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Genes conserved for arbuscular mycorrhizal symbiosis identified through phylogenomics

Nature Plants volume 2, Article number: 15208 (2016) Cite this article

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Abstract

Arbuscular mycorrhizal symbiosis (AMS), a widespread mutualistic association of land plants and fungi1, is predicted to have arisen once, early in the evolution of land plants2–4. Consistent with this notion, several genes required for AMS have been conserved throughout evolution5 and their symbiotic functions preserved, at least between monocot and dicot plants6,7. Despite its significance, knowledge of the plants' genetic programme for AMS is limited. To date, most genes required for AMS have been found through commonalities with the evolutionarily younger nitrogen-fixing Rhizobium legume symbiosis (RLS)8 or by reverse genetic analyses of differentially expressed candidate genes9. Large sequence-indexed insertion mutant collections and recent genome editing technologies have vastly increased the power of reverse genetics but selection of candidate genes, from the thousands of genes that change expression during AMS, remains an arbitrary process. Here, we describe a phylogenomics approach to identify genes whose evolutionary history predicts conservation for AMS and we demonstrate the accuracy of the predictions through reverse genetics analysis. Phylogenomics analysis of 50 plant genomes resulted in 138 genes from Medicago truncatula predicted to function in AMS. This includes 15 genes with known roles in AMS. Additionally, we demonstrate that mutants in six previously uncharacterized AMS-conserved genes are all impaired in AMS. Our results demonstrate that phylogenomics is an effective strategy to identify a set of evolutionarily conserved genes required for AMS.

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Figure 1: Methodology and examples of phylogenetic trees of AMS-conserved genes.
Figure 2: Gene expression summary and categories of AMS-conserved genes.
Figure 3: AMS phenotype of mutants with Tnt1 insertions in AMS-conserved genes.
Figure 4: Arbuscule development phenotype of fatm mutant.

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Acknowledgements

Financial support for this project was provided initially by the TRIAD Foundation and subsequently by the US National Science Foundation grant no. IOS-1127155. The M. truncatula Tnt1 insertion mutant lines were obtained from The Samuel Roberts Noble Foundation Inc. Microscopes in the BTI Plant Cell Imaging Center used in this study were purchased with a National Science Foundation Instrumentation Grant, NSF DBI-0618969. We thank M. Waters and S. de la Torre for critical evaluation of the manuscript, S. Ivanov for the Gateway plasmids used for the complementation assays and members of the Harrison laboratory for helpful comments and discussion.

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  1. Nathan Pumplin

    Present address: †Present address: Department of Biology, Swiss Federal Institute of Technology, 8092 Zurich, Switzerland.,

Authors and Affiliations

  1. Boyce Thompson Institute for Plant Research, 533 Tower Road, Ithaca, 14853, New York, USA

    Armando Bravo, Thomas York, Nathan Pumplin, Lukas A. Mueller & Maria J. Harrison

Authors
  1. Armando Bravo
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Contributions

A.B., N.P., L.A.M. and M.J.H. conceived the experiments; T.Y. and L.A.M. developed and ran the automated bioinformatics pipeline; T.Y. and A.B. analysed the data; A.B. ran manual phylogenetic analyses, reverse genetic analyses and mycorrhiza experiments; T.Y. and A.B. wrote the methods; A.B. and M.J.H. wrote the manuscript.

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Correspondence to Maria J. Harrison.

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Bravo, A., York, T., Pumplin, N. et al. Genes conserved for arbuscular mycorrhizal symbiosis identified through phylogenomics. Nature Plants 2, 15208 (2016). https://doi.org/10.1038/nplants.2015.208

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