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A coumarin exudation pathway mitigates arbuscular mycorrhizal incompatibility in Arabidopsis thaliana

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Abstract

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Overexpression of genes involved in coumarin production and secretion can mitigate mycorrhizal incompatibility in nonhost Arabidopsis plants. The coumarin scopoletin, in particular, stimulates pre-penetration development and metabolism in mycorrhizal fungi.

Abstract

Although most plants can benefit from mutualistic associations with arbuscular mycorrhizal (AM) fungi, nonhost plant species such as the model Arabidopsis thaliana have acquired incompatibility. The transcriptional response of Arabidopsis to colonization by host-supported AM fungi switches from initial AM recognition to defense activation and plant growth antagonism. However, detailed functional information on incompatibility in nonhost–AM fungus interactions is largely missing. We studied interactions between host-sustained AM fungal networks of Rhizophagus irregularis and 18 Arabidopsis genotypes affected in nonhost penetration resistance, coumarin production and secretion, and defense (salicylic acid, jasmonic acid, and ethylene) and growth hormones (auxin, brassinosteroid, cytokinin, and gibberellin). We demonstrated that root-secreted coumarins can mitigate incompatibility by stimulating fungal metabolism and promoting initial steps of AM colonization. Moreover, we provide evidence that major molecular defenses in Arabidopsis do not operate as primary mechanisms of AM incompatibility nor of growth antagonism. Our study reveals that, although incompatible, nonhost plants can harbor hidden tools that promote initial steps of AM colonization. Moreover, it uncovered the coumarin scopoletin as a novel signal in the pre-penetration dialogue, with possible implications for the chemical communication in plant–mycorrhizal fungi associations.

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Acknowledgements

This work was funded by NWO Grant 823.02.019 of The Netherlands Organization for Scientific Research, Incoming Post-doctoral Fellowship of the Fonds Spéciaux de Recherche from the Wallonie-Bruxelles Federation of Belgium (to M.C.), and ERC Advanced Investigator Grant No. 269072 of the European Research Council (to C.M.J.P.). The authors are thankful to Daniel Grimm and Maryline Calonne for help with some of the experiments, and to Emilie Reinen, Joyce Elberse, Ioannis Stringlis, Ke Yu and Thomas Schmülling for providing Arabidopsis seeds.

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  1. Plant-Microbe Interactions, Department of Biology, Science4Life, Utrecht University, PO Box 800.56, 3508 TB, Utrecht, the Netherlands

    Marco Cosme, Iván Fernández, Marcel G. A. van der Heijden & Corné M. J. Pieterse

  2. Mycology, Applied Microbiology, Earth and Life Institute, Université Catholique de Louvain, Croix du sud 2, bte L7.05.06, 1348, Louvain-la-Neuve, Belgium

    Marco Cosme & Stéphane Declerck

  3. Plant–Soil Interactions, Department of Agroecology and Environment, Agroscope Reckenholz, Reckenholzstrasse 191, 8046, Zurich, Switzerland

    Marcel G. A. van der Heijden

  4. Department of Plant and Microbial Biology, University of Zürich, 8057, Zurich, Switzerland

    Marcel G. A. van der Heijden

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  1. Marco Cosme
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  2. Iván Fernández
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All authors planned and designed the research. MC performed the experiments. MC, SD, MGAvdH and CMJP analyzed results. All authors wrote the manuscript.

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Cosme, M., Fernández, I., Declerck, S. et al. A coumarin exudation pathway mitigates arbuscular mycorrhizal incompatibility in Arabidopsis thaliana. Plant Mol Biol 106, 319–334 (2021). https://doi.org/10.1007/s11103-021-01143-x

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