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Relative abundance of TF genes differentially regulated upon mycorrhization in tomato. Percentage of AM-repressed and AM-induced TF genes, with RNA-seq fold change <− or > 2 and p < 0.05, belonging to each TF gene family in tomato.
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The formation and functioning of arbuscular mycorrhizal (AM) symbiosis are complex and tightly regulated processes. Transcriptional regulation mechanisms have been reported to mediate gene expression changes closely associated with arbuscule formation, where nutrients move between the plant and fungus. Numerous genes encoding transcription factors...
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Citations
... GRAS proteins are involved in the regulation of defensive responses in tomato, as these proteins are induced in resistant tomato plants after pathogen attack [23,132]. Also, GRAS tomato genes are upregulated upon mycorrhization [133]. On the other hand, DELLA proteins are also related to defence against abiotic stress, such as salt stress in Arabidopsis [73]. ...
Understanding the resistance mechanisms of plants against pests contributes to the sustainable deployment of plant resistance in Integrated Pest Management (IPM) programmes. The Mi-1 gene in tomato is the only one described with the capacity to provide resistance to different types of harmful organisms such as plant parasitic nematodes and pest insects, including the whitefly Bemisia tabaci MED (Mediterranean species). In this work, gene expression in the interaction of B. tabaci with susceptible tomato plants lacking the Mi-1 gene (cv. Moneymaker, compatible interaction), and with resistant plants carrying the Mi-1 gene (cv. Motelle, incompatible interaction) was studied using the oligonucleotide microarray technique. Both interactions were studied 2 and 12 days post infestation (dpi) of plants with adult insects. At 2 dpi, 159 overexpressed and 189 repressed transcripts were detected in the incompatible interaction, while these figures were 32 and 47 in the compatible one. Transcriptional reprogramming was more intense at 12 dpi but, as at 2 dpi, the number of transcripts overexpressed and repressed was higher in the incompatible (595 and 437, respectively) than in the compatible (71 and 52, respectively) interaction. According to the Mapman classification, these transcripts corresponded mainly to genes in the protein and RNA categories, some of which are involved in the defence response (signalling, respiratory burst, regulation of transcription, PRs, HSPs, cell wall or hormone signalling). These results provide a wealth of information about possible genes related to the resistance provided by the Mi-1 gene to B. tabaci, and whose role deserves further investigation.
... Genome-wide identification, expression analysis, and functional characterization of GRAS family genes under AM symbiosis are explored in mycorrhizal plants, like M. truncatula [26], L. japonicus [27], and S. lycopersicum [28], and a large number of GRAS genes are involved in the AM symbiosis process, including RAD1, RAM1, NSP1, NSP2, MIG1, and DELLA, and these genes play various roles in the AM fungi induced cascade signaling pathway, which is essential for the signaling dialogue and the establish of reciprocal symbiosis between plant and AM fungi [17,27,29,30]. Recently, novel mycorrhizal symbiosis regulatory GRAS transcription factors have been identified. ...
... Among them, two key regulatory factors of the AM symbiosis signaling pathway in M. truncatula, MtRAM1, and MtRAD1 were identified, which were reported to regulate arbuscular formation and nutrient exchange between AM fungi and host plants by forming protein complex, and inducing downstream AM-related genes [18,20]. According to the previous studies, the branch of RAD1 and RAM1 was absent in the whole non-AM host Brassicaceae family, suggesting this branch was AM-specific branch [28,43]. Notably, PtGRAS6, PtGRAS12, PtGRAS18, and PtGRAS40 were identified in this branch, indicating that these four genes might play significant roles in AM symbiosis in P. trifoliata. ...
Arbuscular mycorrhizal (AM) fungi establish mutualistic symbiosis with most land plants, facilitating mineral nutrient uptake in exchange for photosynthates. As one of the most commercially used rootstocks in citrus, Poncirus trifoliata heavily depends on AM fungi for nutrient absorption. The GRAS gene family plays essential roles in plant growth and development, signaling transduction, and responses to biotic and abiotic stresses. However, the identification and functional characterization of GRAS family genes in P. trifoliata remains largely unexplored. In this study, a comprehensive genome-wide analysis of PtGRAS family genes was conducted, including their identification, physicochemical properties, phylogenetic relationships, gene structures, conserved domains, chromosome localization, and collinear relationships. Additionally, the expression profiles and protein interaction of these genes under AM symbiosis were systematically investigated. As a result, 41 GRAS genes were identified in the P. trifoliata genome, and classified into nine distinct clades. Collinearity analysis revealed seven segmental duplications but no tandem duplications, suggesting that segmental duplication played a more important role in the expansion of the PtGRAS gene family compared to tandem duplication. Additionally, 18 PtGRAS genes were differentially expressed in response to AM symbiosis, including orthologs of RAD1, RAM1, and DELLA3 in P. trifoliata. Yeast two-hybrid (Y2H) screening further revealed that PtGRAS6 and PtGRAS20 interacted with both PtGRAS12 and PtGRAS18, respectively. The interactions were subsequently validated through bimolecular fluorescence complementation (BiFC) assays. These findings underscored the crucial role of GRAS genes in AM symbiosis in P. trifoliata, and provided valuable candidate genes for improving nutrient uptake and stress resistance in citrus rootstocks through molecular breeding approaches.
