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Modulation of plant and bacterial polyamine metabolism during the compatible interaction between tomato and Pseudomonas syringae
Abstract
The polyamines putrescine, spermidine and spermine participate in a variety of cellular processes in all organisms. Many studies have shown that these polycations are important for plant immunity, as well as for the virulence of diverse fungal phytopathogens. However, the polyamines’ roles in the pathogenesis of phytopathogenic bacteria have not been thoroughly elucidated to date. To obtain more information on this topic, we assessed the changes in polyamine homeostasis during the infection of tomato plants by Pseudomonas syringae. Our results showed that polyamine biosynthesis and catabolism are activated in both tomato and bacteria during the pathogenic interaction. This activation results in the accumulation of putrescine in whole leaf tissues, as well as in the apoplastic fluids, which is explained by the induction of its synthesis in plant cells and also on the basis of its excretion by bacteria. We showed that the excretion of this polyamine by P. syringae is stimulated under virulence-inducing conditions, suggesting that it plays a role in plant colonization. However, no activation of bacterial virulence traits or induction of plant invasion was observed after the exogenous addition of putrescine. In addition, no connection was found between this polyamine and plant defence responses. Although further research is warranted to unravel the biological functions of these molecules during plant-bacterial interactions, this study contributes to a better understanding of the changes associated with the homeostasis of polyamines during plant pathogenesis.
... Our previous work also suggests that the synthesis of polyamines might play a significant role in bacterial pathogenesis. In this regard, we showed the induction of this pathway during plant colonization and the accumulation of putrescine in the plant apoplast [15]. Furthermore, we conducted a meta-analysis of publicly accessible transcriptomic data on phytopathogenic bacteria that demonstrated that genes from this metabolic route are induced during the early stages of infection and that they are suppressed by plant immunity mechanisms [16]. ...
... Based on the values of chlorophyll concentrations, we determined that under our experimental conditions, the cytosolic contamination of the apoplastic washing fluids (AWF) was under 1%. Free polyamines in these samples were quantified as previously described in [15]. ...
... The reaction mixture was incubated for 1 h at 37 °C. Quantitative real-time PCR (qRT-PCR) was performed using the primers and protocol as described in Vilas et al. [15]. ...
This study investigates the role of polyamine biosynthesis in the pathogenesis of the bacterial phytopathogen Pseudomonas syringae pv. tomato . Through a comprehensive phenotypic analysis of mutant strains affected in the synthesis of putrescine and spermidine, we reveal a complex interplay between this metabolic pathway and bacterial virulence. Disruption of putrescine synthesis impairs a variety of virulence traits such as motility, biofilm formation, siderophore production, prevention of plant stomatal closure and the functionality of the type III secretion system. This is reversed by reintroducing the deleted genes, but not by the supplementation of culture media with putrescine or apoplastic washing fluids (AWF). Similarly, suppression of spermidine biosynthesis results in a comparable phenotype. However, in this case, the wild-type phenotype is restored by adding spermidine, AWF or expressing the spermidine synthase gene. We conclude that both putrescine and spermidine are important for bacterial virulence and that plant-derived spermidine can partially compensate for bacterial needs. Accordingly, whereas putrescine deficiency leads to a hypovirulent phenotype, spermidine synthesis perturbation does not affect plant colonization. These findings emphasize the critical role of polyamine metabolism in the plant invasion process by bacterial pathogens.
... To explain this observation, it should be considered that free Spd could have different sources. For instance, it might be residual Spd absorbed during the preparation of the inocula in LB, which contains polyamines in its composition 24 . An alternative explanation consists in the release of free Spd from the fraction that exists conjugated to organic compounds 25,26 . ...
... However, it should be considered that the model depicted here could differ in the plant environment since polyamines, whether derived from the bacterial or plant metabolism, may have dissimilar functions. For instance, it has been shown that Put accumulates in plant tissues during bacterial infections 21,24,59 . This effect, for some bacterial species, is a consequence of the action of secreted effectors that increments plant arginine decarboxylase activities to promote Put production and the activation of defense responses, which ultimately reduce bacterial cell proliferation 59,60 . ...
... Membrane-attached polyamines were isolated according to Johnson et al. 20 . Polyamine quantification was performed by derivatization with dansyl chloride as previously described by Vilas et al. 24 . Protein concentrations were determined by the Bradford assay 65 . ...
Bacterial phytopathogens living on the surface or within plant tissues may experience oxidative stress because of the triggered plant defense responses. Although it has been suggested that polyamines can defend bacteria from this stress, the mechanism behind this action is not entirely understood. In this study, we investigated the effects of oxidative stress on the polyamine homeostasis of the plant pathogen Pseudomonas syringae and the functions of these compounds in bacterial stress tolerance. We demonstrated that bacteria respond to H2O2 by increasing the external levels of the polyamine putrescine while maintaining the inner concentrations of this compound as well as the analogue amine spermidine. In line with this, adding exogenous putrescine to media increased bacterial tolerance to H2O2. Deletion of arginine decarboxylase (speA) and ornithine decarboxylate (speC), prevented the synthesis of putrescine and augmented susceptibility to H2O2, whereas targeting spermidine synthesis alone through deletion of spermidine synthase (speE) increased the level of extracellular putrescine and enhanced H2O2 tolerance. Further research demonstrated that the increased tolerance of the ΔspeE mutant correlated with higher expression of H2O2-degrading catalases and enhanced outer cell membrane stability. Thus, this work demonstrates previously unrecognized connections between bacterial defense mechanisms against oxidative stress and the polyamine metabolism.
... As previously mentioned, free and conjugated Put levels are enhanced in plant tissues infected by fungi and bacteria [185,198]. In most cases, Put levels in infected tissues are the result of de novo biosynthesis [192], although it was also proposed that Put is excreted by the pathogen during plant tissue colonisation [198]. ...
... As previously mentioned, free and conjugated Put levels are enhanced in plant tissues infected by fungi and bacteria [185,198]. In most cases, Put levels in infected tissues are the result of de novo biosynthesis [192], although it was also proposed that Put is excreted by the pathogen during plant tissue colonisation [198]. Vilas et al. [198] explained the accumulation of Put in the whole leaf tissues, as well as in the apoplast of tomato plants infected with the bacterial P. syringae by the induction of its synthesis in plant cells and also by the excretion of bacteria. ...
... In most cases, Put levels in infected tissues are the result of de novo biosynthesis [192], although it was also proposed that Put is excreted by the pathogen during plant tissue colonisation [198]. Vilas et al. [198] explained the accumulation of Put in the whole leaf tissues, as well as in the apoplast of tomato plants infected with the bacterial P. syringae by the induction of its synthesis in plant cells and also by the excretion of bacteria. The excretion of Put by P. syringae was stimulated under virulence inducing conditions, but no activation of bacterial virulence traits or induction of plant invasion were observed after the exogenous addition of Put. ...
Putrescine (Put) is the starting point of the polyamines (PAs) pathway and the most common PA in higher plants. It is synthesized by two main pathways (from ornithine and arginine), but recently a third pathway from citrulline was reported in sesame plants. There is strong evidence that Put may play a crucial role not only in plant growth and development but also in the tolerance responses to the major stresses affecting crop production. The main strategies to investigate the involvement of PA in plant systems are based on the application of competitive inhibitors, exogenous PAs treatments, and the most efficient approaches based on mutant and transgenic plants. Thus, in this article, the recent advances in understanding the role of this metabolite in plant growth promotion and protection against abiotic and biotic stresses will be discussed to provide an overview for future research.
