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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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References

  1. Sanderson, M. J., Thorne, J. L., Wikström, N. & Bremer, K. Molecular evidence on plant divergence times. Am. J. Bot. 91, 1656–1665 (2004).

    Article  CAS  Google Scholar 

  2. Karol, K. G., McCourt, R. M., Cimino, M. T. & Delwiche, C. F. The closest living relatives of land plants. Science 294, 2351–2353 (2001).

    Article  CAS  Google Scholar 

  3. Turmel, M., Ehara, M., Otis, C. & Lemieux, C. Phylogenetic relationships among streptophytes as inferred from chloroplast small and large subunit rRNA gene sequences. J. Phycol. 38, 364–375 (2002).

    Article  Google Scholar 

  4. Leliaert, F. et al. Phylogeny and molecular evolution of the green algae. Crit. Rev. Plant Sci. 31, 1–46 (2012).

    Article  Google Scholar 

  5. Timme, R. E. & Delwiche, C. F. Uncovering the evolutionary origin of plant molecular processes: comparison of Coleochaete (Coleochaetales) and Spirogyra (Zygnematales) transcriptomes. BMC Plant Biol. 10, 96 (2010).

    Article  Google Scholar 

  6. Wodniok, S. et al. Origin of land plants: Do conjugating green algae hold the key? BMC Evol. Biol. 11, 104 (2011).

    Article  Google Scholar 

  7. McManus, M. T. Annual Plant Reviews, The Plant Hormone Ethylene (Wiley-Blackwell, 2012).

  8. Jackson, M. B. Ethylene-promoted elongation: an adaptation to submergence stress. Ann. Bot. 101, 229–248 (2008).

    Article  CAS  Google Scholar 

  9. Merchante, C., Alonso, J. M. & Stepanova, A. N. Ethylene signaling: simple ligand, complex regulation. Curr. Opin. Plant Biol. 16, 554–560 (2013).

    Article  CAS  Google Scholar 

  10. Mount, S. M. & Chang, C. Evidence for a plastid origin of plant ethylene receptor genes. Plant Physiol. 130, 10–14 (2002).

    Article  CAS  Google Scholar 

  11. Wang, W. et al. Identification of important regions for ethylene binding and signaling in the transmembrane domain of the ETR1 ethylene receptor of Arabidopsis. Plant Cell 18, 3429–3442 (2006).

    Article  CAS  Google Scholar 

  12. Timme, R. E., Bachvaroff, T. R. & Delwiche, C. F. Broad phylogenomic sampling and the sister lineage of land plants. PLoS ONE 7, e29696. (2012).

    Article  CAS  Google Scholar 

  13. Hori, K. et al. Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation. Nature Commun. 5, 3978. (2014).

    Article  CAS  Google Scholar 

  14. Yang, S. F. & Hoffman, N. E. Ethylene biosynthesis and its regulation in higher plants. Ann. Rev. Plant Physiol. 35, 155–189 (1984).

    Article  CAS  Google Scholar 

  15. Garcia-Jimenez, P. & Robaina, R. R. Effects of ethylene on tetrasporogenesis in Pterocladiella capillacea (Rhodophyta). J. Phycol. 48, 710–715 (2012).

    Article  CAS  Google Scholar 

  16. Maillard, P., Thepenier, C. & Gudin, C. Determination of an ethylene biosynthesis pathway in the unicellular green alga, Haematococcus pluvialis. Relationship between growth and ethylene production. J. Appl. Phycol. 5, 93–98 (1993).

    Article  CAS  Google Scholar 

  17. Huang, T.-C. & Chow, T.-J. Ethylene production by blue-green algae. Bot. Bull. Academia Sinica 25, 81–86 (1984).

    CAS  Google Scholar 

  18. Bleecker, A. B., Estelle, M. A., Somerville, C. & Kende, H. Insensitivity to ethylene conferred by a dominant mutation in Arabidopsis thaliana. Science 241, 1086–1089 (1988).