... The release of chitinaceous molecules (Myc-LCOs) by AM fungi, which are detected by specific LysM receptor-like kinases (LysM-RLKs) located in the plasma membrane of the host plant cell, is essential for the onset of molecular signaling leading to host colonization (Ho-Plágaro and García-Garrido, 2022). It has been shown that several TFs including CCaMK, CYCLOPS, GRAS, DELLA, MIG1, SCL3, and RAM1 influence the transcriptional regulatory network which facilitates the hosting and development of arbuscules in the host plant (Ho-Plágaro et al., 2019). ...
... Previously characterized ram1 mutants showed reduced arbuscular branching and colonization across several plant species (Gobbato et al., 2012;Park et al., 2015;Rich et al., 2017;Müller et al., 2020). The tomato SlRAM1 (SlGRAS27) characterized in this study was initially reported as one of the GRAS tomato genes up-regulated upon mycorrhization (Ho-Plágaro et al., 2019). In this study, plants with SlRAM1-silenced roots colonized with the AM fungus Rhizophagus irregularis (Ri) showed a significant reduction in mycorrhization parameters including the percentage of total root length colonization and the prevalence of different types of arbuscules, as well as a decreased gene expression of the AM-associated phosphate transporter gene (SlPT4), suggesting SlGRAS27 as the putative RAM1 ortholog in tomato (Ho-Plágaro et al., 2024). ...
This article comments on:
Ho-Plágaro T, Tamayo-Navarrete MI, Ćavar Zeljković S, Tarkowski P, García-Garrido JM. 2024. A dual regulatory role of the arbuscular mycorrhizal master regulator RAM1 in tomato. Journal of Experimental Botany 75, 5021–5036. https://doi.org/10.1093/jxb/erae210
... Response to drought, Jasmonic acid signalling, and Auxin signalling process pathways; Table S11. The available literature from the investigated transcription factor and stress enzyme genes showed a significant expression change, detailed in Figures 7 and 8 [96]. Figure S1. ...
In this study, we report the interaction between an arbuscular mycorrhizal fungus, Septoglomus constrictum, and tomato plants under heat stress. For the first time, this interaction was studied by Illumina RNA-seq, followed by a comprehensive bioinformatic analysis that investigated root and leaf tissue samples. The genome-wide transcriptional profiling displayed fewer transcriptomic changes in the root under heat-stress conditions caused by S. constrictum. The top 50 DEGs suggested significant changes in the expression of genes encoding heat-shock proteins, transporter proteins, and genes of phytohormone metabolism involving jasmonic acid signalling. S. constrictum induced the upregulation of genes associated with pathways such as ‘drought-responsive’ and the ‘development of root hair’ in the root, as well as ‘glycolipid desaturation’, ‘intracellular auxin transport’, and ‘ethylene biosynthesis’ in the leaf. The pathways ‘biotin biosynthesis’ and ‘threonine degradation’ were found in both investigated tissue types. Expression analysis of transcription factors showed 2 and 11 upregulated transcription factors in heat-stressed root and leaf tissues, respectively. However, we did not find shared transcription factors. Heat-stressed arbuscular mycorrhizal plants suffered less oxidative stress when exposed to high temperatures. Colorimetric tests demonstrated less accumulation of H2O2 and MDA in heat-stressed mycorrhizal plants. This phenomenon was accompanied by the higher expression of six stress genes that encode peroxidases, glutathione S-transferase and ubiquitin carboxyl-terminal hydrolase in roots and leaves. Our findings provide a new perspective on elucidating the functional metabolic processes of tomato plants under mycorrhizal-heat stressed conditions.
