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Molecular Plant-Microbe Interactions

A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Microbiology".

Deadline for manuscript submissions: closed (28 February 2022) | Viewed by 34254

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Guest Editor
College of Life Sciences Chromatography Center, Brigham Young University, Provo, UT 84602, USA
Interests: molecular plant-microbe interactions; metabolomics; biotic/abiotic stress; functional genomics; chemical biology; maize
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Special Issue Information

Dear Colleagues,

I would like to invite you to submit a research article or a review for the IJMS Special Issue "Molecular Plant–Microbe Interactions".

When considering the billions of interorganismal interactions occurring on earth, those between plants and microbes are some of the most diverse and economically impactful. Central to these interactions are genes, proteins, and their metabolite products that serve as bioactive modulators of plant and microbe physiology. With the recent advent of omic-technologies, the discovery of active genes, proteins, and molecules that regulate these interactions has progressed rapidly. This Special Issue will highlight the biochemistry, genetics, genomics, molecular biology, and physiology associated with pathogenic, symbiotic, and associative interactions of microbes with plants. Studies that utilize multi-disciplinary approaches to characterize these interactions are strongly encouraged.

Plant–microbe interactions are not only fundamental to plant biology but are critical to crop protection. Toward the goal of contributing to crop improvement, we solicit original research articles and welcome reviews that increase our understanding of the mechanisms mediating plant–microbe interactions rather than those that merely provide a descriptive work.

Dr. Shawn Christensen
Guest Editor

Manuscript Submission Information

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Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. International Journal of Molecular Sciences is an international peer-reviewed open access semimonthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. There is an Article Processing Charge (APC) for publication in this open access journal. For details about the APC please see here. Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • plant–microbe interactions
  • plant defense
  • metabolomics
  • genetics
  • biochemistry

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Published Papers (10 papers)