... In this way, Put derived from the higher number of bacterial cells accumulated in these mutants over time (as compared to WT plants) probably contributed to the increase in Put detected in plant tissues, along with Put derived from plant metabolism. In this regard, it has previously been shown that Put derived from Pst is accumulated in infected tomato tissues (Vilas et al., 2018). Moreover, Lowe-Power et al. (2018) demonstrated that the pathogenic bacterium Ralstonia solanacearum excretes Put to the apoplast of infected tomato plants, which leads to increase bacterial virulence as a result of the accumulation of this diamine. ...
... Besides, the addition of SA to the growth medium caused an increment in the concentration of Put, whereas Spd and Spm were slightly diminished (Figure 2). Previous studies demonstrated the occurrence of a rise in apoplastic Put content during the recognition of virulent and nonvirulent microbes Marina et al., 2008;Vilas et al., 2018;Yoda et al., 2009), suggesting that Put might have an important role in this compartment during the elicitation of plant defense. Even though the rise in Put concentration provoked by SA may be explained by the mechanisms discussed in previous paragraphs, our results also showed that SA treatment leads to a reduction of AO activity ( Figure 3C). ...
... In this regard, the increased susceptibility of sid2-2 and mpk6-2 mutants to bacterial infection is known to lead to higher bacterial titers than in WT plants, which could counterbalance the lower accumulation of plant-derived Put in the mutant lines. Virulence-inducing conditions have been shown to stimulate Put release to the extracellular medium by Pst (Vilas et al., 2018), thus providing support to the idea that higher bacterial titers could lead to increased Put levels in infected plant tissues. However, it should also be taken into account that increased bacterial titers in sid2-2 and mpk6-2 could also affect the host's PA pools or the availability of precursors of PA biosynthesis. ...
Polyamines (PAs) play important roles in plant defense against pathogens, but the regulation of PA metabolism by hormone‐mediated defense signaling pathways has not been studied in depth. In this study, the modulation of PA metabolism by salicylic acid (SA) was analyzed in Arabidopsis by combining the exogenous application of this hormone with PA biosynthesis and SA synthesis/signaling mutants. SA induced notable modifications of PA metabolism, mainly consisting in putrescine (Put) accumulation both in whole‐plant extracts and apoplastic fluids. Put was accumulated at the expense of increased biosynthesis by ARGININE DECARBOXYLASE 2 and decreased oxidation by copper amine oxidase. Enhancement of Put levels by SA was independent of the regulatory protein NONEXPRESSOR OF PATHOGENESIS‐RELATED GENES 1 (NPR1) and the signaling kinases MKK4 and MPK3, but depended on MPK6. However, plant infection by Pseudomonas syringae pv. tomato DC3000 elicited Put accumulation in an SA‐dependent way. The present study demonstrates a clear connection between SA signaling and plant PA metabolism in Arabidopsis and contributes to understanding the mechanisms by which SA modulates PA levels during plant‐pathogen interactions.
... Different studies have shown that both free and conjugated Put levels rise considerably in plant tissues infected by fungi (Rodríguez-Kessler, Ruiz, Maiale, Ruiz-Herrera, & Jiménez-Bremont, 2008;Wojtasik, Kulma, Namysł, Preisner, & Szopa, 2015) and bacteria (Vilas et al., 2018). In most cases, Put levels in infected tissues are the result of de novo biosynthesis (Kim, Kim, & Hwang, 2013;Rossi, Marina, & Pieckenstain, 2015), although it has also been proposed that Put is excreted by the pathogen during plant tissue colonisation (Vilas et al., 2018). ...
... Different studies have shown that both free and conjugated Put levels rise considerably in plant tissues infected by fungi (Rodríguez-Kessler, Ruiz, Maiale, Ruiz-Herrera, & Jiménez-Bremont, 2008;Wojtasik, Kulma, Namysł, Preisner, & Szopa, 2015) and bacteria (Vilas et al., 2018). In most cases, Put levels in infected tissues are the result of de novo biosynthesis (Kim, Kim, & Hwang, 2013;Rossi, Marina, & Pieckenstain, 2015), although it has also been proposed that Put is excreted by the pathogen during plant tissue colonisation (Vilas et al., 2018). Reduced Put levels, in adc loss-of-function mutants and adc- Although a complete picture of the roles of PAs in plant defence is still difficult to be drawn, it has been found that free PAs can restrict the growth of some fungal pathogens in vitro (Mo et al., 2015b;Wojtasik et al., 2015) and that exogenous application of Put can suppress nematode development in infected plants (Khajuria & Ohri, 2018). ...
... Perhaps under plant-pathogen interactions, phosphorylation events might also be responsible for the modulation of PA levels in infected tissues through the specific activation of PA transporters. As mentioned before, the accumulation of PAs (mainly Put) in infected tissues can result from de novo plant PA biosynthesis and also bacterial Put excretion into the apoplast (Vilas et al., 2018). However, it should not be ruled out ...
Polyamines are low molecular weight amines, with versatile and essential functions during the lifespan of prokaryotes and eukaryotes. Modulation of polyamine metabolism under biotic stress has attracted a great deal of interest; however, the precise functions of these amines in plant defence responses to pathogen attack are still poorly understood. Herein we summarise and review important aspects of the regulation of polyamine biosynthesis, catabolism and conjugation under biotic stress that might contribute to improve present‐day knowledge about these compounds in plant immunity. Particular attention is paid to the intracellular localisation of the proteins/enzymes associated to polyamine metabolism, as well as the impact of pathogen effector proteins on the control of plant polyamine metabolism is discussed.
... However, increase of leaf PA levels, by the same experimental approaches, led to increased necrosis in planta due to infection by Sclerotinia sclerotiorum, and the PA-induced increase of leaf necrosis after fungal infection was attenuated by inhibiting the activity of DAO and PAO (Marina et al., 2008). There is evidence that exogenous PA application modifies pathogenic responses depending on the strategy of the specific pathogen (Marina et al., 2008;Stes et al., 2011;Valdes-Santiago et al., 2012;Vilas et al., 2018). ...
... Plants have developed a series of strategies to thwart pathogen attack (Vilas et al., 2018). The production of ROS is one of the defense responses against pathogen attack. ...
... This is probably related to the ability of plant PAOs to oxidize t-Spm in a wide range of tissues and organs, as occurs when other PAs such as Spm are accumulated throughout the plant (Marina et al., 2013). In addition to that, pathogens activate their own and the plant PA metabolism during the compatible interaction between tomato and Pseudomonas syringae (Vilas et al., 2018). This activation results in the accumulation of Put in whole leaf tissues, as well as in the apoplastic fluids, which is explained by the induction of its synthesis in plant cells and also on the basis of its excretion by bacteria (Vilas et al., 2018). ...
Polyamine (PA) catabolic processes are performed by copper-containing amine oxidases (CuAOs) and flavin-containing PA oxidases (PAOs). So far, several CuAOs and PAOs have been identified in many plant species. These enzymes exhibit different subcellular localization, substrate specificity, and functional diversity. Since PAs are involved in numerous physiological processes, considerable efforts have been made to explore the functions of plant CuAOs and PAOs during the recent decades. The stress signal transduction pathways usually lead to increase of the intracellular PA levels, which are apoplastically secreted and oxidized by CuAOs and PAOs, with parallel production of hydrogen peroxide (H2O2). Depending on the levels of the generated H2O2, high or low, respectively, either programmed cell death (PCD) occurs or H2O2 is efficiently scavenged by enzymatic/nonenzymatic antioxidant factors that help plants coping with abiotic stress, recruiting different defense mechanisms, as compared to biotic stress. Amine and PA oxidases act further as PA back-converters in peroxisomes, also generating H2O2, possibly by activating Ca²⁺ permeable channels. Here, the new research data are discussed on the interconnection of PA catabolism with the derived H2O2, together with their signaling roles in developmental processes, such as fruit ripening, senescence, and biotic/abiotic stress reactions, in an effort to elucidate the mechanisms involved in crop adaptation/survival to adverse environmental conditions and to pathogenic infections.
