LCO Receptors Involved in Arbuscular Mycorrhiza Are Functional for Rhizobia Perception in Legumes

Girardin, Ariane; Wang, Tongming; Ding, Yi; Keller, Jean; Buendia, Luis; Gaston, Mégane; Ribeyre, Camille; Gasciolli, Virginie; Auriac, Marie‐Christine; Vernié, Tatiana; Bendahmane, Abdelhafid; Ried, Martina Katharina; Parniske, Martin; Morel, Patrice; Vandenbussche, Michiel; Schorderet, Martine; Reinhardt, Didier; Delaux, Pierre-Marc; Bono, Jean‐Jacques; Lefebvre, Benoît

doi:10.1016/j.cub.2019.11.038

Cited by 52 publications

(64 citation statements)

References 78 publications

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“…(2) The NFP1-NFP2 duplication occurred in an ancestor of the Fagales-Cucurbitales-Rosales lineages after the divergence of the Fabales order. The recent finding that ectopic expression of the NFP-type gene of two species outside of the nitrogen-fixing clade (Petunia hybrida PhLYK10 and tomato SlLYK10) can, at least partially, transcomplement the M. truncatula and L. japonicus Mtnfp and Ljnfr5 mutant phenotypes demonstrates that LCO receptor functionality is ancestral to the NFP1-NFP2 duplication (Girardin et al, 2019). The putative promoters of PhLYK10 and SlLYK10 show a noduleenhanced expression profile similar to that reported for PanNFP2 (Girardin et al, 2019), which may support the second scenario, where the duplication of NFP1-NFP2 occurred only after the divergence of the Fabales clade.…”

Section: Discussionmentioning

confidence: 99%

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Duplication of Symbiotic Lysin Motif Receptors Predates the Evolution of Nitrogen-Fixing Nodule Symbiosis

et al. 2020

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Rhizobium nitrogen-fixing nodule symbiosis occurs in two taxonomic lineages: legumes (Fabaceae) and the genus Parasponia (Cannabaceae). Both symbioses are initiated upon the perception of rhizobium-secreted lipochitooligosaccharides (LCOs), called Nod factors. Studies in the model legumes Lotus japonicus and Medicago truncatula showed that rhizobium LCOs are perceived by a heteromeric receptor complex of distinct Lys motif (LysM)-type transmembrane receptors named NOD FACTOR RECEPTOR1 (LjNFR1) and LjNFR5 (L. japonicus) and LYSM DOMAIN CONTAINING RECEPTOR KINASE3 (MtLYK3)-NOD FACTOR PERCEPTION (MtNFP; M. truncatula). Recent phylogenomic comparative analyses indicated that the nodulation traits of legumes, Parasponia spp., as well as so-called actinorhizal plants that establish a symbiosis with diazotrophic Frankia spp. bacteria share an evolutionary origin about 110 million years ago. However, the evolutionary trajectory of LysM-type LCO receptors remains elusive. By conducting phylogenetic analysis, transcomplementation studies, and CRISPR-Cas9 mutagenesis in Parasponia andersonii, we obtained insight into the origin of LCO receptors essential for nodulation. We identified four LysMtype receptors controlling nodulation in P. andersonii: PanLYK1, PanLYK3, PanNFP1, and PanNFP2. These genes evolved from ancient duplication events predating and coinciding with the origin of nodulation. Phylogenetic and functional analyses associated the occurrence of a functional NFP2-orthologous receptor to LCO-driven nodulation. Legumes and Parasponia spp. use orthologous LysM-type receptors to perceive rhizobium LCOs, suggesting a shared evolutionary origin of LCO-driven nodulation. Furthermore, we found that both PanLYK1 and PanLYK3 are essential for intracellular arbuscule formation of mutualistic endomycorrhizal fungi. PanLYK3 also acts as a chitin oligomer receptor essential for innate immune signaling, demonstrating functional analogy to CHITIN ELECITOR RECEPTOR KINASE-type receptors.