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Research

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21 pages, 5088 KiB  
Article
Phytoplasma Infection Blocks Starch Breakdown and Triggers Chloroplast Degradation, Leading to Premature Leaf Senescence, Sucrose Reallocation, and Spatiotemporal Redistribution of Phytohormones
by Wei Wei, Junichi Inaba, Yan Zhao, Joseph D. Mowery and Rosemarie Hammond
Int. J. Mol. Sci. 2022, 23(3), 1810; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23031810 - 05 Feb 2022
Cited by 12 | Viewed by 2910
Abstract
Witches’-broom (WB, excessive initiation, and outgrowth of axillary buds) is one of the remarkable symptoms in plants caused by phytoplasmas, minute wall-less intracellular bacteria. In healthy plants, axillary bud initiation and outgrowth are regulated by an intricate interplay of nutrients (such as sugars), [...] Read more.
Witches’-broom (WB, excessive initiation, and outgrowth of axillary buds) is one of the remarkable symptoms in plants caused by phytoplasmas, minute wall-less intracellular bacteria. In healthy plants, axillary bud initiation and outgrowth are regulated by an intricate interplay of nutrients (such as sugars), hormones, and environmental factors. However, how these factors are involved in the induction of WB by phytoplasma is poorly understood. We postulated that the WB symptom is a manifestation of the pathologically induced redistribution of sugar and phytohormones. Employing potato purple top phytoplasma and its alternative host tomato (Solanum lycopersicum), sugar metabolism and transportation, and the spatiotemporal distribution of phytohormones were investigated. A transmission electron microscopy (TEM) analysis revealed that starch breakdown was inhibited, resulting in the degradation of damaged chloroplasts, and in turn, premature leaf senescence. In the infected source leaves, two marker genes encoding asparagine synthetase (Sl-ASN) and trehalose-6-phosphate synthase (Sl-TPS) that induce early leaf senescence were significantly up-regulated. However, the key gibberellin biosynthesis gene that encodes ent-kaurene synthase (Sl-KS) was suppressed. The assessment of sugar content in various infected tissues (mature leaves, stems, roots, and leaf axils) indicated that sucrose transportation through phloem was impeded, leading to sucrose reallocation into the leaf axils. Excessive callose deposition and the resulting reduction in sieve pore size revealed by aniline blue staining and TEM provided additional evidence to support impaired sugar transport. In addition, a spatiotemporal distribution study of cytokinin and auxin using reporter lines detected a cytokinin signal in leaf axils where the axillary buds initiated. However, the auxin responsive signal was rarely present in such leaf axils, but at the tips of the newly elongated buds. These results suggested that redistributed sucrose as well as cytokinin in leaf axils triggered the axillary bud initiation, and auxin played a role in the bud elongation. The expression profiles of genes encoding squamosa promoter-binding proteins (Sl-SBP1), and BRANCHED1 (Sl-BRC1a and Sl-BRC1b) that control axillary bud release, as determined by quantitative reverse transcription (qRT)-PCR, indicated their roles in WB induction. However, their interactions with sugars and cytokinins require further study. Our findings provide a comprehensive insight into the mechanisms by which phytoplasmas induce WB along with leaf chlorosis, little leaf, and stunted growth. Full article
(This article belongs to the Special Issue Molecular Plant-Microbe Interactions)
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14 pages, 4668 KiB  
Article
Magnaporthe oryzae Transcription Factor MoBZIP3 Regulates Appressorium Turgor Pressure Formation during Pathogenesis
by Chengyu Liu, Ningning Shen, Qian Zhang, Minghui Qin, Tingyan Cao, Shuai Zhu, Dingzhong Tang and Libo Han
Int. J. Mol. Sci. 2022, 23(2), 881; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23020881 - 14 Jan 2022
