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Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza

Nature volume 469, pages 58–63 (2011)Cite this article

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Abstract

Arbuscular mycorrhiza (AM) is a root endosymbiosis between plants and glomeromycete fungi. It is the most widespread terrestrial plant symbiosis, improving plant uptake of water and mineral nutrients. Yet, despite its crucial role in land ecosystems, molecular mechanisms leading to its formation are just beginning to be unravelled. Recent evidence suggests that AM fungi produce diffusible symbiotic signals. Here we show that Glomus intraradices secretes symbiotic signals that are a mixture of sulphated and non-sulphated simple lipochitooligosaccharides (LCOs), which stimulate formation of AM in plant species of diverse families (Fabaceae, Asteraceae and Umbelliferae). In the legume Medicago truncatula these signals stimulate root growth and branching by the symbiotic DMI signalling pathway. These findings provide a better understanding of the evolution of signalling mechanisms involved in plant root endosymbioses and will greatly facilitate their molecular dissection. They also open the way to using these natural and very active molecules in agriculture.

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Figure 1: Detection and characterization of LCOs in mycorrhized carrot root exudates.
Figure 2: Detection and characterization of LCOs in germinating G. intraradices spore exudates.
Figure 3: Chemical structures of natural and synthetic Myc-LCOs.
Figure 4: Effect of Myc-LCOs on mycorrhization by G. intraradices.
Figure 5: Synthetic Myc-LCOs stimulate M. truncatula root branching by the DMI pathway.

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Acknowledgements

This work was supported in part by a grant from EMD Crop BioScience and by the Charles-Léopold Mayer Prize (2005) attributed to J.D. by the French Academy of Sciences. M.G. was supported by an Institut National de la Recherche Agronomique fellowship. We are grateful to C. Gough and G. Oldroyd for providing seeds of M. truncatula mutants, and to S. Roy and J. Loubradou for providing sterile mycorrhized roots and spores of G. intraradices. The UPLC/QToF mass spectrometer was made available to us by the Institut des Technologies Avancées du Vivant and the QTRAP mass spectrometer by the Metabolomics and fluxomics platform (MetaToul). We thank S. Danoun for her help with UPLC/QToF mass spectrometry, F. Letisse for his advice and help in setting up experiments on the QTrap mass spectrometer, P. Lavedan for NMR measurements, C. Hervé for her advice and help for quantitative PCR with reverse transcription experiments and C. Brière for his advice for statistical analysis. We thank C. Gough, J. Cullimore and G. Oldroyd for their comments on this manuscript.

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Author notes

  1. Fabienne Maillet, Véréna Poinsot and Olivier André: These authors contributed equally to this work.

Authors and Affiliations

  1. Laboratoire des Interactions Plantes-Microorganismes, UMR 441/2594 INRA-CNRS, B.P. 52627, F-31326 Castanet-Tolosan CEDEX, France

    Fabienne Maillet, Olivier André, Alexandra Haouy, Monique Gueunier, Laurence Cromer, Delphine Giraudet, Andreas Niebel & Jean Dénarié

  2. Laboratoire des IMRCP, UMR 5623 CNRS-Université Paul Sabatier, 118 route de Narbonne, F-31062 Toulouse CEDEX, France

    Véréna Poinsot

  3. Université de Toulouse, UPS, UMR 5546, Surfaces Cellulaires et Signalisation chez les Végétaux, BP 42617, F-31326 Castanet-Tolosan CEDEX, France

    Virginie Puech-Pagès, Monique Gueunier, Damien Formey & Guillaume Bécard

  4. CNRS, UMR 5546, BP 42617, F-31326 Castanet-Tolosan CEDEX, France

    Virginie Puech-Pagès, Monique Gueunier, Damien Formey & Guillaume Bécard

  5. Centre de Recherches sur les Macromolécules Végétales, CNRS (affiliated to Université Joseph Fourier), B.P. 53, F-38041 Grenoble CEDEX 9, France

    Eduardo Andres Martinez & Hugues Driguez

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  1. Fabienne Maillet
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Contributions

F.M. coordinated experiments for all bioassays, designed and performed the VsHab assay, and designed and performed M. truncatula bioassays with O.A. O.A. and V.P. purified fungal Myc-LCOs. M.G. and A.H. prepared germinating spores. L.C. and A.H. performed the ENOD11 bioassay. A.H. designed and performed mycorrhization tests on carrots and Tagetes. O.A. performed statistical analyses. F.M. and D.G. extracted Myc-LCO analogues from rhizobial mutant cultures, and E.A.M. and H.D. synthesized Myc-LCOs by the cell factory technique. For mass spectrometry, UPLC/QToF was performed by V.P. and V.P.-P., and QTRAP by V.P.-P. Quantitative PCR with reverse transcription experiments were designed and analysed by A.N. and realized by D.F. and O.A. G.B. supervised devising, planning and interpreting experiments with AM fungal material (material production, spore germination and mycorrhization tests). J.D. conceived and directed the project, and wrote the manuscript with the help of F.M., V.P. and G.B.

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Correspondence to Jean Dénarié.

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Maillet, F., Poinsot, V., André, O. et al. Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469, 58–63 (2011). https://doi.org/10.1038/nature09622

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