... Putrescine is also a polyamine may be a metabolic signal related to the increase in the bacterial titer Lxx in sugarcane, being a metabolite that favors colonization in leaf tissues. Studies showed that putrescine is to virulence of bacteria in plants and for the development of the morphological structures of fungus(Vilas et al. 2018; Sánchez-Elordi et al.2019), as it is also associated with a defense response against pathogenic microorganisms. Putrescine is an essential metabolite for disease severity, such as bacterial wilt in tomato caused by Ralstonia solanacearum (Lowe-Power et al. 2018). ...
... Putrescine is an essential metabolite for disease severity, such as bacterial wilt in tomato caused by Ralstonia solanacearum (Lowe-Power et al. 2018). In Pseudomonas syringae, the absence of putrescine inhibits the growth of the bacteria in the plant, while the accumulation of putrescine in the apoplast favors colonization in the leaf(Vilas et al. 2018).Can the reduction in sulfur content in sugarcane be linked to the susceptibility of sugarcane to disease? Sulfur is an important nutrient involved in plant defense against vascular pathogens (Willians and Copper, 2003). ...
Aims Leifsonia xyli subsp. xyli (Lxx) is the most common sugarcane bacterial pathogen that affects plant development and primary metabolism. For example, cysteine and methionine are sulfur-containing essential amino acids used for bacterial growth and the title of Lxx in sugarcane plants might affect sulfur metabolism. The goal of this study were to evaluate how the increase in bacterial titers affects nutritional status and sulfur metabolism in sugarcane.
Methods: The study was carried out with a susceptible sugarcane (Saccharum officinarum) genotype CB49260, with low and high Lxx titers, evaluating the mineral status and levels of primary metabolites.
Results: Plants with high Lxx titers increased leaf sulfur content (S) compared to plants with low Lxx titers where plants with high Lxx titers displayed increased levels of sulfate, sucrose, maltose, raffinose, shikimic acid, malate, putrescine, glycerol, and, erythritol but decreased levels of methionine and glutathione in leaves. In the culm, plants with high Lxx titers displayed increased contents of maltose but decreased levels of threonine, ornithine, phenylalanine and myo-inositol when compared with plants with low Lxx titers.
Conclusions: This study thus demonstrated that high bacterial titers increase sulfur demand in sugarcane. However, the increase in S content in the leaf did not result in higher sulfur assimilation, which was verified by increases sulfate level and decreases in methionine and glutathione levels. Therefore, our study showed that plant metabolism fails to meet the increased sulfur organic compound demand due to lower methionine and glutathione biosynthesis and methionine catabolism to putrescine biosynthesis in the leaves.
... For instance, it was reported that Spd is required for the synthesis of the toxin Phevamine A in Pseudomonas syringae, which helps to suppress the oxidative burst elicited in plant tissues following pathogen recognition (O'Neill et al., 2018). In addition, the secretion of Put by phytopathogenic bacteria has been observed in different bacterial species, such as Ralstonia solanacearum, P. syringae, and Dickeya zeae (Lowe-Power et al., 2018;Vilas et al., 2018;Shi et al., 2019). Based on various reports demonstrating that polyamines can scavenge reactive oxygen species (ROS) and activate the antioxidant machinery (Bors et al., 1989;Das and Misra, 2004;Nayyar and Chander, 2004;Tang and Newton, 2005), it was proposed that Put secretion by bacteria constitutes a mechanism to counteract the oxidative stress imposed by plants at the site of the infection, a function that has yet to be confirmed. ...
... These results curtail the importance of polyamines in supporting growth in low-nutrient media (meaning that more preferred metabolites would be synthesized instead under these circumstances) and besides, they also suggest that the mechanisms governing polyamine homeostasis are distinct from those inducing bacterial pathogenicity. Even though this observation contradicts our previous gene expression analysis in Pst using qRT-PCR (where the polyamine biosynthetic gene speC and the catabolic enzymes pauA3 and pauB2 resulted mildly upregulated in minimal medium), it should be considered that in the mentioned work only samples taken 6 hpi were analyzed and that variations in gene expression before or after that time could have been missed (Vilas et al., 2018). ...
To succeed in plant invasion, phytopathogenic bacteria rely on virulence mechanisms to subvert plant immunity and create favorable conditions for growth. This process requires a precise regulation in the production of important proteins and metabolites. Among them, the family of compounds known as polyamines have attracted considerable attention as they are involved in important cellular processes, but it is not known yet how phytopathogenic bacteria regulate polyamine homeostasis in the plant environment. In the present study, we performed a meta-analysis of publicly available transcriptomic data from experiments conducted on bacteria to begin delving into this topic and better understand the regulation of polyamine metabolism and its links to pathogenicity. We focused our research on Pseudomonas syringae, an important phytopathogen that causes disease in many economically valuable plant species. Our analysis discovered that polyamine synthesis, as well as general gene expression activation and energy production are induced in the early stages of the disease. On the contrary, synthesis of these compounds is inhibited whereas its transport is upregulated later in the process, which correlates with the induction of virulence genes and the metabolism of nitrogen and carboxylic acids. We also found that activation of plant defense mechanisms affects bacterial polyamine synthesis to some extent, which could reduce bacterial cell fitness in the plant environment. Furthermore, data suggest that a proper bacterial response to oxidative conditions requires a decrease in polyamine production. The implications of these findings are discussed.
... In addition, the secretion of Put by phytopathogenic bacteria has recently attracted some attention. This process was demonstrated to occur in different bacterial species such as Ralstonia solanacearum growing at the plant xylem, P. syringae dwelling at the apoplastic compartment, and Dickeya zeae growing under in vitro conditions [23][24][25] . On the basis of different reports demonstrating that polyamines have the ability to scavenge reactive oxygen species (ROS) and activate the antioxidant machinery 26-29 , it was proposed that Put secretion by bacteria constitutes a mechanism to counteract the oxidative stress imposed by plants at the site of the infection, a function that remains to be corroborated. ...
... These results curtail the importance of polyamines to support growth in minimal media (so that the synthesis of other metabolites is preferred) and besides, suggest that the mechanisms governing polyamine homeostasis differ from those inducing bacterial virulence. Even though this observation contradicts our previous gene expression analysis in Pst using qRT-PCR (where the polyamine biosynthetic gene speC and the catabolic enzymes pauA3 and pauB2 resulted mildly up-regulated in minimal medium), it should be considered that only samples taken 6 hai were analysed in that work and that variations in gene expression before or after that time could have been missed 24 . ...
Pseudomonas syringae is a phytopathogenic bacteria causing disease in a wide variety of economically important plant species. To succeed in plant invasion, these bacteria rely on virulence mechanisms that subvert plant immunity and create favorable conditions for growth. This process requires a precise regulation in the production of important proteins and metabolites. Among them, the family of compounds known as polyamines have attracted attention as they are involved in essential cellular processes. However, it is not known yet how phytopathogenic bacteria regulates polyamine homeostasis in the plant environment. In this work, we conducted a meta-analysis of publicly available transcriptomic data with the purpose to understand the regulation of the metabolism of polyamines and their links to pathogenicity in P. syringae . We demonstrated that polyamine synthesis is induced in the early stages of the disease, along with gene expression activation and energy production. On the contrary, the synthesis of these compounds is repressed whereas its transport is up-regulated at later stages, which correlates with the expression of virulence genes and the metabolism of nitrogen and carboxylic acids. We also showed that plant defense mechanisms partially hinder polyamine synthesis, which could reduce cell fitness in the plant environment. In addition, our analysis suggested that a proper bacterial response to oxidative conditions requires a reduction in polyamine production. The implications of these conclusions are discussed.