Cited by 7 | Viewed by 1948
Abstract
The devastating fungus Magnaporthe oryzae (M. oryzae) forms a specialized infection structure known as appressorium, which generates enormous turgor, to penetrate the plant cells. However, how M. oryzae regulates the appressorium turgor formation, is not well understood. In this study, we [...] Read more.
The devastating fungus Magnaporthe oryzae (M. oryzae) forms a specialized infection structure known as appressorium, which generates enormous turgor, to penetrate the plant cells. However, how M. oryzae regulates the appressorium turgor formation, is not well understood. In this study, we identified MoBZIP3, a bZIP transcription factor that functioned in pathogenesis in M. oryzae. We found that the pathogenicity of the MoBZIP3 knockout strain (Δmobzip3) was significantly reduced, and the defect was restored after re-expression of MoBZIP3, indicating that MoBZIP3 is required for M. oryzae virulence. Further analysis showed that MoBZIP3 functions in utilization of glycogen and lipid droplets for generation of glycerol in appressorium. MoBZIP3 localized in the nucleus and could bind directly to the promoters of the glycerol synthesis-related genes, MoPTH2, MoTGL1 and MoPEX6, and regulate their expression which is critical for glycerol synthesis in the appressorium turgor pressure generation. Furthermore, the critical turgor sensor gene MoSln1 was also down regulated and its subcellular localization was aberrant in Δmobzip3, which leads to a disordered actin assembly in the Δmobzip3 appressorium. Taken together, these results revealed new regulatory functions of the bZIP transcription factor MoBZIP3, in regulating M. oryzae appressorium turgor formation and infection. Full article
(This article belongs to the Special Issue Molecular Plant-Microbe Interactions)
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18 pages, 2918 KiB  
Article
Silencing of ATP Synthase β Impairs Egg Development in the Leafhopper Scaphoideus titanus, Vector of the Phytoplasma Associated with Grapevine Flavescence Dorée
by Matteo Ripamonti, Luca Cerone, Simona Abbà, Marika Rossi, Sara Ottati, Sabrina Palmano, Cristina Marzachì and Luciana Galetto
Int. J. Mol. Sci. 2022, 23(2), 765; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23020765 - 11 Jan 2022
Cited by 4 | Viewed by 2090
Abstract
Scaphoideus titanus (Hemiptera: Cicadellidae) is the natural vector of Flavescence dorée phytoplasma, a quarantine pest of grapevine with severe impact on European viticulture. RNA interference (RNAi) machinery components are present in S. titanus transcriptome and injection of ATP synthase β dsRNAs into [...] Read more.
Scaphoideus titanus (Hemiptera: Cicadellidae) is the natural vector of Flavescence dorée phytoplasma, a quarantine pest of grapevine with severe impact on European viticulture. RNA interference (RNAi) machinery components are present in S. titanus transcriptome and injection of ATP synthase β dsRNAs into adults caused gene silencing, starting three days post injection (dpi) up to 20 dpi, leading to decrease cognate protein. Silencing of this gene in the closely related leafhopper Euscelidiusvariegatus previously showed female sterility and lack of mature eggs in ovaries. Here, alteration of developing egg morphology in S. titanus ovaries as well as overexpression of hexamerin transcript (amino acid storage protein) and cathepsin L protein (lysosome proteinase) were observed in dsATP-injected females. To evaluate RNAi-specificity, E.variegatus was used as dsRNA-receiving model-species. Different doses of two sets of dsRNA-constructs targeting distinct portions of ATP synthase β gene of both species induced silencing, lack of egg development, and female sterility in E. variegatus, indicating that off-target effects must be evaluated case by case. The effectiveness of RNAi in S. titanus provides a powerful tool for functional genomics of this non-model species and paves the way toward RNAi-based strategies to limit vector population, despite several technical and regulatory constraints that still need to be overcome to allow open field application. Full article
