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Ligand-receptor co-evolution shaped the jasmonate pathway in land plants

Nature Chemical Biology volume 14, pages 480–488 (2018)Cite this article

Abstract

The phytohormone jasmonoyl-isoleucine (JA-Ile) regulates defense, growth and developmental responses in vascular plants. Bryophytes have conserved sequences for all JA-Ile signaling pathway components but lack JA-Ile. We show that, in spite of 450 million years of independent evolution, the JA-Ile receptor COI1 is functionally conserved between the bryophyte Marchantia polymorpha and the eudicot Arabidopsis thaliana but COI1 responds to different ligands in each species. We identified the ligand of Marchantia MpCOI1 as two isomeric forms of the JA-Ile precursor dinor-OPDA (dinor-cis-OPDA and dinor-iso-OPDA). We demonstrate that AtCOI1 functionally complements Mpcoi1 mutation and confers JA-Ile responsiveness and that a single-residue substitution in MpCOI1 is responsible for the evolutionary switch in ligand specificity. Our results identify the ancestral bioactive jasmonate and clarify its biosynthetic pathway, demonstrate the functional conservation of its signaling pathway, and show that JA-Ile and COI1 emergence in vascular plants required co-evolution of hormone biosynthetic complexity and receptor specificity.

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Fig. 1: MpCOI1 regulates responses to OPDA.
Fig. 2: AtCOI1 complements the Mpcoi1-1 mutant and confers JA-Ile/COR responsiveness to M. polymorpha.
Fig. 3: AtCOI1 complements Mpcoi1 insensitivity to OPDA-induced gene expression.
Fig. 4: A single amino acid of COI1 determines ligand specificity.
Fig. 5: OPDA is a precursor of dinor-OPDA and both accumulate after wounding.
Fig. 6: dinor-OPDA is the bioactive ligand of MpCOI1 in M. polymorpha.

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Acknowledgements

We thank J. Paz-Ares and members of Solano's lab for critical reading of the manuscript and C. Mark for English editing. We thank K. Inoue (Kyoto University) for vector construction and assistance with CRISPR–Cas9D10A cloning. We also thank H. Matsuura (Hokkaido Univ.) for assistance with OPDA synthesis. J. Langdale (Oxford University) kindly provided Anthoceros agrestis and B. Benito (CBGP-UPM-INIA) Physcomitrella patens. E.E. Farmer (University of Lausanne) kindly provided Methyl-dn-OPDA and M. Alfonso (EEAD-CSIC) provided dn-OPDA. L. Colombo (University of Milan) kindly provided pTFT vector. This work was funded by the Spanish Ministry for Science and Innovation grant BIO2016-77216-R (MINECO/FEDER). I.M. was supported by a predoctoral fellowship from the Ministerio de Educación, Spain (grant AP2010-1410) and EMBO Short Term Fellowship (ASTF 385-2013). This work was partly supported by MEXT KAKENHI Grant Numbers JP15K21758 and JP25113009 to TK. P.R and C.G.-D. are funded by the Swiss National Science Foundation Grant Nr. 31003A_169278

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Authors and Affiliations

  1. Department of Plant Molecular Genetics, Centro Nacional de Biotecnología, Consejo Superior de Investigaciones Científicas (CNB-CSIC), Madrid, Spain

    Isabel Monte & Roberto Solano

  2. Graduate School of Biostudies, Kyoto University, Kyoto, Japan

    Sakiko Ishida, Ryuichi Nishihama & Takayuki Kohchi

  3. Environmental Biology Department, University of Navarra, Navarra, Spain

    Angel M. Zamarreño & José M. García-Mina

  4. Division of Physiological Chemistry II, Department of Medical Biochemistry and Biophysics, Karolinska Institutet, Stockholm, Sweden

    Mats Hamberg

  5. Genomics Unit, Centro Nacional de Biotecnología, Consejo Superior de Investigaciones Científicas (CNB-CSIC), Madrid, Spain

    José M. Franco-Zorrilla & Gloria García-Casado

  6. Department of Plant Molecular Biology, University of Lausanne, Lausanne, Switzerland

    Caroline Gouhier-Darimont & Philippe Reymond

  7. Research Faculty of Agriculture, Division of Applied Bioscience, Hokkaido University, Sapporo, Japan

    Kosaku Takahashi

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Contributions

I.M. and R.S. designed the experiments. I.M. performed experiments in Figs. 1,2,4 and 6 and Supplementary Figs. 1, 2, 3a, 4, 5, 6, 7 and 9 and prepared the samples for experiments in Figs. 3 and 5 and Supplementary Fig. 8. S.I. identified Mpcoi1-1. A.M.Z. quantified oxylipins (Figs. 1 and 5 and Supplementary Figs. 1 and 8). M.H. synthesized all chemicals described in Methods. J.M.F.-Z. designed and analyzed microarray data. G.G.-C. performed gene expression analysis. C.G.-D. performed insect feeding assays. P.R. designed, supervised and analyzed insect feeding assays. K.T. synthesized OPDA and OPDA-Ile. J.M.G.-M. designed and supervised LC–MS experiments. R.N. and T.K. designed and supervised homologous recombination and CRISPR experiments to obtain Mpcoi1 mutants. R.S. supervised the work. I.M and R.S. wrote the manuscript. All authors discussed the results and edited the manuscript.

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Correspondence to Roberto Solano.

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Supplementary Figure 1–10, Table 1–2

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Supplementary Data Set 1

Relative expression values (Log2 ratio) of the genes included in the clustering analysis shown in Figure 3b

Supplementary Data Set 2

Enriched Gene Ontology (GO) terms based on Marchantia annotations of the gene clusters shown in Figure 3b

Supplementary Data Set 3

Enriched Gene Ontology (GO) terms based on the Arabidopsis orthologues of genes shown in clusters in Figure 3b

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Monte, I., Ishida, S., Zamarreño, A.M. et al. Ligand-receptor co-evolution shaped the jasmonate pathway in land plants. Nat Chem Biol 14, 480–488 (2018). https://doi.org/10.1038/s41589-018-0033-4

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