Lipo-chitooligosaccharides as regulatory signals of fungal growth and development

Rush, Tomás A.; Puech‐Pagès, Virginie; Bascaules, Adeline; Jargeat, Patricia; Maillet, Fabienne; Haouy, Alexandra; Maës, Arthur Quy Manh; Carriel, Cristobal Carrera; Khokhani, Devanshi; Keller-Pearson, Michelle; Tannous, Joanna; Cope, Kevin R.; Garcia, Kevin; Maeda, Jun; Johnson, Chad; Kleven, Bailey; Choudhury, Quanita J.; Labbé, Jessy; Swift, Candice L.; O’Malley, Michelle; Bok, Jin Woo; Cottaz, Sylvain; Fort, Sébastien; Poinsot, Véréna; Sussman, Michael R.; Lefort, Corinne; Nett, Jeniel E.; Keller, Nancy P.; Bécard, Guillaume; Ané, Jean‐Michel

doi:10.1038/s41467-020-17615-5

Cited by 78 publications

(92 citation statements)

References 71 publications

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“…LysM receptors j legume symbiosis j lipochitooligosaccharide signaling j receptor-ligand interaction j kinetic proofreading B acteria and fungi surrounding plants synthesize amphiphilic lipochitooligosaccharide (LCO)-signaling molecules consisting of a chitin backbone decorated with a large variety of substitutions at the terminal moieties including hydrophobic acyls at the nonreducing end (1)(2)(3). The selectivity and activation mechanisms of single-pass transmembrane receptors involved in deciphering between this myriad of extracellular signals is still unknown.…”

mentioning

confidence: 99%

Kinetic proofreading of lipochitooligosaccharides determines signal activation of symbiotic plant receptors

Gysel

Laursen

Thygesen

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

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Plants and animals use cell surface receptors to sense and interpret environmental signals. In legume symbiosis with nitrogen-fixing bacteria, the specific recognition of bacterial lipochitooligosaccharide (LCO) signals by single-pass transmembrane receptor kinases determines compatibility. Here, we determine the structural basis for LCO perception from the crystal structures of two lysin motif receptor ectodomains and identify a hydrophobic patch in the binding site essential for LCO recognition and symbiotic function. We show that the receptor monitors the composition of the amphiphilic LCO molecules and uses kinetic proofreading to control receptor activation and signaling specificity. We demonstrate engineering of the LCO binding site to fine-tune ligand selectivity and correct binding kinetics required for activation of symbiotic signaling in plants. Finally, the hydrophobic patch is found to be a conserved structural signature in this class of LCO receptors across legumes that can be used for in silico predictions. Our results provide insights into the mechanism of cell-surface receptor activation by kinetic proofreading of ligands and highlight the potential in receptor engineering to capture benefits in plant–microbe interactions.

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confidence: 99%

Kinetic proofreading of lipochitooligosaccharides determines signal activation of symbiotic plant receptors

Gysel

Laursen

Thygesen

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

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“…Rush et al 41 observed that COs slightly enhance spore germination in Aspergillus fumigatus and pseudohyphae formation in Candida glabrata, albeit to a significantly more limited extent, compared to LCOs 40 . Further analyses will be necessary to investigate if analogous effects are also present in AM fungi.…”

Section: Discussionmentioning

confidence: 99%

Extraction of short chain chitooligosaccharides from fungal biomass and their use as promoters of arbuscular mycorrhizal symbiosis

Crosino

Moscato

Blangetti

et al. 2021

Sci Rep

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Short chain chitooligosaccharides (COs) are chitin derivative molecules involved in plant-fungus signaling during arbuscular mycorrhizal (AM) interactions. In host plants, COs activate a symbiotic signalling pathway that regulates AM-related gene expression. Furthermore, exogenous CO application was shown to promote AM establishment, with a major interest for agricultural applications of AM fungi as biofertilizers. Currently, the main source of commercial COs is from the shrimp processing industry, but purification costs and environmental concerns limit the convenience of this approach. In an attempt to find a low cost and low impact alternative, this work aimed to isolate, characterize and test the bioactivity of COs from selected strains of phylogenetically distant filamentous fungi: Pleurotus ostreatus, Cunninghamella bertholletiae and Trichoderma viride. Our optimized protocol successfully isolated short chain COs from lyophilized fungal biomass. Fungal COs were more acetylated and displayed a higher biological activity compared to shrimp-derived COs, a feature that—alongside low production costs—opens promising perspectives for the large scale use of COs in agriculture.

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“…Extracellular domains mediate the recognition of ubiquitous and conserved MAMPs such as peptides derived from bacterial flagellin, chito-oligosaccharides, that are constituents of the cell wall or lipo-chitooligosaccharides. The latter two had formerly been associated with symbiosis (16) but their presence extends beyond symbiotic fungi (17). Changes in receptor complexes, often involving conserved co-receptors such as BAK1 or SOBIR1 can then result in elevated, or oscillating, concentrations of intracellular calcium and the activation of downstream kinase cascades to activate defense gene networks.…”

Section: Extra-and Intracellular Immunitymentioning

confidence: 99%

Plant evolution driven by interactions with symbiotic and pathogenic microbes

Delaux

Schornack

2021

Science

205

124

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During 450 million years of diversification on land, plants and microbes have evolved together. This is reflected in today’s continuum of associations, ranging from parasitism to mutualism. Through phylogenetics, cell biology, and reverse genetics extending beyond flowering plants into bryophytes, scientists have started to unravel the genetic basis and evolutionary trajectories of plant-microbe associations. Protection against pathogens and support of beneficial, symbiotic, microorganisms are sustained by a blend of conserved and clade-specific plant mechanisms evolving at different speeds. We propose that symbiosis consistently emerges from the co-option of protection mechanisms and general cell biology principles. Exploring and harnessing the diversity of molecular mechanisms used in nonflowering plant-microbe interactions may extend the possibilities for engineering symbiosis-competent and pathogen-resilient crops.

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Lipo-chitooligosaccharides as regulatory signals of fungal growth and development

Cited by 78 publications

References 71 publications

Kinetic proofreading of lipochitooligosaccharides determines signal activation of symbiotic plant receptors

Kinetic proofreading of lipochitooligosaccharides determines signal activation of symbiotic plant receptors

Extraction of short chain chitooligosaccharides from fungal biomass and their use as promoters of arbuscular mycorrhizal symbiosis

Plant evolution driven by interactions with symbiotic and pathogenic microbes

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