(This article belongs to the Special Issue Molecular Plant-Microbe Interactions)
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41 pages, 27605 KiB  
Article
Trichoderma-Based Biopreparation with Prebiotics Supplementation for the Naturalization of Raspberry Plant Rhizosphere
by Karolina Oszust, Michał Pylak and Magdalena Frąc
Int. J. Mol. Sci. 2021, 22(12), 6356; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms22126356 - 14 Jun 2021
Cited by 14 | Viewed by 3698
Abstract
The number of raspberry plants dying from a sudden outbreak of gray mold, verticillium wilt, anthracnosis, and phytophthora infection has increased in recent times, leading to crop failure. The plants suffer tissue collapse and black roots, symptoms similar to a BotrytisVerticillium–Colletotrichum [...] Read more.
The number of raspberry plants dying from a sudden outbreak of gray mold, verticillium wilt, anthracnosis, and phytophthora infection has increased in recent times, leading to crop failure. The plants suffer tissue collapse and black roots, symptoms similar to a BotrytisVerticillium–ColletotrichumPhytophthora disease complex. A sizeable number of fungal isolates were acquired from the root and rhizosphere samples of wild raspberries from different locations. Subsequent in vitro tests revealed that a core consortium of 11 isolates of selected Trichoderma spp. was the most essential element for reducing in phytopathogen expansion. For this purpose, isolates were characterized by the efficiency of their antagonistic properties against Botrytis, Verticillium, Colletotrichum and Phytophthora isolates and with hydrolytic properties accelerating the decomposition of organic matter in the soil and thus making nutrients available to plants. Prebiotic additive supplementation with a mixture of adonitol, arabitol, erythritol, mannitol, sorbitol, and adenosine was proven in a laboratory experiment to be efficient in stimulating the growth of Trichoderma isolates. Through an in vivo pathosystem experiment, different raspberry naturalization-protection strategies (root inoculations and watering with native Trichoderma isolates, applied separately or simultaneously) were tested under controlled phytotron conditions. The experimental application of phytopathogens attenuated raspberry plant and soil properties, while Trichoderma consortium incorporation exhibited a certain trend of improving these features in terms of a short-term response, depending on the pathosystem and naturalization strategy. What is more, a laboratory-scale development of a biopreparation for the naturalization of the raspberry rhizosphere based on the Trichoderma consortium was proposed in the context of two application scenarios. The first was a ready-to-use formulation to be introduced while planting (pellets, gel). The second was a variant to be applied with naturalizing watering (soluble powder). Full article
(This article belongs to the Special Issue Molecular Plant-Microbe Interactions)
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15 pages, 3203 KiB  
Article
A Novel Hexose Transporter ChHxt6 Is Required for Hexose Uptake and Virulence in Colletotrichum higginsianum
by Qinfeng Yuan, Yaqin Yan, Muhammad Aamir Sohail, Hao Liu, Junbin Huang, Tom Hsiang and Lu Zheng
Int. J. Mol. Sci. 2021, 22(11), 5963; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms22115963 - 31 May 2021
Cited by 5 | Viewed by 2207
Abstract
Colletotrichum higginsianum is an important hemibiotrophic plant pathogen that causes crucifer anthracnose worldwide. To date, some hexose transporters have been identified in fungi. However, the functions of hexose transporters in virulence are not clear in hemibiotrophic phytopathogens. In this study, we identified and [...] Read more.