... In line with this, previous research has shown that Pas content and metabolism are augmented in plants under pathogen attack independently of whether the pathogen infection strategy is via biotrophic or necrotrophic interactions (Walters, 2003;Jiménez Bremont et al. 2014;Romero et al. 2018). It has also been demonstrated that phytopathogens perturb the activity and functionality of photosystem and Pas levels (Vilas et al., 2018). Plants respond to biotic stress by adjusting their machinery to maintain photosynthetic activity. ...
... Results from the present study demonstrate that the Pas found in pecan leaves correspond to those that are most abundant in the majority of plants, namely Put, Spd, and Spm. In line with this, the free Pas levels in pecan leaflets (Fig. 2) showed similar values to those found in other plant species, such as rice, soybean, corn, tomato, hazelnut, malus, peach, and mandarin (Bartolini et al., 2009;Campestre et al., 2011;Maiale et al., 2004;Liu and Moriguchi, 2007;Mirsoleimani and Shahsavar, 2018;Rey et al., 1994;Rodriguez-Kessler et al., 2008;Vilas et al., 2018). In all these plants, only Put, Spd, and Spm were detected and the values corresponding to the three of them coincided with those reported in fresh weight in the present study. ...
Pecan plants are attacked by the fungus Phomopsis spp. that causes stem canker, a serious and emerging disease in commercial orchards. Stem canker, which has been reported in several countries, negatively affects tree canopy health, eventually leading to production losses. The purpose of this study was to inquire into the physiology of pecan plants under stem canker attack by Phomopsis spp. To this end, pecan plants were inoculated with an isolate of Phomopsis spp. and several parameters, such as polyamines, proline, sugars, starch, chlorophyll fluorescence and canopy temperature were analysed. Under artificial inoculation, a high disease incidence was observed with symptoms similar to those in plants showing stem canker under field conditions. Furthermore, the infected stem showed dead tissue with brown necrotic discolouration in the xylem tissue. The free polyamines putrescine, spermidine, and spermine were detected and their levels decreased as leaves aged in the infected plants with respect to the controls. Chlorophyll fluorescence parameters, such as Sm, ψEO, and QbRC decreased under plant infection and therefore the K-band increased. Canopy temperature and proline content increased in the infected plants with respect to the controls while sugar content decreased. These data suggest that stem canker caused by Phomopsis spp. induces physiological changes that are similar to those observed in plants under drought stress. To our knowledge, this is the first study that documents the physiological and biochemical effects derived from pecan-Phomopsis interaction.
... Genes encoding proteins involved in iron metabolism and transport, siderophore synthesis, and other transport processes were also induced in bluelight-treated epiphytic populations. Interestingly, some of these genes have been related to epiphytic fitness, assisting bacteria to cope with nutrient fluctuations and plant-defence-derived compounds, as well as to compete for limiting nutrients and ecological niches (Kachroo and Kachroo, 2009;Ryffel et al., 2016;Vilas et al., 2018). ...
... We also found up-regulation by blue light of the expression of genes involved in GABA metabolism, nucleotide, iron, fatty acid, and polyamine metabolism and transport, and siderophores synthesis and transport. Previous reports have shown that these compounds are key players during the confrontation of PsPto with plant immunity (Kachroo and Kachroo, 2009;McCraw et al., 2016;Ryffel et al., 2016;Nobori et al., 2018;Vilas et al., 2018). Blue light was found to be related to an increase in plant defence against P. syringae (Wu and Yang, 2010). ...
Adaptation and efficient colonization of the phyllosphere are essential processes for the switch to an epiphytic stage in foliar bacterial pathogens. Here, we explore the interplay among light perception and global transcriptomic alterations in epiphytic populations of the hemibiotrophic pathogen Pseudomonas syringae pv. tomato DC3000 (PsPto) following contact with tomato leaves. We found that blue‐light perception by PsPto on leaf surfaces is required for optimal colonization. Blue light triggers the activation of metabolic activity and increases the transcript levels of five chemoreceptors through the function of light oxygen voltage and BphP1 photoreceptors. The inactivation of PSPTO_1008 and PSPTO_2526 chemoreceptors causes a reduction in virulence. Our results indicate that during PsPto interaction with tomato plants, light perception, chemotaxis, and virulence are highly interwoven processes. Blue light increases chemotaxis and metabolic activity in Pseudomonas syringae, permitting an optimal response to plant signals that facilitates bacterial plant entry.
... Overall, the polyamine Spm seems important for the establishment of HR and basal defense responses to hemibiotrophic pathogens in tobacco and Arabidopsis. Conversely, Put has not been observed to have such defense-promoting activities, although its content is remarkably increased in response to pathogens (Yoda et al., 2003;Mitsuya et al., 2009;Sagor et al., 2012;Vilas et al., 2018;Seifi and Shelp, 2019). ...
... Some polyamines have been reported to accumulate in the apoplast of Arabidopsis, tobacco, tomato, and rice during defense (Yoda et al., 2009;Vilas et al., 2018). Under basal conditions (0 h), the levels of free polyamines in the apoplastic enriched fractions were undetectable. ...
Polyamines are involved in defense against pathogenic microorganisms in plants. However, the role of the polyamine putrescine (Put) during plant defense has remained elusive. In this work, we studied the implication of polyamines during pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI) in the model species Arabidopsis thaliana. Our data indicate that polyamines, particularly Put, accumulate in response to non-pathogenic Pseudomonas syringae pv. tomato DC3000 hrcC and in response to the purified PAMP flagellin22. Exogenously supplied Put to Arabidopsis seedlings induces defense responses compatible with PTI activation, such as callose deposition and transcriptional up-regulation of several PTI marker genes. Consistent with this, we show that Put primes for resistance against pathogenic bacteria. Through chemical and genetic approaches, we find that PTI-related transcriptional responses induced by Put are hydrogen peroxide and NADPH oxidase (RBOHD and RBOHF) dependent, thus suggesting that apoplastic ROS mediates Put signaling. Overall, our data indicate that Put amplifies PTI responses through ROS production, leading to enhanced disease resistance against bacterial pathogens.
... The presence or absence of specific metabolites is related to resistance or susceptibility to pathogenic microorganisms (Garcia et al. 2023a ). For instance, quinolizidine alkaloids in lupins provide resistance against herbivores, but their absence in domesticated varieties led to increased susceptibility, highlighting the importance of secondary metabolites in plant breeding and the potential risks of losing these compounds during crop domestication (Lowe-Power et al. 2018, Vilas et al. 2018. Other studies showed that secondary metabolites increase plant resistance against pathogens due to the increase in plant defense compounds, such as glutathione, which functions as a redox buffer and participates in various enzymatic reactions, including detoxifying reactive oxygen species (ROS) (Gu et al. 2021, Yang et al. 2022. ...
