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Conservation of ethylene as a plant hormone over 450 million years of evolution

Nature Plants volume 1, Article number: 14004 (2015) Cite this article

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Abstract

Land plants evolved more than 450 million years ago from a lineage of freshwater charophyte green algae1. The extent to which plant signalling systems existed before the evolutionary transition to land is unknown. Although charophytes occupy a key phylogenetic position for elucidating the origins of such signalling systems2–4, there is a paucity of sequence data for these organisms5,6. Here we carry out de novo transcriptomics of five representative charophyte species, and find putative homologues for the biosynthesis, transport, perception and signalling of major plant hormones. Focusing on the plant hormone ethylene, we provide evidence that the filamentous charophyte Spirogyra pratensis possesses an ethylene hormone system homologous to that in plants. Spirogyra produces ethylene and exhibits a cell elongation response to ethylene. Spirogyra ethylene-signalling homologues partially rescue mutants of the angiosperm Arabidopsis thaliana and respond post-translationally to ethylene when expressed in plant cells, indicative of unambiguously homologous ethylene-signalling pathways in Spirogyra and Arabidopsis. These findings imply that the common aquatic ancestor possessed this pathway prior to the colonization of land and that cell elongation was possibly an ancestral ethylene response. This highlights the importance of charophytes for investigating the origins of fundamental plant processes.

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Figure 1: Plant phylogeny and sequence conservation of ethylene pathway genes in representative species.
Figure 2: Ethylene biosynthesis and response in Spirogyra.
Figure 3: Spirogyra homologues functionally conserved with the corresponding ER membrane-localized Arabidopsis ethylene-signalling proteins.
Figure 4: Spirogyra homologues functionally conserved with the corresponding nuclear-localized Arabidopsis ethylene-signalling proteins.

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Acknowledgements

We thank Hidetoshi Sakayama (Kobe University) for help with the Nitella transcriptome, Mark Tucker (USDA-ARS, Beltsville) for 1-MCP, Brad Binder (University of Tennessee, Knoxville) for preliminary ethylene measurements, Jocelyn Rose (Cornell University), and B. Binder and Chang lab members for comments on the manuscript. We thank the Imaging Core Facility, as well as the Institute for Bioscience and Biotechnology Research at University of Maryland. This work was supported in part by NSF grants EF0523719 (Microbial Genome Sequencing) and DEB-1036506 (Assembling the Tree of Life) to C.F.D., NSF grant MCB-0923796 to C.C., a Belgian American Educational Foundation Fellowship to B.V.d.P. and the HHMI Undergraduate Research Fellowship (from UMD) and ASPB Summer Undergraduate Fellowship to J.H.T. C.C. and C.F.D. are supported in part by the Maryland Agricultural Experiment Station.

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Author notes

  1. Bram Van de Poel & James H. Thierer

    Present address: † Present addresses: Department of Physiology, Ghent University, B-9000 Gent, Belgium (B.V.d.P.). Department of Embryology, Carnegie Institution for Science, Baltimore, Maryland 21218, USA (J.H.T.),

  2. Chuanli Ju, Bram Van de Poel, Endymion D. Cooper and James H. Thierer: These authors contributed equally to this work

Authors and Affiliations

  1. Department of Cell Biology and Molecular Genetics, University of Maryland, College Park, 20742, Maryland, USA

    Chuanli Ju, Bram Van de Poel, Endymion D. Cooper, James H. Thierer, Theodore R. Gibbons, Charles F. Delwiche & Caren Chang

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  1. Chuanli Ju
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Contributions

C.J. designed and carried out experiments in Arabidopsis, tobacco and yeast. B.V.d.P. designed and carried out experiments in Spirogyra and onion cells. E.D.C. designed and carried out bioinformatic analyses and transcriptome assembly. J.H.T. initiated the project and designed some of the experiments. T.R.G. performed initial transcriptome assembly and assisted with bioinformatic analyses. C.F.D. conceived and co-directed the project. C.C. co-directed the project and wrote the manuscript with assistance from the co-authors.

Corresponding authors

Correspondence to Charles F. Delwiche or Caren Chang.

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The authors declare no competing financial interests.

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Ju, C., Van de Poel, B., Cooper, E. et al. Conservation of ethylene as a plant hormone over 450 million years of evolution. Nature Plants 1, 14004 (2015). https://doi.org/10.1038/nplants.2014.4

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