Colletotrichum higginsianum is an important hemibiotrophic plant pathogen that causes crucifer anthracnose worldwide. To date, some hexose transporters have been identified in fungi. However, the functions of hexose transporters in virulence are not clear in hemibiotrophic phytopathogens. In this study, we identified and characterized a new hexose transporter gene named ChHxt6 from a T-DNA insertion pathogenicity-deficient mutant G256 in C. higginsianum. Expression profiling analysis revealed that six ChHxt genes, ChHxt1 to ChHxt6, exhibited specific expression patterns in different infection phases of C. higginsianum. The ChHxt1 to ChHxt6 were separately deleted using the principle of homologous recombination. ChHxt1 to ChHxt6 deletion mutants grew normally on PDA plates, but only the virulence of ChHxt4 and ChHxt6 deletion mutants was reduced. ChHxt4 was required for fungal infection in both biotrophic and necrotrophic stages, while ChHxt6 was important for formation of necrotrophic hyphae during infection. In addition, ChHxts were functional in uptake of different hexoses, but only ChHxt6-expressing cells could grow on all five hexoses, indicating that the ChHxt6 was a central hexose transporter and crucial for hexose uptake. Site-directed mutation of T169S and P221L positions revealed that these two positions were necessary for hexose transport, whereas only the mutation Thr169 caused reduced virulence and defect in formation of necrotrophic hyphae. Taken together, ChHxt6 might regulate fungal virulence by modulating the utilization of hexose. Full article
(This article belongs to the Special Issue Molecular Plant-Microbe Interactions)
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22 pages, 4967 KiB  
Article
CgEnd3 Regulates Endocytosis, Appressorium Formation, and Virulence in the Poplar Anthracnose Fungus Colletotrichum gloeosporioides
by Xiaolian Wang, Dongxiao Lu and Chengming Tian
Int. J. Mol. Sci. 2021, 22(8), 4029; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms22084029 - 14 Apr 2021
Cited by 11 | Viewed by 2262
Abstract
The hemibiotrophic ascomycete fungus Colletotrichum gloeosporioides is the causal agent of anthracnose on numerous plants, and it causes considerable economic losses worldwide. Endocytosis is an essential cellular process in eukaryotic cells, but its roles in C. gloeosporioides remain unknown. In our study, we [...] Read more.
The hemibiotrophic ascomycete fungus Colletotrichum gloeosporioides is the causal agent of anthracnose on numerous plants, and it causes considerable economic losses worldwide. Endocytosis is an essential cellular process in eukaryotic cells, but its roles in C. gloeosporioides remain unknown. In our study, we identified an endocytosis-related protein, CgEnd3, and knocked it out via polyethylene glycol (PEG)-mediated protoplast transformation. The lack of CgEnd3 resulted in severe defects in endocytosis. C. gloeosporioides infects its host through a specialized structure called appressorium, and ΔCgEnd3 showed deficient appressorium formation, melanization, turgor pressure accumulation, penetration ability of appressorium, cellophane membrane penetration, and pathogenicity. CgEnd3 also affected oxidant adaptation and the expression of core effectors during the early stage of infection. CgEnd3 contains one EF hand domain and four calcium ion-binding sites, and it is involved in calcium signaling. A lack of CgEnd3 changed the responses to cell-wall integrity agents and fungicide fludioxonil. However, CgEnd3 regulated appressorium formation and endocytosis in a calcium signaling-independent manner. Taken together, these results demonstrate that CgEnd3 plays pleiotropic roles in endocytosis, calcium signaling, cell-wall integrity, appressorium formation, penetration, and pathogenicity in C. gloeosporioides, and it suggests that CgEnd3 or endocytosis-related genes function as promising antifungal targets. Full article
(This article belongs to the Special Issue Molecular Plant-Microbe Interactions)
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Review