As sessile organisms, plants are constantly exposed to various abiotic and biotic factors in their environment. Among the biotic factors, beneficial microorganisms, pathogens, and insects cause metabolic changes that affect growth and productivity. In response to these interactions and stress conditions, plants have developed sophisticated metabolic plasticity, adjusting their primary and secondary metabolic pathways. Secondary metabolites are specialized compounds that serve various ecological functions, such as defense against herbivores and pathogens, allelopathy, interaction with beneficial microorganisms, and attraction of pollinators and seed dispersers. These metabolites also act as signaling molecules in plant-microbe interactions, regulating the relationship between plants and microbes. Recent genetic and chemical research has revealed that secondary metabolites have multiple functions, acting as powerful regulators of both plant growth and defense beyond their roles in primary metabolism. This review explored the microbiome's complexity and emerging trends in understanding how microbiome composition and/or synthetic microbial community (SynCom) influence microbial and plant metabolic activities. Addressing the correlation between the varieties of microorganisms or SynCom and their metabolic profiles is crucial for elucidating the biological mechanisms that induce alterations in microbial communities and their metabolic functions within the rhizosphere and plant microbiomes. This knowledge will contribute to developing strategies to enhance beneficial interactions and mitigate the effects of pathogens that can reduce plant growth and productivity.
... Both plants and pathogens secrete PAs into the extracellular environment. P. syringae secretes Put into the host apoplast to promote virulence, suggesting its role in plant colonization [20,69] (Figure 2). Although the exact mechanism by which Put enhances P. syringae virulence is unclear, it is hypothesized that Put secretion may mitigate the effects of ROS produced by plant defense responses. ...
Polyamines (PAs), which are aliphatic polycationic compounds with a low molecular weight, are found in all living organisms and play essential roles in plant–pathogen interactions. Putrescine, spermidine, and spermine, the most common PAs in nature, respond to and function differently in plants and pathogens during their interactions. While plants use certain PAs to enhance their immunity, pathogens exploit PAs to facilitate successful invasion. In this review, we compile recent studies on the roles of PAs in plant–pathogen interactions, providing a comprehensive overview of their roles in both plant defense and pathogen pathogenicity. A thorough understanding of the functions of PAs and conjugated PAs highlights their potential applications in fungicide development. The creation of new fungicides and compounds derived from PAs demonstrates their promising potential for further research and innovation in this field.
... Pseudomonas Syringae It can increase the plant defense system. [220] Turmeric (Curcuma longa) Zingiberaceae ...
The application of biostimulants has been proven to be an advantageous tool and an appropriate form of management towards the effective use of natural resources, food security, and the beneficial effects on plant growth and yield. Plant-growth-promoting rhizobacteria (PGPR) are microbes connected with plant roots that can increase plant growth by different methods such as producing plant hormones and molecules to improve plant growth or providing increased mineral nutrition. They can colonize all ecological niches of roots to all stages of crop development, and they can affect plant growth and development directly by modulating plant hormone levels and enhancing nutrient acquisition such as of potassium, phosphorus, nitrogen, and essential minerals, or indirectly via reducing the inhibitory impacts of different pathogens in the forms of biocontrol parameters. Many plant-associated species such as Pseudomonas, Acinetobacter, Streptomyces, Serratia, Arthrobacter, and Rhodococcus can increase plant growth by improving plant disease resistance, synthesizing growth-stimulating plant hormones, and suppressing pathogenic microorganisms. The application of biostimulants is both an environmentally friendly practice and a promising method that can enhance the sustainability of horticultural and agricultural production systems as well as promote the quantity and quality of foods. They can also reduce the global dependence on hazardous agricultural chemicals. Science Direct, Google Scholar, Springer Link, CAB Direct, Scopus, Springer Link, Taylor and Francis, Web of Science, and Wiley Online Library were checked, and the search was conducted on all manuscript sections in accordance with the terms Acinetobacter, Arthrobacter, Enterobacter, Ochrobactrum, Pseudomonas, Rhodococcus, Serratia, Streptomyces, Biostimulants, Plant growth promoting rhizobactera, and Stenotrophomonas. The aim of this manuscript is to survey the effects of plant-growth-promoting rhizobacteria by presenting case studies and successful paradigms in various agricultural and horticultural crops.
... In this transcriptome analysis, transcript abundance of several genes implicated with polyamine biosynthesis and transport was significantly upregulated in the mutant strain. In phytopathogens, synthesis and secretion of putrescine was reported in R. solanacearum, P. syringae, and Dickeya zeae (116)(117)(118), which play an important role in alleviating the oxidative stress by scavenging the reactive oxygen species (119,120). Further, two genes (osmC and ompW) associated with osmotic stress were significantly downregulated in the mutant strain, which was in concordance with our previous result in which the tssM mutant displayed reduced growth when exposed to osmotic stress (57). ...
Type VI secretion system (T6SS) is a versatile, contact-dependent contractile nano-weapon in Gram-negative bacteria that fires proteinaceous effector molecules directly into prokaryotic and eukaryotic cells aiding in manipulation of the host and killing of competitors in complex niches. In plant pathogenic xanthomonads, T6SS has been demonstrated to play these diverse roles in individual pathosystems. However, the molecular network underlying the regulation of T6SS is still elusive in Xanthomonas spp. To bridge this knowledge gap, we conducted an in vitro transcriptome screen using plant apoplast mimicking minimal medium, XVM2 medium, to decipher the effect of tssM deletion, a core gene belonging to T6SS-cluster i3*, on the regulation of gene expression in Xanthomonas perforans strain AL65. Transcriptomic data revealed that a total of 277 and 525 genes were upregulated, while 307 and 392 genes were downregulated in the mutant strain after 8 and 16 hours of growth in XVM2 medium. The transcript abundance of several genes associated with flagellum and pilus biogenesis as well as type III secretion system was downregulated in the mutant strain. Deletion of tssM of cluster-i3* resulted in upregulation of several T6SS genes belonging to cluster-i3*** and genes involved in biofilm and cell wall biogenesis. Similarly, transcription regulators like rpoN , Pho regulon, rpoE , and csrA were identified to be upregulated in the mutant strain. Our results suggest that T6SS modulates the expression of global regulators like csrA , rpoN , and pho regulons, triggering a signaling cascade, and co-ordinates the expression of suite of virulence factors, stress response genes, and metabolic genes.
IMPORTANCE
T6SS has received attention due to its significance in mediating interorganismal competition through contact-dependent release of effector molecules into prokaryotic and eukaryotic cells. Reverse-genetic studies have indicated the role of T6SS in virulence in a variety of plant pathogenic bacteria, including the one studied here, Xanthomonas . However, it is not clear whether such effect on virulence is merely due to a shift in the microbiome-mediated protection or if T6SS is involved in a complex virulence regulatory network. In this study, we conducted in vitro transcriptome profiling in minimal medium to decipher the signaling pathways regulated by tssM-i3* in X. perforans AL65. We show that TssM-i3* regulates the expression of a suite of genes associated with virulence and metabolism either directly or indirectly by altering the transcription of several regulators. These findings further expand our knowledge on the intricate molecular circuits regulated by T6SS in phytopathogenic bacteria.
... In this transcriptome analysis, transcript abundance of several genes implicated with polyamine biosynthesis and transport were significantly upregulated in the mutant strain. In phytopathogens, synthesis and secretion of putrescine was reported in R. solanacearum, P. syringae, and Dickeya zeae (103)(104)(105), which play an important role in alleviating the oxidative stress by scavenging the . CC-BY-NC-ND 4.0 International license made available under a (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. ...