    Article  CAS  Google Scholar 

  19. Blankenship, S. M. & Dole, J. M. 1-methylcyclopropene: a review. Postharv. Biol. Technol. 28, 1–25 (2003).

    Article  CAS  Google Scholar 

  20. Yasumura, Y. et al. Studies of Physcomitrella patens reveal that ethylene-mediated submergence responses arose relatively early in land-plant evolution. Plant J. 72, 947–959 (2012).

    Article  CAS  Google Scholar 

  21. Smalle, J., Haegman, M., Kurepa, J., Van Montagu, M. & Van Der Straeten, D. Ethylene can stimulate Arabidopsis hypocotyl elongation in the light. Proc. Natl Acad. Sci. USA 94, 2756–2761 (1997).

    Article  CAS  Google Scholar 

  22. Chen, Y. F., Randlett, M. D., Findell, J. L. & Schaller, G. E. Localization of the ethylene receptor ETR1 to the endoplasmic reticulum of Arabidopsis. J. Biol. Chem. 277, 19861–19866 (2002).

    Article  CAS  Google Scholar 

  23. Grefen, C. et al. Subcellular localization and in vivo interaction of the Arabidopsis thaliana ethylene receptor family members. Molecular Plant 1, 308–320 (2008).

    Article  CAS  Google Scholar 

  24. Clark, K. L., Larsen, P. B., Wang, X. & Chang, C. Association of the Arabidopsis CTR1 Raf-like kinase with the ETR1 and ERS ethylene receptors. Proc. Natl Acad. Sci. USA 95, 5401–5406 (1998).

    Article  CAS  Google Scholar 

  25. Gao, Z et al. Localization of the Raf-like kinase CTR1 to the endoplasmic reticulum of Arabidopsis through participation in ethylene receptor signaling complexes. J. Biol. Chem. 278, 34725–34732 (2003).

    Article  CAS  Google Scholar 

  26. Ju, C. et al. CTR1 phosphorylates the central regulator EIN2 to control ethylene hormone signaling from the ER membrane to the nucleus in Arabidopsis. Proc. Natl Acad. Sci. USA 109, 19486–19491 (2012).

    Article  CAS  Google Scholar 

  27. Alonso, J. M. et al. EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science 284, 2148–2152 (1999).

    Article  CAS  Google Scholar 

  28. Qiao, H. et al. Processing and subcellular trafficking of ER-tethered EIN2 control response to ethylene gas. Science 338, 390–393 (2012).

    Article  CAS  Google Scholar 

  29. Guo, H. & Ecker, J. R. Plant responses to ethylene gas are mediated by SCFEBF1/EBF2-dependent proteolysis of EIN3 transcription factor. Cell 115, 667–677 (2003).

    Article  CAS  Google Scholar 

  30. Chao, Q. et al. Activation of the ethylene gas response pathway in Arabidopsis by the nuclear protein ETHYLENE-INSENSITIVE3 and related proteins. Cell 89, 1133–1144 (1997).

    Article  CAS  Google Scholar 

  31. Solano, R., Stepanova, A., Chao, Q. & Ecker, J. R. Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSE-FACTOR1. Genes Dev. 12, 3703–3714 (1998).

    Article  CAS  Google Scholar 

  32. Hua, J. & Meyerowitz, E. M. Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana. Cell 94, 261–271 (1998).

    Article  CAS  Google Scholar 

  33. Nakano, T., Suzuki, K., Fujimura, T. & Shinshi, H. Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol. 140, 411–432 (2006).

    Article  CAS  Google Scholar 

  34. Sakayama, H., Hara,Y. & Nozaki, H. Taxonomic re-examination of six species of Nitella (Charales, Charophyceae) from Asia, and phylogenetic relationships within the genus based on rbcL and atpB gene sequences. Phycologia 43, 91–104 (2004).

    Article  Google Scholar 

  35. Grabherr, M. G. et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnol. 29, 644–652 (2011).

    Article  CAS  Google Scholar 

  36. Voinnet, O., Rivas, S., Mestre, P. & Baulcombe, D. An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J. 33, 949–956 (2003).

    Article  CAS  Google Scholar 

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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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