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16 pages, 2021 KiB  
Review
Emerging Roles of Motile Epidermal Chloroplasts in Plant Immunity
by Hiroki Irieda
Int. J. Mol. Sci. 2022, 23(7), 4043; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23074043 - 06 Apr 2022
Cited by 2 | Viewed by 2472
Abstract
Plant epidermis contains atypical small chloroplasts. However, the physiological role of this organelle is unclear compared to that of large mesophyll chloroplasts, the well-known function of which is photosynthesis. Although knowledge of the involvement of chloroplasts in the plant immunity has been expanded [...] Read more.
Plant epidermis contains atypical small chloroplasts. However, the physiological role of this organelle is unclear compared to that of large mesophyll chloroplasts, the well-known function of which is photosynthesis. Although knowledge of the involvement of chloroplasts in the plant immunity has been expanded to date, the differences between the epidermal and mesophyll chloroplasts are beyond the scope of this study. Given the role of the plant epidermis as a barrier to environmental stresses, including pathogen attacks, and the immune-related function of chloroplasts, plant defense research on epidermal chloroplasts is an emerging field. Recent studies have revealed the dynamic movements of epidermal chloroplasts in response to fungal and oomycete pathogens. Furthermore, epidermal chloroplast-associated proteins and cellular events that are tightly linked to epidermal resistance against pathogens have been reported. In this review, I have focused on the recent progress in epidermal chloroplast-mediated plant immunity. Full article
(This article belongs to the Special Issue Molecular Plant-Microbe Interactions)
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18 pages, 1272 KiB  
Review
Scent of a Symbiont: The Personalized Genetic Relationships of Rhizobium—Plant Interaction
by Lisa Cangioli, Francesca Vaccaro, Margherita Fini, Alessio Mengoni and Camilla Fagorzi
Int. J. Mol. Sci. 2022, 23(6), 3358; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23063358 - 20 Mar 2022
Cited by 6 | Viewed by 2859
Abstract
Many molecular signals are exchanged between rhizobia and host legume plants, some of which are crucial for symbiosis to take place, while others are modifiers of the interaction, which have great importance in the competition with the soil microbiota and in the genotype-specific [...] Read more.
Many molecular signals are exchanged between rhizobia and host legume plants, some of which are crucial for symbiosis to take place, while others are modifiers of the interaction, which have great importance in the competition with the soil microbiota and in the genotype-specific perception of host plants. Here, we review recent findings on strain-specific and host genotype-specific interactions between rhizobia and legumes, discussing the molecular actors (genes, gene products and metabolites) which play a role in the establishment of symbiosis, and highlighting the need for research including the other components of the soil (micro)biota, which could be crucial in developing rational-based strategies for bioinoculants and synthetic communities’ assemblage. Full article
(This article belongs to the Special Issue Molecular Plant-Microbe Interactions)
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22 pages, 1979 KiB  
Review
Microbial Contributions for Rice Production: From Conventional Crop Management to the Use of ‘Omics’ Technologies
by Febri Doni, Nurul Shamsinah Mohd Suhaimi, Muhamad Shakirin Mispan, F Fathurrahman, Betty Mayawatie Marzuki, Joko Kusmoro and Norman Uphoff
Int. J. Mol. Sci. 2022, 23(2), 737; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23020737 - 10 Jan 2022
Cited by 24 | Viewed by 7298
Abstract
Rice, the main staple food for about half of the world’s population, has had the growth of its production stagnate in the last two decades. One of the ways to further improve rice production is to enhance the associations between rice plants and [...] Read more.
Rice, the main staple food for about half of the world’s population, has had the growth of its production stagnate in the last two decades. One of the ways to further improve rice production is to enhance the associations between rice plants and the microbiome that exists around, on, and inside the plant. This article reviews recent developments in understanding how microorganisms exert positive influences on plant growth, production, and health, focusing particularly on rice. A variety of microbial species and taxa reside in the rhizosphere and the phyllosphere of plants and also have multiple roles as symbiotic endophytes while living within plant tissues and even cells. They alter the morphology of host plants, enhance their growth, health, and yield, and reduce their vulnerability to biotic and abiotic stresses. The findings of both agronomic and molecular analysis show ways in which microorganisms regulate the growth, physiological traits, and molecular signaling within rice plants. However, many significant scientific questions remain to be resolved. Advancements in high-throughput multi-omics technologies can be used to elucidate mechanisms involved in microbial–rice plant associations. Prospectively, the use of microbial inoculants and associated approaches offers some new, cost-effective, and more eco-friendly practices for increasing rice production. Full article
(This article belongs to the Special Issue Molecular Plant-Microbe Interactions)
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27 pages, 22618 KiB  
Review
Rhizobial Exopolysaccharides: Genetic Regulation of Their Synthesis and Relevance in Symbiosis with Legumes
by Sebastián Acosta-Jurado, Francisco Fuentes-Romero, Jose-Enrique Ruiz-Sainz, Monika Janczarek and José-María Vinardell
Int. J. Mol. Sci. 2021, 22(12), 6233; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms22126233 - 09 Jun 2021
Cited by 30 | Viewed by 3953
Abstract
Rhizobia are soil proteobacteria able to engage in a nitrogen-fixing symbiotic interaction with legumes that involves the rhizobial infection of roots and the bacterial invasion of new organs formed by the plant in response to the presence of appropriate bacterial partners. This interaction [...] Read more.
Rhizobia are soil proteobacteria able to engage in a nitrogen-fixing symbiotic interaction with legumes that involves the rhizobial infection of roots and the bacterial invasion of new organs formed by the plant in response to the presence of appropriate bacterial partners. This interaction relies on a complex molecular dialogue between both symbionts. Bacterial N-acetyl-glucosamine oligomers called Nod factors are indispensable in most cases for early steps of the symbiotic interaction. In addition, different rhizobial surface polysaccharides, such as exopolysaccharides (EPS), may also be symbiotically relevant. EPS are acidic polysaccharides located out of the cell with little or no cell association that carry out important roles both in free-life and in symbiosis. EPS production is very complexly modulated and, frequently, co-regulated with Nod factors, but the type of co-regulation varies depending on the rhizobial strain. Many studies point out a signalling role for EPS-derived oligosaccharides in root infection and nodule invasion but, in certain symbiotic couples, EPS can be dispensable for a successful interaction. In summary, the complex regulation of the production of rhizobial EPS varies in different rhizobia, and the relevance of this polysaccharide in symbiosis with legumes depends on the specific interacting couple. Full article
(This article belongs to the Special Issue Molecular Plant-Microbe Interactions)
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