that, although the apparent senescence symptoms of Arabidopsis leaf appear similar regardless of the senescence-inducing factors, the detailed molecular state of leaf cells during senescence induced by different senescence-inducing factors is different. The pSEN3 clone encodes a polyubiquitin and the pSEN4 clone encodes a peptide related to endoxyloglucan transferase. This result is consistent with the expected roles of senescence-induced genes during leaf senescence.
The metallothionein gene, LSC54, shows increased expression during leaf senescence in Brassica napus and Arabidopsis thaliana. A number of abiotic and biotic stresses have been shown to induce senescence-like symptoms in plants and, to investigate this further, the promoter of the LSC54 gene was cloned and fused to the GUS gene and transformed into Arabidopsis. The promoter was highly induced during leaf senescence and also in response to wounding; histochemical analysis indicated that this induction was localised to a few cells close to the wound site. The transgenic Arabidopsis tissue was infected with compatible and incompatible isolates of both the fungal biotroph, Peronospora parasitica and the bacterial necrotroph, Pseudomonas syringae. Incompatible isolates induced rapid cell death (the hypersensitive response) at the site of infection and, with both pathogens, early, localised expression of the GUS gene was observed. In contrast, relatively slow induction of the GUS gene was seen in the compatible interaction and this was correlated with the appearance of senescence-like symptoms in the biotrophic interaction and cell death by necrosis that occurred in response to the necrotrophic pathogen. These results suggest that there are common steps in the signalling pathways that lead to cell death in the hypersensitive response, pathogen induced necrosis and senescence.
A system of cluster analysis for genome-wide expression data from DNA microarray hybridization is described that uses standard statistical algorithms to arrange genes according to similarity in pattern of gene expression. The output is displayed graphically, conveying the clustering and the underlying expression data simultaneously in a form intuitive for biologists. We have found in the budding yeast Saccharomyces cerevisiae that clustering gene expression data groups together efficiently genes of known similar function, and we find a similar tendency in human data. Thus patterns seen in genome-wide expression experiments can be interpreted as indications of the status of cellular processes. Also, coexpression of genes of known function with poorly characterized or novel genes may provide a simple means of gaining leads to the functions of many genes for which information is not available currently.
Controlled cellular suicide is an important process that can be observed in various organs during plant development. From the generation of proper sexual organs in monoecious plants to the hypersensitive response (HR) that occurs during incompatible pathogen interactions, programmed cell death (PCD) can be readily observed. Although several biochemical and morphological parameters have been described for various types of cell death in plants, the relationships existing between those different types of PCD events remain unclear. In this work, we set out to examine if two early molecular markers of HR cell death (HIN1 and HSR203J) as well as a senescence marker (SAG12) are coordinately induced during these processes. Our result indicates that although there is evidence of some cross-talk between both cell death pathways, spatial and temporal characteristics of activation for these markers during hypersensitive response and senescence are distinct. These observations indicate that these markers are relatively specific for different cell death programs. Interestingly, they also revealed that a senescence-like process seems to be triggered at the periphery of the HR necrotic lesion. This suggests that cells committed to die during the HR might release a signal able to induce senescence in the neighboring cells. This phenomenon could correspond to the establishment of a second barrier against pathogens. Lastly, we used those cell death markers to better characterize cell death induced by copper and we showed that this abiotic induced cell death presents similarities with HR cell death.
To determine the range of gene activities associated with leaf senescence, we have identified genes that show preferential transcript accumulation during this developmental stage. The mRNA levels of a diverse array of gene products increases during leaf senescence, including a protease, a ribosomal protein, two cinnamyl alcohol dehydrogenases, a nitrilase and glyoxalase II. Two of the genes identified are known to be pathogen-induced. The senescence specificity of each gene was determined by characterization of transcript accumulation during leaf development and in different tissues. The increased expression of nitrilase in senescent leaves is paralleled by an increase in free indole-3-acetic acid (IAA) levels. Additionally, we have demonstrated that the induction of defense-related genes during leaf senescence is pathogen-independent and that salicylic acid accumulation is not essential for this induction. Our data indicate that the induction of certain genes involved in plant defense responses is a component of the leaf senescence program.
The expression patterns of senescence-related genes were determined during ozone (O(3)) exposure in Arabidopsis. Rosettes were treated with 0.15 microL L(-1) O(3) for 6 h d(-1) for 14 d. O(3)-treated leaves began to yellow after 10 d of exposure, whereas yellowing was not apparent in control leaves until d 14. Transcript levels for eight of 12 senescence related genes characterized showed induction by O(3). SAG13 (senescence-associated gene), SAG21, ERD1 (early responsive to dehydration), and BCB (blue copper-binding protein) were induced within 2 to 4 d of O(3) treatment; SAG18, SAG20, and ACS6 (ACC synthase) were induced within 4 to 6 d; and CCH (copper chaperone) was induced within 6 to 8 d. In contrast, levels of photosynthetic gene transcripts, rbcS (small subunit of Rubisco) and cab (chlorophyll a/b-binding protein), declined after 6 d. Other markers of natural senescence, SAG12, SAG19, MT1 (metallothionein), and Atgsr2 (glutamine synthetase), did not show enhanced transcript accumulation. When SAG12 promoter-GUS (beta-glucuronidase) and SAG13 promoter-GUS transgenic plants were treated with O(3), GUS activity was induced in SAG13-GUS plants after 2 d but was not detected in SAG12-GUS plants. SAG13 promoter-driven GUS activity was located throughout O(3)-treated leaves, whereas control leaves generally showed activity along the margins. The acceleration of leaf senescence induced by O(3) is a regulated event involving many genes associated with natural senescence.