... Among the AM-induced tomato GRAS TFs, Ho-Plágaro et al. (2019) identified putative orthologues to genes with a previously established functionality in AM regulation in other plant species, including the clades NSP2, RAM1, RAD1, LISCL, and the AM-host exclusive clade SCLB, which includes the MIG1 transcription factor (Maillet et al., 2011;Gobbato et al., 2012;Yu et al., 2014;Fiorilli et al., 2015;Xue et al., 2015;Heck et al., 2016;Rich et al., 2017;Ho-Plágaro et al., 2019). SlGRAS27 (SlRAM1), which is also a GRAS gene induced upon mycorrhization and expressed in arbuscule-containing cells, was characterized as the putative homologue of MtRAM1 and PhATA/RAM1 from Medicago and Petunia, respectively (Ho-Plágaro et al., 2019). ...
... Among the AM-induced tomato GRAS TFs, Ho-Plágaro et al. (2019) identified putative orthologues to genes with a previously established functionality in AM regulation in other plant species, including the clades NSP2, RAM1, RAD1, LISCL, and the AM-host exclusive clade SCLB, which includes the MIG1 transcription factor (Maillet et al., 2011;Gobbato et al., 2012;Yu et al., 2014;Fiorilli et al., 2015;Xue et al., 2015;Heck et al., 2016;Rich et al., 2017;Ho-Plágaro et al., 2019). SlGRAS27 (SlRAM1), which is also a GRAS gene induced upon mycorrhization and expressed in arbuscule-containing cells, was characterized as the putative homologue of MtRAM1 and PhATA/RAM1 from Medicago and Petunia, respectively (Ho-Plágaro et al., 2019). ...
... Among the AM-induced tomato GRAS TFs, Ho-Plágaro et al. (2019) identified putative orthologues to genes with a previously established functionality in AM regulation in other plant species, including the clades NSP2, RAM1, RAD1, LISCL, and the AM-host exclusive clade SCLB, which includes the MIG1 transcription factor (Maillet et al., 2011;Gobbato et al., 2012;Yu et al., 2014;Fiorilli et al., 2015;Xue et al., 2015;Heck et al., 2016;Rich et al., 2017;Ho-Plágaro et al., 2019). SlGRAS27 (SlRAM1), which is also a GRAS gene induced upon mycorrhization and expressed in arbuscule-containing cells, was characterized as the putative homologue of MtRAM1 and PhATA/RAM1 from Medicago and Petunia, respectively (Ho-Plágaro et al., 2019). Here we report a functional analysis of the SlRAM1 gene using RNAi and overexpressing (OE) hairy root composite tomato plants. ...
The REQUIRED FOR ARBUSCULAR MYCORRHIZATION1 (RAM1) transcription factor from the GRAS family is well-known by its role as a master regulator of the arbuscular mycorrhizal (AM) symbiosis in dicot and monocot species, being essential in the transcriptional reprograming for the development and functionality of the arbuscules. In tomato, SlGRAS27 is the putative ortholog of RAM1 (here named SlRAM1), but has not yet been characterized. A reduced colonization of the root and an impaired arbuscule formation were observed in the SlRAM1 silenced plants, confirming the functional conservation of the RAM1 ortholog in tomato . However, unexpectedly, SlRAM1 overexpressing (UBIL:SlRAM1) plants also showed a decreased mycorrhizal colonization. Analysis of non-mycorrhizal UBIL:SlRAM1 roots revealed an overall regulation of AM-related genes and a reduction of strigolactone biosynthesis. Moreover, the external application of the strigolactone analogue GR244DO almost completely reversed the negative effects of SlRAM1 overexpression on the frequency of mycorrhization. However, it only partially recovered the pattern of arbuscule distribution observed in control plants. Our results strongly suggest that SlRAM1 has a dual regulatory role during mycorrhization and, apart from its recognized action as a positive regulator of arbuscule development, SlRAM1 is also involved in different mechanisms for the negative regulation of mycorrhization, including the repression of strigolactone biosynthesis.
... The literature data are limited, and there is no information about DEGs that coincide in GO with those identified in our work and expressed in leaves. But earlier it was shown that genes belonging to the GRAS family and playing a role in cell division (such as SHR, SCR, SCL3, etc.) were induced in roots of Solanum lycopersicum during mycorrhization with R. irregularis [69]. ...