Type VI secretion system (T6SS) is a versatile, contact dependent contractile nano-weapon in Gram-negative bacteria that fires proteinaceous effector molecules directly into prokaryotic and eukaryotic cells aiding in manipulation of the host and killing of competitors in complex niches. In plant pathogenic xanthomonads, T6SS has been demonstrated to play these diverse roles in individual pathosystems. However, the regulatory circuit involved in mediating biological functions carried out by T6SS are still elusive in Xanthomonas sp. To bridge this knowledge gap, we conducted an in vitro transcriptome screen using plant apoplast mimicking minimal medium, XVM2 medium, to decipher the effect of tssM deletion, a core gene belonging to T6SS-cluster i3*, on the regulation of gene expression in Xanthomonas perforans strain AL65. Transcriptomic data revealed that a total of 277 and 525 genes were upregulated, while 307 and 392 genes were downregulated in the mutant strain post 8 and 16 hours of growth in XVM2 medium. The transcript abundance of several genes associated with flagellum and pilus biogenesis as well as type III secretion system were downregulated in the mutant strain. Deletion of tssM of cluster-i3* resulted in upregulation of several T6SS genes belonging to cluster-i3*** and genes involved in biofilm and cell wall biogenesis. Similarly, transcription regulators like rpoN , Pho regulon, rpoE and csrA were identified to be upregulated in the mutant strain. Our results suggest that T6SS modulates the expression of global regulators like csrA , rpoN and pho regulons triggering a signaling cascade and co-ordinates the expression of suite of virulence factors, stress response genes and metabolic genes.
Importance
Type VI secretion system (T6SS) has received attention due to its significance in mediating inter-organismal competition through contact-dependent release of effector molecules into prokaryotic and eukaryotic cells. Reverse-genetic studies targeting core genes of T6SS have indicated the role of T6SS in virulence in a variety of plant pathogenic bacteria, including Xanthomonas studied here. However, it is not clear whether such effect on virulence is merely because of a shift in the microbiome-mediated protection or if T6SS is involved in a complex regulatory network governing virulence in plant pathogens involving type III secretion system or c-di-GMP signaling pathways. In this study, we conducted in vitro transcriptome profiling in minimal medium to decipher the signaling pathways regulated by tssM -i3* in Xanthomonas perforans strain AL65. We show that TssM-i3* regulates the expression of a suite of genes associated with virulence and metabolism either directly or indirectly by altering the transcription of several regulators. These findings further expand our knowledge on the intricate molecular circuits regulated by T6SS in phytopathogenic bacteria.
... Amino acids are another group of the primary metabolites involved in the induction of plant defense responses biochemically related to the polyamine metabolism (Vilas et al. 2018). Alterations in polyamines metabolism can influence the amino acid levels in plant cells (Majumdar et al. 2016). ...
Polyamines, as regulatory compounds, contribute to plant growth, development, and defense responses. Despite attempts to elucidate polyamines effect on the secondary metabolites biosynthesis, their functional roles require further investigation. Here, the role of putrescine on the lignans production and different signaling and metabolic pathways modulation has been investigated in Linum album hairy roots. Our results revealed that putrescine affects the oxidative status of cells by increasing the hydrogen peroxide (H2O2) and malondialdehyde (MDA) levels, and activating superoxide dismutase (SOD), catalase (CAT) and peroxidases (POD) enzymes. Besides, nitric oxide (NO) content augmented during the first hours of the treatment with putrescine. Metabolic assays suggest that putrescine treatment shifts energy and metabolic flows, via changing the carbohydrates and amino acids biosynthesis, towards the phenolics production. Putrescine-induced activation of phenylalanine ammonia lyase (PAL) and tyrosine ammonia lyase (TAL) occurred, likely via the H2O2 and NO signaling pathways. The activation of the PAL and TAL enzymes ultimately led to an increase in phenolic acids, which either play a regulatory role or are precursors to other phenolic compounds such as flavonoids and lignans. The general assumption is that putrescine regulates the lignan biosynthesis by inducing signaling pathways, altering oxidative status, and modifying metabolite profiles in L. album hairy roots.
... To explain this observation, it should be considered that free Spd could have different sources. For instance, it might be residual Spd absorbed during the preparation of the inocula in LB, which contains polyamines in its composition 24 . An alternative explanation consists in the release of free Spd from the fraction that exists conjugated to organic compounds 25,26 . ...
Bacterial phytopathogens thriving in the surface or the interior of plants may experience oxidative stress because of the activation of plant defense responses. Polyamines have been proposed to participate in the protection of bacteria against this stress, but the mechanisms behind their functions are mostly unclear. In this study, we sought to understand the effects of oxidative stress on the polyamine homeostasis of the plant pathogen Pseudomonas syringae and decipher the functions of these compounds in stress tolerance. We showed that bacteria react to H 2 O 2 by raising the extracellular amount of the polyamine putrescine while the intracellular levels of this compound as well as the analogue spermidine remained unchanged. Consistent with this, supplementation of media with exogenous putrescine enhanced bacterial tolerance to H 2 O 2 . Deletion of arginine decarboxylase ( speA ) and ornithine decarboxylate ( speC ), prevented the synthesis of putrescine and augmented susceptibility to H 2 O 2 , whereas targeting spermidine synthesis alone through deletion of spermidine synthase ( speE ) increased the level of extracellular putrescine and enhanced H 2 O 2 tolerance. Further research demonstrated that the increased tolerance of the ΔspeE mutant correlated both with increased expression of H 2 O 2 -degrading catalases and enhanced outer cell membrane stability. Thus, this work demonstrates previously unidentified links between the metabolism of polyamines and the defense against oxidative stress in bacteria.
... When attacked by pathogens, a host activates a large number of gene expression and metabolic pathways to cope with the biotic stress [4]. Plants respond to pathogen attack by modifying their defense gene expression and inducing the production of myriad proteins and metabolites [5]. During the constant 3 interaction between plants and pathogens, a compatible response leads to pathogen invasion and disease development, while an incompatible response ignites the plant's immune system and prevents pathogen invasion. ...
A plant’s early response to pathogen stress is a vital indicator of its disease resistance. In order to study the response mechanism of resistant and susceptible flax cultivars to Fusarium oxysporum f. sp. lini (Foln), we applied RNA-sequencing to analyze transcriptomes of flax with Foln 0.5, 2 and 8 hours post inoculation (hpi). We found a significant difference in the number of differential expression genes (DEGs) between resistant and susceptible flax clutivars. The number of DEGs in the Fusarium-resistant cultivar increased dramatically at 2 hpi, and a large number of DEGs participated in the Fusarium-susceptible cultivar response to Foln infection 0.5 hpi. GO enrichment analysis determined that the up-regulated DEGs of both flax cultivars were enriched such as oxidoreductase activity and oxidation-reduction process. At the same time, the genes involved in diterpenoid synthesis were up-regulated in resistant cultivar, while those involved in extracellular region, cell wall and organophosphate ester transport were down-regulated in susceptible cultivar. KEGG enrichment analysis showed the genes encoded WRKY 22 and WRKY33 which involved in MAPK signaling pathway were up-regulated expressed in S-29 and down-regulated expressed in R-7, negatively regulated the disease resistance of flax; The genes encoded Hsp 90 family which in involved in plant pathogen interaction pathway were up-regulated in R-7 and down-regulated in S-29, which positively regulated the disease resistance of flax; The genes encoded MYC2 transcription factor and TIFY proteins which involved in plant hormone signaling pathway were up-regulated in R-7, and regulated the jasmonic acid metabolism of flax and the signal transduction of plant hormones. Meanwhile seven regulatory genes with the most correlation were screened out, Among Lus10025000.g and Lus10026447.g regulated other genes expressed both in plant hormone signal transduction pathway and MAPK signal pathway. In conclusion, these findings will facilitate further studies on the function of these candidate genes in flax of response to Fusarium stress, and the breeding of disease-resistant flax cultivar.
... The intermediate agmatine is further converted to putrescine via N-carbamoyl-putrescine using agmatine deiminase (EC 3.5.3.12) and N-carbamoyl-putrescine amidase (EC 3.5.1.53) (Michael, 2016;Vilas et al., 2018). Finally, strain 169 contained genes for the conversion of putrescine to spermidine (speE). ...