Leaf senescence is a complex process that is controlled by multiple developmental and environmental signals and is manifested by induced expression of a large number of different genes. In this paper we describe experiments that show, for the first time, that the salicylic acid (SA)-signalling pathway has a role in the control of gene expression during developmental senescence. Arabidopsis plants defective in the SA-signalling pathway (npr1 and pad4 mutants and NahG transgenic plants) were used to investigate senescence-enhanced gene expression, and a number of genes showed altered expression patterns. Senescence-induced expression of the cysteine protease gene SAG12, for example, was conditional on the presence of SA, together with another unidentified senescence-specific factor. Changes in gene expression patterns were accompanied by a delayed yellowing and reduced necrosis in the mutant plants defective in SA-signalling, suggesting a role for SA in the cell death that occurs at the final stage of senescence. We propose the presence of a minimum of three senescence-enhanced signalling factors in senescing leaves, one of which is SA. We also suggest that a combination of signalling factors is required for the optimum expression of many genes during senescence.
Exposure to UV‐B radiation resulted in a loss of chlorophyll and an increase in lipid damage in a similar manner to that induced
during natural senescence. In addition, exposure to UV‐B led to the induction of a number of genes associated with senescence
(SAG12, 13, 14, and 17). These results show, for the first time, that exposure to UV‐B can lead to cellular decline through active and regulated
processes involving many genes also associated with natural senescence.
Polysaccharides and proteins are secreted to the inner surface of the growing cell wall, where they assemble into a network that is mechanically strong, yet remains extensible until the cells cease growth. This review focuses on the agents that directly or indirectly enhance the extensibility properties of growing walls. The properties of expansins, endoglucanases, and xyloglucan transglycosylases are reviewed and their postulated roles in modulating wall extensibility are evaluated. A summary model for wall extension is presented, in which expansin is a primary agent of wall extension, whereas endoglucanases, xyloglucan endotransglycosylase, and other enzymes that alter wall structure act secondarily to modulate expansin action.
WRKY proteins constitute a large family of plant-specific transcription factors whose precise functions have yet to be elucidated. Here we show that expression of one representative in Arabidopsis, AtWRKY6, is influenced by several external and internal signals often involved in triggering senescence processes and plant defence responses. Progressive 5' deletions of the AtWRKY6 promoter allowed separation of defined regions responsible for the expression in distinct organs or upon pathogen challenge. Nuclear localization of AtWRKY6 was demonstrated; protein truncations and gain-of-function studies enabled delineation of a region harbouring a novel type of functional nuclear localization signal (NLS).
We have compared the time course of leaf senescence in pea (Pisum sativum L. cv Messire) plants subjected to a mild water deficit to that of monocarpic senescence in leaves of three different ages in well-watered plants and to that of plants in which leaf senescence was delayed by flower excision. The mild water deficit (with photosynthesis rate maintained at appreciable levels) sped up senescence by 15 d (200 degrees Cd), whereas flower excision delayed it by 17 d (270 degrees Cd) compared with leaves of the same age in well-watered plants. The range of life spans in leaves of different ages in control plants was 25 d (340 degrees Cd). In all cases, the first detected event was an increase in the mRNA encoding a cysteine-proteinase homologous to Arabidopsis SAG2. This happened while the photosynthesis rate and the chlorophyll and protein contents were still high. The 2-fold variability in life span of the studied leaves was closely linked to the duration from leaf unfolding to the beginning of accumulation of this mRNA. In contrast, the duration of the subsequent phases was essentially conserved in all studied cases, except in plants with excised flowers, where the degradation processes were slower. These results suggest that senescence in water-deficient plants was triggered by an early signal occurring while leaf photosynthesis was still active, followed by a program similar to that of monocarpic senescence. They also suggest that reproductive development plays a crucial role in the triggering of senescence.
Botrytis cinerea is a non-specific necrotrophic pathogen that attacks more than 200 plant species. In contrast to biotrophs, the necrotrophs obtain their nutrients by first killing the host cells. Many studies have shown that infection of plants by necrosis-causing pathogens induces a systemic acquired resistance (SAR), which provides protection against successive infections by a range of pathogenic organisms. We analyzed the role of SAR in B. cinerea infection of Arabidopsis. We show that although B. cinerea induced necrotic lesions and camalexin biosynthesis, it did not induce SAR-mediated protection against virulent strains of Pseudomonas syringae, or against subsequent B. cinerea infections. Induction of SAR with avirulent P. syringae or by chemical treatment with salicylic acid (SA) or benzothiadiazole also failed to inhibit B. cinerea growth, although removal of basal SA accumulation by expression of a bacterial salicylate hydroxylase (NahG) gene or by infiltration of 2-aminoindan-2-phosphonic acid, an inhibitor of phenylpropanoid pathway, increased B. cinerea disease symptoms. In addition, we show that B. cinerea induced expression of genes associated with SAR, general stress and ethylene/jasmonate-mediated defense pathways. Thus, B. cinerea does not induce SAR nor is it affected by SAR, making it a rare example of a necrogenic pathogen that does not cause SAR.