The study is aimed at revealing the effects of Rhizophagus irregularis inoculation on the transcriptome of Medicago lupulina leaves at the early (second leaf formation) and later (flowering) stages of plant development. A pot experiment was conducted under conditions of low phosphorus (P) level in the substrate. M. lupulina plants were characterized by high mycorrhizal growth response and mycorrhization parameters. Library sequencing was performed on the Illumina HiseqXTen platform. Significant changes in the expression of 4863 (padj < 0.01) genes from 34049 functionally annotated genes were shown by Massive Analysis of cDNA Ends (MACE-Seq). GO enrichment analysis using the Kolmogorov–Smirnov test was performed, and 244 functional GO groups were identified, including genes contributing to the development of effective AM symbiosis. The Mercator online tool was used to assign functional classes of differentially expressed genes (DEGs). The early stage was characterized by the presence of six functional classes that included only upregulated GO groups, such as genes of carbohydrate metabolism, cellular respiration, nutrient uptake, photosynthesis, protein biosynthesis, and solute transport. At the later stage (flowering), the number of stimulated GO groups was reduced to photosynthesis and protein biosynthesis. All DEGs of the GO:0016036 group were downregulated because AM plants had higher resistance to phosphate starvation. For the first time, the upregulation of genes encoding thioredoxin in AM plant leaves was shown. It was supposed to reduce ROS level and thus, consequently, enhance the mechanisms of antioxidant protection in M. lupulina plants under conditions of low phosphorus level. Taken together, the obtained results indicate genes that are the most important for the effective symbiosis with M. lupulina and might be engaged in other plant species.
... GRAS transcription factors are involved in hormone signalling, regulation of tissue development, root and axillary shoot development, and response to external stress during plant growth and development [24][25][26][27][28][29]. For example, the SCR and SHR subfamilies regulate lateral root development in Arabidopsis and SHR/SCR/SCL3 may be involved in regulating gibberellins during mycorrhization in tomato [30]; AtPAT1, a member of the AtPAT1 subfamily, is involved in phytochrome A signalling in Arabidopsis [31]; overexpression of PeSCL7 in Populus euphratica (belonging to subfamily AtSCL4/7) enhances drought tolerance and salt tolerance in transgenic Arabidopsis plants [32]; and SHR and SCR are expressed in young leaf primordia, leaves, leaf vascular tissue, and vascular sheath cells [33]. It is worth noting that GAs regulate plant growth and senescence mainly by linking with hormonal pathways and this linkage is pivoted by DELLA proteins. ...
The GRAS protein family is involved in plant growth and development, plant disease resistance, and abiotic stress response. Although the GRAS protein family has been systematically studied and reported in many plants, it has not been reported in oat, an excellent foodstuff crop of Gramineae. We identified 90 AsGRAS genes and all of the AsGRAS genes were randomly distributed on 21 chromosomes with 6 tandem duplicated genes and 49 pairs of segmental duplications, which may be the main reason for the expansion of the GRAS gene family. According to the phylogenetic tree, 90 AsGRASs were classified into 10 distinct subfamilies. Gene structure revealed introns varying from zero to seven, and all genes have conserved motifs and GRAS structure domain. Protein–protein interaction and miRNA prediction analysis showed that AsGRAS proteins mainly interacted with GA signalling, cell division, etc., and that the AsGRAS genes were targeted by miRNA171. RNA-seq and qRT–PCR data showed that GRAS genes were expressed at different growth and developmental stages and under different abiotic stresses in oat, indicating the potential role of GRAS genes in promoting growth and stress tolerance in oat. Overall, our evolutionary and expression analysis of AsGRAS genes contributes to the elucidation of a theoretical basis for the GRAS gene family. Moreover, it helped reveal gene function and laid the foundation for future agricultural improvement of oats based on functional properties.
... Previous studies have shown that GRAS genes induced by arbuscular mycorrhizal (AM) fungi are commonly found in SCLB and RAD1 subfamilies. These genes have been reported to play a crucial role in regulating AM development, including SlGRAS33 (Solyc06g009610), SlGRAS23 (Solyc01g079380), SlGRAS22 (Solyc01g079370), SlGRAS21 (Solyc01g059960), and SlGRAS28 (Solyc03g11095) in tomato [78]. Based on this information, we hypothesize a potential association between the specific motifs and the observed expression patterns in the six cucurbit crops within the SCLB and RAD1 subfamilies, and that these changes may have led to the emergence of new functions in these genes within the Cucurbitaceae family. ...