Plant-associated Stenotrophomonas isolates have great potential for plant growth promotion, especially under stress conditions, due to their ability to promote tolerance to abiotic stresses such as salinity or drought. The endophytic strain Stenotrophomonas sp. 169, isolated from a field-grown poplar, increased the growth of inoculated in vitro plants, with a particular effect on root development, and was able to stimulate the rooting of poplar cuttings in the greenhouse. The strain produced high amounts of the plant growth-stimulating hormone auxin under in vitro conditions. The comparison of the 16S rRNA gene sequences and the phylogenetic analysis of the core genomes showed a close relationship to Stenotrophomonas chelatiphaga and a clear separation from Stenotrophomonas maltophilia . Whole genome sequence analysis revealed functional genes potentially associated with attachment and plant colonization, growth promotion, and stress protection. In detail, an extensive set of genes for twitching motility, chemotaxis, flagella biosynthesis, and the ability to form biofilms, which are connected with host plant colonization, could be identified in the genome of strain 169. The production of indole-3-acetic acid and the presence of genes for auxin biosynthesis pathways and the spermidine pathway could explain the ability to promote plant growth. Furthermore, the genome contained genes encoding for features related to the production of different osmoprotective molecules and enzymes mediating the regulation of stress tolerance and the ability of bacteria to quickly adapt to changing environments. Overall, the results of physiological tests and genome analysis demonstrated the capability of endophytic strain 169 to promote plant growth. In contrast to related species, strain 169 can be considered non-pathogenic and suitable for biotechnology applications.
... Overall, most defense traits related to polyamines have been attributed to Spm oxidation. Even though Put accumulation is a conserved metabolic hallmark of plant stress, the contribution of Put to defense has remained elusive (Mitsuya et al., 2009;Sagor et al., 2012;Vilas et al., 2018;Yoda, Yamaguchi, & Sano, 2003). We recently reported that Put accumulates during PTI and amplifies PTI responses in a ROS and RESPIRATORY BURST OXIDASE HOMOLOG (RBOH) D and RBOHF-dependent manner (Liu, Atanasov, Tiburcio, & Alcázar, 2019). ...
Polyamines are small amines that accumulate during stress and contribute to disease resistance through as yet unknown signaling pathways. Using a comprehensive RNA‐sequencing analysis, we show that early transcriptional responses triggered by each of the most abundant polyamines (putrescine, spermidine, spermine, thermospermine and cadaverine) exhibit specific quantitative differences, suggesting that polyamines (rather than downstream metabolites) elicit defense responses. Signaling by putrescine, which accumulates in response to bacteria that trigger effector triggered immunity (ETI) and systemic acquired resistance (SAR), is largely dependent on the accumulation of hydrogen peroxide, and is partly dependent on salicylic acid (SA), the expression of ENHANCED DISEASE SUSCEPTIBILITY (EDS1) and NONEXPRESSOR of PR GENES1 (NPR1). Putrescine elicits local SA accumulation as well as local and systemic transcriptional reprogramming that overlaps with SAR. Loss‐of‐function mutations in arginine decarboxylase 2 (ADC2), which is required for putrescine synthesis and copper amine oxidase (CuAO), which is involved in putrescine oxidation, compromise basal defenses, as well as putrescine and pathogen‐triggered systemic resistance. These findings confirm that putrescine elicits ROS‐dependent SA pathways in the activation of plant defenses.
... Leaves were adapted to dark before measurement during 20 min and exposed to a light intensity of 3500 μmol m −2 s −1 for 3 s. Parameters derived from the OJIP test (O: Initial fluorescence, at 50 μs or less, J-I: intermediate levels at 2 ms and 30 ms, P: maximal fluorescence) were analysed in order to characterize the status of the photosystem II (PSII) in plants as described by Vilas et al. (2018): Fv/Fm (Φ Po ), Maximum quantum yield of the primary photochemistry; PIabs, Performance Index on the Absorption Basis; ABS, contribution of the absorption of light energy; Sm, normalized total complementary area above the OJIP transient; TRo, trapping of excitation energy, ETo, conversion of excitation energy to electron transport; DIo, Dissipation flux; RC, reaction centre, CSo, Cross section; Ψ Eo , Electron transport from quinone a to plastoquinone efficiency; Φ Eo , maximum yield of electron transport from Qa to plastoquinone primary photochemistry. ...
The interactions established between plants and endophytic fungi span a continuum from beneficial to pathogenic associations. The aim of this work was to isolate potentially beneficial fungal endophytes in the legume Lotus tenuis and explore the mechanisms underlying their effects. One of the nine fungal strains isolated was identified as Fusarium solani and shows the highest phosphate-solubilisation activity, and also grows endophytically in roots of L. japonicus and L. tenuis. Interestingly, fungal invasion enhances plant growth in L. japonicus but provokes a contrasting effect in L. tenuis. These differences were also evidenced when the rate of photosynthesis as well as sugars and K contents were assessed. Our results indicate that the differential responses observed are due to distinct mechanisms deployed during the establishment of the interactions that involve the regulation of photosynthesis, potassium homeostasis, and carbohydrate metabolism. These responses are employed by these plant species to maintain fitness during the endophytic interaction.
Microbial infections have been a widely studied area of disease research since historical times, yet they are a cause of severe illness and deaths worldwide. Furthermore, infections by pathogens are not just restricted to humans; instead, a diverse range of hosts, including plants, livestock, marine organisms and fish, cause significant economic losses and pose threats to humans through their transmission in the food chain. It is now believed that both the pathogen and the host contribute to the outcomes of a disease pathology. Researchers have unravelled numerous aspects of host-pathogen interactions, offering valuable insights into the physiological, cellular and molecular processes and factors that contribute to the development of infectious diseases. Polyamines are key factors regulating cellular processes and human ageing and health. However, they are often overlooked in the context of host-pathogen interactions despite playing a dynamic role as a defence molecule from the perspective of the host as well as the pathogen. They form a complex network interacting with several molecules within the cell, with reactive oxygen species being a key component. This review presents a thorough overview of the current knowledge of polyamines and their intricate interactions with reactive oxygen species in the infection of multiple pathogens in diverse hosts. Interestingly, the review covers the interplay of the commensals and pathogen infection involving polyamines and reactive oxygen species, highlighting an unexplored area within this field. From a future perspective, the dynamic interplay of polyamines and oxidative stress in microbial pathogenesis is a fascinating area that widens the scope of developing therapeutic strategies to combat deadly infections.
AimsSugarcane plants infected with Leifsonia xyli subsp. xyli (Lxx) have their primary metabolism affected with decreased levels of sugars and amino acids. Cysteine and methionine are sulfur-containing essential amino acids used for bacterial growth and the Lxx titer in sugar cane leaves could affect the animo acid concentrations. The goal of this study was to evaluate how the increase in Lxx titer affects the nutritional status and sulfur metabolism in sugar cane leaves.Methods
Susceptible sugar cane (Saccharum officinarum) genotype: CB49260 was used in this study with low (256 cells) and high (2090 cells) Lxx titers and macronutrients and primary metabolites assessed from leaves and culms.ResultsPlants with high Lxx titers accumulated more biomass in the main culm, leaves, and shoots than plants with low Lxx titers. Additionally, plants with high Lxx titers had 26% more sulfur content in leaves than plants with low Lxx titers. Higher levels of sulfate, sucrose, maltose, raffinose, shikimic acid, malate, putrescine, glycerol, and, erythritol were also present in plants with high Lxx titers; but decreased levels of methionine and glutathione in leaves. In the culm, plants with high Lxx titers also had increased levels of maltose; but decreased levels of threonine, ornithine, phenylalanine and myo-inositol when compared with plants with low Lxx titers.Conclusions
This study demonstrated that high bacterial titers increase sulfur demand in sugar cane; however, the increased S content in the leaf did not result in higher sulfur assimilation, verified by increased sulfate but decreased methionine and glutathione levels. Therefore, our study showed that lower methionine availability, and methionine catabolism to putrescine in the leaves may fail to meet the increased sulfur organic compound demand of Lxx. The decrease in glutathione biosynthesis may reflect impaired biosynthesis or a drain on this antioxidant resulting from oxidative stresss by pathogenesis of Lxx.