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Section: Discussionmentioning

confidence: 99%

“…Classes are presented according to Trouvelot et al (1986). conducted with CAMV35S (Girardin et al, 2019). Such overexpression may mask differences in substrate affinity and/or specificity, under which native transcriptional regulation is biologically relevant.…”

Section: Discussionmentioning

confidence: 99%

Duplication of Symbiotic Lysin Motif Receptors Predates the Evolution of Nitrogen-Fixing Nodule Symbiosis

et al. 2020

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“…In this study, we asked whether a legume, here M. truncatula, is capable of distinguishing lipo-chitooligosaccharide molecules that share similar structures and induce the same developmental root responses. Regulation of root development by LCOs seems to be a conserved plant response observed in legume and non-legume plants (Sun et al, 2015;Tanaka et al, 2015;Buendia et al, 2019), raising the question of its possible evolutionary origin and molecular conservation. The Nod-LCO molecules we used, LCO-IV(C16:2, Ac, S), are produced by the rhizobial symbiont of M. truncatula.…”

Section: Discussionmentioning

confidence: 99%

“…Another property of LCOs is their ability to modify root architecture by stimulating Lateral Root Formation (LRF). The stimulation of LRF appears to be a general response, observed in legume species such as Medicago truncatula treated with Nod Factors or Myc-LCOs (Olah et al, 2005;Maillet et al, 2011), but also in the monocots rice and Brachypodium distachyon (Sun et al, 2015;Buendia et al, 2019). Other positive effects of LCOs on soybean or maize root development are reported (Souleimanov et al, 2002;Tanaka et al, 2015).…”

Section: Introductionmentioning

confidence: 91%

“…Without genetic proof that these molecules are essential for mycorrhization, but since they activate the CSSP as well as symbiotic gene expression changes in host plants, they are considered, together with their oligosaccharidic precursors (COs), as key mycorrhizal signals (Gough & Cullimore, 2011;Genre et al, 2013;Camps et al, 2015;Sun et al, 2015). This is supported by the recent finding in Solanum lycopersicum, that the receptor protein SlLYK10 binds Myc-LCOs and controls the AM symbiosis (Girardin et al, 2019). Also recently, Cope et al showed both that the CSSP is used for establishment of the ectomycorrhizal symbiosis between Laccaria bicolor and poplar, and that L. bicolor can produce LCOs with similar structures to Nod factors (Cope et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

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Distinct genetic bases for plant root responses to lipo-chitooligosaccharide signal molecules from distinct microbial origins

Bonhomme

Bensmihen

Olivier

et al. 2020

Preprint

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SummaryLipo-chitooligosaccharides (LCOs) were originally found as symbiotic signals called Nod Factors (Nod-LCOs) controlling nodulation of legumes by rhizobia. More recently LCOs were also found in symbiotic fungi and, more surprisingly, very widely in the kingdom fungi including in saprophytic and pathogenic fungi. The LCO-V(C18:1, Fuc/MeFuc), hereafter called Fung-LCOs, are the LCO structures most commonly found in fungi. This raises the question of how legume plants, such as Medicago truncatula, can perceive and discriminate between Nod-LCOs and these Fung-LCOs.To address this question, we performed a Genome Wide Association Study on 173 natural accessions of Medicago truncatula, using a root branching phenotype and a newly developed local score approach.Both Nod- and Fung-LCOs stimulated root branching in most accessions but there was very little correlation in the ability to respond to these types of LCO molecules. Moreover, heritability of root response was higher for Nod-LCOs than for Fung-LCOs. We identified 123 loci for Nod-LCO and 71 for Fung-LCO responses, but only one was common.This suggests that Nod- and Fung-LCOs both control root branching but use different molecular mechanisms. The tighter genetic constraint of the root response to Fung-LCOs possibly reflects the ancestral origin of the biological activity of these molecules.

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Molecular interplay of symbiotic and defensive responses in the non-model legume Arachis hypogaea

Rodriguez,

Tonelli,

Fabra

et al. 2024

Symbiosis

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LCO Receptors Involved in Arbuscular Mycorrhiza Are Functional for Rhizobia Perception in Legumes

Cited by 52 publications

References 78 publications

Duplication of Symbiotic Lysin Motif Receptors Predates the Evolution of Nitrogen-Fixing Nodule Symbiosis

Duplication of Symbiotic Lysin Motif Receptors Predates the Evolution of Nitrogen-Fixing Nodule Symbiosis

Distinct genetic bases for plant root responses to lipo-chitooligosaccharide signal molecules from distinct microbial origins

Molecular interplay of symbiotic and defensive responses in the non-model legume Arachis hypogaea

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