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An ancestral signalling pathway is conserved in intracellular symbioses-forming plant lineages

Nature Plants volume 6, pages 280–289 (2020)Cite this article

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Abstract

Plants are the foundation of terrestrial ecosystems, and their colonization of land was probably facilitated by mutualistic associations with arbuscular mycorrhizal fungi. Following this founding event, plant diversification has led to the emergence of a tremendous diversity of mutualistic symbioses with microorganisms, ranging from extracellular associations to the most intimate intracellular associations, where fungal or bacterial symbionts are hosted inside plant cells. Here, through analysis of 271 transcriptomes and 116 plant genomes spanning the entire land-plant diversity, we demonstrate that a common symbiosis signalling pathway co-evolved with intracellular endosymbioses, from the ancestral arbuscular mycorrhiza to the more recent ericoid and orchid mycorrhizae in angiosperms and ericoid-like associations of bryophytes. By contrast, species forming exclusively extracellular symbioses, such as ectomycorrhizae, and those forming associations with cyanobacteria, have lost this signalling pathway. This work unifies intracellular symbioses, revealing conservation in their evolution across 450 million yr of plant diversification.

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Fig. 1: Conservation of the symbiotic genes in land plants.
Fig. 2: Maximum-likelihood trees of genes specific to the AMS or intracellular symbioses in land plants.
Fig. 3: Loss of symbiotic genes following mutualism abandonment in Marchantia.
Fig. 4: Conservation of biochemical properties of CCaMK and CYCLOPS in land plants.
Fig. 5: Maximum-likelihood trees of infection-related genes.
Fig. 6: Model for the conservation of symbiotic genes across symbiosis types.

Data availability

All assemblies and gene annotations generated in this project can be found in SymDB (www.polebio.lrsv.ups-tlse.fr/symdb/). Raw sequencing data can be found under NCBI Bioproject PRJNA576233 (B. pusilla), PRJNA362997 and PRJNA362995 (M. paleacea genome and transcriptome, respectively) and PRJNA576577 (M. polymorpha ssp. montivagans and ssp. polymorpha).

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Acknowledgements

This work was supported by the Agence Nationale de la Recherche (ANR) grant EVOLSYM (ANR-17-CE20-0006-01) to P.-M.D., by the Bill and Melinda Gates Foundation as Engineering the Nitrogen Symbiosis for Africa (OPP1172165), by the BBSRC as OpenPlant to G.E.D.O (BB/L014130/1), by the 10KP initiative (BGI-Shenzhen), by the National Science Foundation (DEB1831428) to F.-W.L. and by the Swedish Research Council Vetenskapsrådet (VR) to U.L. (2011‐5609 and 2014‐522) and to D.M.E (2016-05180). G.V.R is additionally supported by a Biotechnology and Biological Sciences Research Council Discovery Fellowship (BB/S011005/1). Part of this work was conducted at the Laboratoire de Recherche en Sciences Végétales (LRSV) laboratory, which belongs to the TULIP Laboratoire d’Excellence (ANR-10-LABX-41). We are grateful to the genotoul bioinformatics platform Toulouse Midi–Pyrenees for providing computing and storage resources. We thank F. Roux for helping with the collection of M. polymorpha accessions, A. Cooke for assistance with M. paleacea DNA extraction, P. Szoevenyi for advice on M. polymorpha DNA extraction, and D. Barker and members of the Engineering Nitrogen Symbiosis for Africa (ENSA) project for helpful comments and discussion. Figure 6b was prepared by J. Calli (www.jeremy-calli.fr).

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Author notes

  1. These authors contributed equally: Guru V. Radhakrishnan, Jean Keller, Melanie K. Rich, Tatiana Vernié.

Authors and Affiliations

  1. John Innes Centre, Norwich, UK

    Guru V. Radhakrishnan, Jitender Cheema & Giles E. D. Oldroyd

  2. LRSV, Université de Toulouse, CNRS, UPS, Castanet-Tolosan, France

    Jean Keller, Melanie K. Rich, Tatiana Vernié, Duchesse L. Mbadinga Mbadinga, Nicolas Vigneron, Hélène San Clemente, Cyril Libourel & Pierre-Marc Delaux

  3. LIPM, Université de Toulouse, INRA, CNRS, Castanet-Tolosan, France

    Ludovic Cottret

  4. Plant Ecology and Evolution, Department of Ecology and Genetics, Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden

    Anna-Malin Linde, D. Magnus Eklund & Ulf Lagercrantz

  5. Agricultural Genome Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China

    Shifeng Cheng

  6. BGI-Shenzhen, Shenzhen, China

    Gane K. S. Wong

  7. Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada

    Gane K. S. Wong

  8. Department of Medicine, University of Alberta, Edmonton, Alberta, Canada

    Gane K. S. Wong

  9. Boyce Thompson Institute, Ithaca, New York, NY, USA

    Fay-Wei Li

  10. Plant Biology Section, Cornell University, New York, NY, USA

    Fay-Wei Li

  11. Sainsbury Laboratory, University of Cambridge, Cambridge, UK

    Giles E. D. Oldroyd

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  1. Guru V. Radhakrishnan
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Contributions

P.-M.D., G.V.R., M.K.R., J.K., G.E.D.O. and T.V. conceived the experiments; J.K., H.S.C. and L.C. developed symDB; G.V.R., M.K.R., J.K., T.V., D.L.M.M., N.V., C.L., J.C. and P.-M.D. conducted the experiments; A.-M.L., D.M.E. and U.L. generated the M. polymorpha subspecies genomes; F.-W.L., S.C. and G.K.S.W. generated the B. pusilla transcriptome; P.-M.D., G.V.R., M.K.R., J.K. and T.V. analysed the data; J.K. compiled the supplementary material; G.V.R., M.K.R., G.E.D.O. and P.-M.D. wrote the manuscript.

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Correspondence to Giles E. D. Oldroyd or Pierre-Marc Delaux.

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Radhakrishnan, G.V., Keller, J., Rich, M.K. et al. An ancestral signalling pathway is conserved in intracellular symbioses-forming plant lineages. Nat. Plants 6, 280–289 (2020). https://doi.org/10.1038/s41477-020-0613-7

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