The Cucurbitaceae family comprises economically valuable vegetables such as cucumber, melon, and pumpkin. GRAS proteins, which are crucial transcription factors, play diverse roles in plant growth and development. However, comparative investigations of GRAS proteins across Cucurbitaceae species are limited. Here, we identified 241 GRAS family genes in six cucurbit crops. The number of GRAS genes in cucumber, melon, wax gourd, watermelon, and bottle gourd ranged from 36 to 37, while the pumpkin genome contained 57 GRAS genes, possibly due to a recent whole-genome duplication. We classified cucurbit GRAS genes into 16 subfamilies and identified species-specific motifs and specific-expression patterns in the SCLB and RAD1 subfamilies. Notably, we identified 38 tissue-specific expressed genes, particularly fruit-specific genes potentially involved in fruit development. Additionally, we predicted the role of GRAS genes in regulating hypocotyl elongation under weak or dark light conditions in cucurbit plants. These findings enhance our understanding of the characteristics, evolution, and potential functions of GRAS genes in six cucurbit crops, providing valuable resources for genetic research in the Cucurbitaceae family as well as important agronomic traits.
... The SYM signaling pathway and symbionts interactions are mainly regulated by an interplay between TFs and phytohormones (auxin, gibberellin, ABA, STs, and ethylene) (Gutjahr, 2014;Diedhiou and Diouf, 2018;Jiang et al., 2018;Müller and Harrison, 2019;Faizan et al., 2020;Liu et al., 2020;Tominaga et al., 2020;Mitra et al., 2021). Among them, GRAS TFs, specifically the genes NSP1 and RAM1, play essential roles (Floss et al., 2013;Nagae et al., 2014;Hohnjec et al., 2015;Rich et al., 2017;Hartmann et al., 2019;Ho-Plaǵaro et al., 2019;Ho-Plaǵaro and Garcıá-Garrido, 2022b). Arbuscules' formation causes changes in the expression patterns of many genes in the AM roots, leading to variation in primary and secondary metabolites and production improvement (Ren et al., 2019;Sakamoto et al., 2019;Shtark et al., 2021;Kaur et al., 2022;Mishra et al., 2022;Zhao et al., 2022). ...
Introduction
Plants and arbuscular mycorrhizal fungi (AMF) mutualistic interactions are essential for sustainable agriculture production. Although it is shown that AMF inoculation improves cassava physiological performances and yield traits, the molecular mechanisms involved in AM symbiosis remain largely unknown. Herein, we integrated metabolomics and transcriptomics analyses of symbiotic (Ri) and asymbiotic (CK) cassava roots and explored AM-induced biochemical and transcriptional changes.
Results
Three weeks (3w) after AMF inoculations, proliferating fungal hyphae were observable, and plant height and root length were significantly increased. In total, we identified 1,016 metabolites, of which 25 were differentially accumulated (DAMs) at 3w. The most highly induced metabolites were 5-aminolevulinic acid, L-glutamic acid, and lysoPC 18:2. Transcriptome analysis identified 693 and 6,481 differentially expressed genes (DEGs) in the comparison between CK (3w) against Ri at 3w and 6w, respectively. Functional enrichment analyses of DAMs and DEGs unveiled transport, amino acids and sugar metabolisms, biosynthesis of secondary metabolites, plant hormone signal transduction, phenylpropanoid biosynthesis, and plant-pathogen interactions as the most differentially regulated pathways. Potential candidate genes, including nitrogen and phosphate transporters, transcription factors, phytohormone, sugar metabolism-related, and SYM (symbiosis) signaling pathway-related, were identified for future functional studies.
Discussion
Our results provide molecular insights into AM symbiosis and valuable resources for improving cassava production.
... GRAS proteins are members of a major protein family that has been studied extensively in the last decade and are unique to plants [16][17][18][19] . At the same time, GRAS transcription factors play a variety of roles in plant growth, development, and resistance to various biotic and abiotic stresses. ...
Lettuce is one of the most popular leafy vegetables in the world, but it is prone to high-temperature stress in the cultivation process leading to bolting, which affects the yield. The plant-specific transcription factors, GRAS proteins, play an important role which regulates plant growth development and abiotic stress. However, there is no comprehensive study of the GRAS gene family in lettuce. In this study, the complete LsGRAS genome was identified its expression was analyzed. The results showed that the 59 LsGRAS genes were classified phylogenetically divided into 4 conserved subfamilies and distributed unevenly on 9 chromosomes, with 50% physically adjacent to at least one another and 100% localized on the nucleus. Chromosome localization and gene structure analysis suggested that duplication events and a large number presence of intronless genes might be the reason why the LsGRAS gene family expands massively. Combined with gene annotation and interaction network analysis, the expression pattern of the LsGRAS gene under high-temperature treatment was analyzed, revealing the potential different functions of the LsGRAS gene under high-temperature stress. In conclusion, this study provides valuable information and candidate genes for improving the ability of lettuce to tolerate high-temperature stress.
