Genetics of nodulation in Aeschynomene evenia uncovers mechanisms of the rhizobium–legume symbiosis

Quilbé, Johan; Lamy, Léo; Brottier, Laurent; Leleux, Philippe; Fardoux, Joël; Rivallan, Ronan; Benichou, Thomas; Guyonnet, Rémi; Becana, Manuel; Villar, Irene; Garsmeur, Olivier; Hufnagel, Bárbara; Delteil, Amandine; Gully, Djamel; Chaintreuil, Clémence; Pervent, Marjorie; Cartieaux, Fabienne; Bourge, Mickaël; Valentin, Nicolas; Martin, Guillaume; Fontaine, Loïc; Droc, Gaëtan; Dereeper, Alexis; Farmer, Andrew; Libourel, Cyril; Nouwen, Nico; Gressent, Frédéric; Mournet, Pierre; D’Hont, Angélique; Giraud, Éric; Klopp, Christophe; Arrighi, Jean‐François

doi:10.1038/s41467-021-21094-7

Cited by 50 publications

(72 citation statements)

References 65 publications

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“…In particular, el Zahar Haichar et al (2014) and Wheatley et al (2020) identified a 5-aminoimidazole-4-carboxamide-1-β-D-ribofuranosyl 5 -monophosphate in the roots of legumes, a substance able to supplement the rhizobial purine biosynthesis mutants during growth in the rhizosphere. Further, nodulation is controlled by the SHR-SCR module for inducing cortical cell division that is regulated by the nodule inception (NIN) transcription factor, the transcription of which is activated by rhizobial Nod factors via the CSSP (Dong et al, 2021;Quilbé et al, 2021). After nodule establishment, the plant exploits nodule transfer cells to sense the environmental nitrate status, to regulate plasticity of nodule development, by specifically expressing transporters of the NFP (NRT1/PTR FAMILY) .…”

Section: Symbiosismentioning

confidence: 99%

Transcriptomic and Metabolomic Approaches Deepen Our Knowledge of Plant–Endophyte Interactions

et al. 2022

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In natural systems, plant–symbiont–pathogen interactions play important roles in mitigating abiotic and biotic stresses in plants. Symbionts have their own special recognition ways, but they may share some similar characteristics with pathogens based on studies of model microbes and plants. Multi-omics technologies could be applied to study plant–microbe interactions, especially plant–endophyte interactions. Endophytes are naturally occurring microbes that inhabit plants, but do not cause apparent symptoms in them, and arise as an advantageous source of novel metabolites, agriculturally important promoters, and stress resisters in their host plants. Although biochemical, physiological, and molecular investigations have demonstrated that endophytes confer benefits to their hosts, especially in terms of promoting plant growth, increasing metabolic capabilities, and enhancing stress resistance, plant–endophyte interactions consist of complex mechanisms between the two symbionts. Further knowledge of these mechanisms may be gained by adopting a multi-omics approach. The involved interaction, which can range from colonization to protection against adverse conditions, has been investigated by transcriptomics and metabolomics. This review aims to provide effective means and ways of applying multi-omics studies to solve the current problems in the characterization of plant–microbe interactions, involving recognition and colonization. The obtained results should be useful for identifying the key determinants in such interactions and would also provide a timely theoretical and material basis for the study of interaction mechanisms and their applications.

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Section: Symbiosismentioning

confidence: 99%

Transcriptomic and Metabolomic Approaches Deepen Our Knowledge of Plant–Endophyte Interactions

et al. 2022

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“…In L. japonicus and M. truncatula , LjEPR3 and MtLYK10 commit essential functions in rhizobium infection, whereas in Parasponia the orthologous gene is pseudogenized. Earlier studies showed that also in the legume Aeschynomene evenia the LjEPR3/MtLYK10 orthologous gene is absent [ 18 ]. However, this species possesses a close paralog, which possibly evolved as a result of a legume-specific duplication event and that may commit a similar function [ 9 , 18 ].…”