Crop production is significantly dwindled by a plenitude of pathogens that deprive the host plants of nutrients, alter their physiological processes, and ultimately reduce yield. In order to combat biotic stress and enhance their survival, plants have evolved innate immunity which recognizes the presence of pathogens and stimulates defense responses via PAMP-triggered immunity and effector-triggered immunity. The successful activation of plant immune responses and subsequent pathogen defense is governed by an interplay of various phytohormones and signaling molecules of which the role of salicylic acid, jasmonic acid, and ethylene, among others, is well established. In addition, a growing body of evidence also suggests a key role of polyamines (PAs) in the regulation of plant immune responses. Based on the literature evidence, it can be concluded that plants capable of synthesizing PAs during the initial stages of pathogen invasion exhibit resistance, and the PAs so produced are later catabolized to synthesize other signaling molecules such as H2O2 which is required to initiate hypersensitive response induced cell death. This review encapsulates the metabolism of PAs and their role in the amelioration of biotic stresses induced by various pests and pathogens. Further, the crosstalk of PAs with different signaling molecules in modulating the defense system in host plants in response to biotic stress is also presented.
Polyamines (PAs) are ubiquitous amine molecules found in all living organisms. In plants, beside their role in signaling and protection against abiotic stresses, there is increasing evidence that PAs have a major role in the interaction between plants and pathogens. Plant PAs are involved in immunity against pathogens, notably by amplifying pattern-triggered immunity (PTI) responses through the production of reactive oxygen species (ROS). In response, pathogens use phytotoxins and effectors to manipulate the levels of PAs in the plant, most likely to their own benefit. It also appears that pathogenic microorganisms produce PAs during infection, sometimes in large quantities. This may reflect different infectious strategies based on the selective exploitation of these molecules and the functions they perform in the cell.
A specialized group of aliphatic polycations is referred to as polyamines distributed ubiquitously in prokaryotic and eukaryotic organisms. Free polyamines as well as conjugated polyamines are found in living cells. In plants, polyamines are synthesized from arginine via two alternative pathways. Plants have well-organized transport system for polyamine conduction. Among the wide range of physiological functions of polyamines, stress response is an important one. Plants have evolved a variety of mechanisms to recognize distinct stimuli for the alteration of the gene expression in response to different types of stresses (Hatmi et al. Osmotic stress and ABA affect immune response and susceptibility of grapevine berries to gray mold by priming polyamine accumulation. Front Plant Sci 65:75–88. https://doi.org/10.3389/fpls.2018.01010, 2018). Often, partially overlapping sets of responses are activated in different stress conditions, and several points of crosstalk exist between abiotic and biotic stress responses. Rice, an important food grain of South Asian countries, has been confronted with several stresses in the field of agriculture. Destructive pathogenic attack is one of the major challenges for their survival and good production. Apart from the conventional chemical treatment, modulation of genes for polyamine biosynthesis and expression might be a worthwhile means of solution for this problem. Considering the preventive role of polyamines during microbial infection, scientists are now trying to develop resistant varieties with the help of genetic engineering. In the present review, some relevant aspects are talked over to find out some cues about the detailing of the respective gene expression regarding this particular issue.
Microbial immobilization is a novel and environmentally friendly technique in which microbes are used to immobilize heavy metals in the soil. Polyamine-production screening media and high-pressure liquid chromatography were used to isolate polyamine-producing bacteria from Cd- and Pb-polluted rhizosphere soil of lettuce. Enhancement of lettuce growth and reduced accumulation of Cd and Pb in lettuce by the polyamine-producing strains were investigated. Two polyamine-producing bacteria Bacillus megaterium N3 and Enterobacter bugandensis XY7 were obtained by screening. The Cd and Pb removal rates of strains N3 and XY7 ranged from 73.5% to 87.6% in solution containing 1 mg L⁻¹ Cd²⁺ and 5 mg L⁻¹ Pb²⁺. Strains N3 and XY7 increased the dry weight (22.2%-66.7%), improved the polyamines contents and reduced the Cd (57.3%-74.2%) and Pb (44.1%-62.9%) contents of lettuce. Moreover, the strains decreased the bioavailable Cd (27.1%-62.1%) and Pb (35.4%-73.7%) contents but increased polyamines contents and the relative abundance of aguA gene in lettuce rhizosphere soil. The results suggested that strains N3 and XY7 decreased the uptake of Cd and Pb and their translocation into lettuce shoots by i) bacterial cell adsorption, ii) chelation of polyamines to Cd and Pb, iii) decreasing available Cd and Pb in the rhizosphere soil and Cd and Pb translocation from the roots to the shoots, and iv) increasing the polyamine contents and the relative abundance of aguA gene in lettuce rhizosphere soil. Our findings may provide technical support for the remediation of heavy metal contaminated farmlands by bacteria and for safe growth of vegetables crop species.
Polyamines (PAs) are small aliphatic amines with important regulatory activities in plants. Biotic stress results in changes in PA levels due to de novo synthesis and PA oxidation. In Arabidopsis thaliana five FAD-dependent polyamine oxidase enzymes (AtPAO1-5) participate in PA back-conversion and degradation. PAO activity generates H2O2, an important molecule involved in cell signaling, elongation, programmed cell death, and defense responses. In this work we analyzed the role of AtPAO genes in the Arabidopsis thaliana-Pseudomonas syringae pathosystem. AtPAO1 and AtPAO2 genes were transcriptionally up-regulated in infected plants. Atpao1-1 and Atpao2-1 single mutant lines displayed altered responses to Pseudomonas, and an increased susceptibility was found in the double mutant Atpao1-1 x Atpao2-1. These polyamine oxidases mutant lines showed disturbed contents of ROS (H2O2 and O2-) and altered activities of RBOH, CAT and SOD enzymes both in infected and control plants. In addition, changes in the expression levels of AtRBOHD, AtRBOHF, AtPRX33, and AtPRX34 genes were also noticed. Our data indicate an important role for polyamine oxidases in plant defense and ROS homeostasis.
Three tri-substituted spermidines, di-p-coumaroyl-caffeoylspermidine, tri-caffeoylspermidine and tri-p-coumaroylspermidine, isolated from pollen of Quercus alba, were examined for antifungal activity. Both di-p-coumaroyl-caffeoylspermidine and tri-p-coumaroylspermidine reduced mycelial growth of the oat leaf stripe pathogen, Pyrenophora avenae and reduced powdery mildew (Blumeria graminis f. sp. hordei) infection of barley seedlings when applied as a post-inoculation treatment. When used as a pre-inoculation treatment, only di-p-coumaroyl-caffeoylspermidine reduced powdery mildew infection significantly. Growth of P. avenae in the presence of 100 μM di-p-coumaroyl-caffeoylspermidine reduced activity of S-adenosylmethionine decarboxylase (AdoMetDC), and led to a reduction in the incorporation of labelled ornithine into spermidine. The other two spermidine conjugates increased AdoMetDC activity and the flux label from ornithine into spermine in P. avenae significantly.