Section: Resultsmentioning

confidence: 99%

Pseudogenization of the rhizobium-responsive EXOPOLYSACCHARIDE RECEPTOR in Parasponia is a rare event in nodulating plants

et al. 2022

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Background Nodule symbiosis with diazotrophic Frankia or rhizobium occurs in plant species belonging to ten taxonomic lineages within the related orders Fabales, Fagales, Cucurbitales, and Rosales. Phylogenomic studies indicate that this nitrogen-fixing nodulation trait has a single evolutionary origin. In legume model plants, the molecular interaction between plant and rhizobium microsymbiont is mapped to a significant degree. A specific LysM-type receptor kinase, LjEPR3 in Lotus japonicus and MtLYK10 in Medicago truncatula, was found to act in a secondary identity-based mechanism, controlling intracellular rhizobium infection. Furthermore, LjEPR3 showed to bind surface exopolysaccharides of Mesorhizobium loti, the diazotrophic microsymbiont of L. japonicus. EPR3 orthologous genes are not unique to legumes. Surprisingly, however, its ortholog EXOPOLYSACCHARIDE RECEPTOR (EPR) is pseudogenized in Parasponia, the only lineage of non-legume plants that nodulate also with rhizobium. Results Analysis of genome sequences showed that EPR3 orthologous genes are highly conserved in nodulating plants. We identified a conserved retrotransposon insertion in the EPR promoter region in three Parasponia species, which associates with defected transcriptional regulation of this gene. Subsequently, we studied the EPR gene of two Trema species as they represent the sister genus of Parasponia for which it is assumed it lost the nitrogen-fixing nodulation trait. Both Trema species possess apparently functional EPR genes that have a nodulation-specific expression profile when introduced into a Parasponia background. This indicates the EPR gene functioned in nodulation in the Parasponia-Trema ancestor. Conclusion We conclude that nodule-specific expression of EPR3 orthologous genes is shared between the legume and Parasponia-Trema lineage, suggesting an ancestral function in the nitrogen-fixing nodulation trait. Pseudogenization of EPR in Parasponia is an exceptional case in nodulating plants. We speculate that this may have been instrumental to the microsymbiont switch -from Frankia to rhizobium- that has occurred in the Parasponia lineage and the evolution of a novel crack entry infection mechanism.

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“…Legumes also offer advantages in utilisation as livestock feed and a source of income to small-scale farmers (Reddy et al, 2012). They enhance sustainable agriculture due to their nitrogen-fixing ability, limiting the use and impact of inorganic nitrogen fertilisers (Considine et al, 2017;Quilb e et al, 2021). With climate change affecting global agriculture, orphan legumes are alternatives for crop cultivation and utilisation (Murthy and Paek, 2021).…”

Section: Introductionmentioning

confidence: 99%

A review of biotechnological approaches towards crop improvement in African yam bean (Sphenostylis stenocarpa Hochst. Ex A. Rich.)

Oluwole

Aworunse

Aina

et al. 2021

Heliyon

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Globally, climate change is a major factor that contributes significantly to food and nutrition insecurity, limiting crop yield and availability. Although efforts are being made to curb food insecurity, millions of people still suffer from malnutrition. For the United Nations (UN) Sustainable Development Goal of Food Security to be achieved, diverse cropping systems must be developed instead of relying mainly on a few staple crops. Many orphan legumes have untapped potential that can be of significance for developing improved cultivars with enhanced tolerance to changing climatic conditions. One typical example of such an orphan crop is Sphenostylis stenocarpa Hochst. Ex A. Rich. Harms, popularly known as African yam bean (AYB). The crop is an underutilised tropical legume that is climate-resilient and has excellent potential for smallholder agriculture in sub-Saharan Africa (SSA). Studies on AYB have featured morphological characterisation, assessment of genetic diversity using various molecular markers, and the development of tissue culture protocols for rapidly multiplying propagules. However, these have not translated into varietal development, and low yields remain a challenge. The application of suitable biotechnologies to improve AYB is imperative for increased yield, sustainable utilisation and conservation. This review discusses biotechnological strategies with prospective applications for AYB improvement. The potential risks of these strategies are also highlighted.

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Genetics of nodulation in Aeschynomene evenia uncovers mechanisms of the rhizobium–legume symbiosis

Cited by 50 publications

References 65 publications

Transcriptomic and Metabolomic Approaches Deepen Our Knowledge of Plant–Endophyte Interactions

Transcriptomic and Metabolomic Approaches Deepen Our Knowledge of Plant–Endophyte Interactions

Pseudogenization of the rhizobium-responsive EXOPOLYSACCHARIDE RECEPTOR in Parasponia is a rare event in nodulating plants

A review of biotechnological approaches towards crop improvement in African yam bean (Sphenostylis stenocarpa Hochst. Ex A. Rich.)

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