Convergent recruitment of TALE homeodomain life cycle regulators to direct sporophyte development in land plants and brown algae

  1. Alok Arun
  2. Susana M Coelho
  3. Akira F Peters
  4. Simon Bourdareau
  5. Laurent Pérès
  6. Delphine Scornet
  7. Martina Strittmatter
  8. Agnieszka P Lipinska
  9. Haiqin Yao
  10. Olivier Godfroy
  11. Gabriel J Montecinos
  12. Komlan Avia
  13. Nicolas Macaisne
  14. Christelle Troadec
  15. Abdelhafid Bendahmane
  16. J Mark Cock  Is a corresponding author
  1. French National Centre for Scientific Research, France
  2. Bezhin Rosko, France
  3. Collège de France, France
  4. Institut National de la Recherche Agronomique, France

Abstract

Three amino acid loop extension homeodomain transcription factors (TALE HD TFs) act as life cycle regulators in green algae and land plants. In mosses these regulators are required for the deployment of the sporophyte developmental program. We demonstrate that mutations in either of two TALE HD TF genes, OUROBOROS or SAMSARA, in the brown alga Ectocarpus result in conversion of the sporophyte generation into a gametophyte. The OUROBOROS and SAMSARA proteins heterodimerise in a similar manner to TALE HD TF life cycle regulators in the green lineage. These observations demonstrate that TALE-HD-TF-based life cycle regulation systems have an extremely ancient origin, and that these systems have been independently recruited to regulate sporophyte developmental programs in at least two different complex multicellular eukaryotic supergroups, Archaeplastida and Chromalveolata.

Data availability

All the sequencing data that has been generated by or used in this study is described in Supplementary file 9. SRA accession numbers are provided for all samples. Genbank accession numbers for the corrected ORO and SAM genes are provided in the results section.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Alok Arun

    UMR8227, French National Centre for Scientific Research, Roscoff, France
    Competing interests
    The authors declare that no competing interests exist.
  2. Susana M Coelho

    UMR8227, French National Centre for Scientific Research, Roscoff, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9171-2550
  3. Akira F Peters

    Algal Culture, Bezhin Rosko, Santec, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Simon Bourdareau

    UMR8227, French National Centre for Scientific Research, Roscoff, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Laurent Pérès

    UMR8227, French National Centre for Scientific Research, Roscoff, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6016-4785
  6. Delphine Scornet

    UMR8227, French National Centre for Scientific Research, Roscoff, France
    Competing interests
    The authors declare that no competing interests exist.
  7. Martina Strittmatter

    UMR8227, French National Centre for Scientific Research, Roscoff, France
    Competing interests
    The authors declare that no competing interests exist.
  8. Agnieszka P Lipinska

    UMR8227, French National Centre for Scientific Research, Roscoff, France
    Competing interests
    The authors declare that no competing interests exist.
  9. Haiqin Yao

    UMR8227, French National Centre for Scientific Research, Roscoff, France
    Competing interests
    The authors declare that no competing interests exist.
  10. Olivier Godfroy

    UMR8227, French National Centre for Scientific Research, Roscoff, France
    Competing interests
    The authors declare that no competing interests exist.
  11. Gabriel J Montecinos

    UMR8227, French National Centre for Scientific Research, Roscoff, France
    Competing interests
    The authors declare that no competing interests exist.
  12. Komlan Avia

    UMR8227, French National Centre for Scientific Research, Roscoff, France
    Competing interests
    The authors declare that no competing interests exist.
  13. Nicolas Macaisne

    UMR CNRS 7241 / INSERM U1050, Collège de France, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0109-9845
  14. Christelle Troadec

    Institute of Plant Sciences Paris-Saclay, Institut National de la Recherche Agronomique, Orsay, France
    Competing interests
    The authors declare that no competing interests exist.
  15. Abdelhafid Bendahmane

    Institute of Plant Sciences Paris-Saclay, Institut National de la Recherche Agronomique, Orsay, France
    Competing interests
    The authors declare that no competing interests exist.
  16. J Mark Cock

    UMR8227, French National Centre for Scientific Research, Roscoff, France
    For correspondence
    cock@sb-roscoff.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2650-0383

Funding

Centre National de la Recherche Scientifique

  • Alok Arun
  • Susana M Coelho
  • Akira F Peters
  • Simon Bourdareau
  • Laurent Pérès
  • Delphine Scornet
  • Martina Strittmatter
  • Agnieszka P Lipinska
  • Haiqin Yao
  • Olivier Godfroy
  • Gabriel J Montecinos
  • Komlan Avia
  • Nicolas Macaisne
  • Christelle Troadec
  • Abdelhafid Bendahmane
  • J Mark Cock

European Research Council (ERC-SEXYPARTH)

  • Abdelhafid Bendahmane

Agence Nationale de la Recherche (ANR-10-BLAN-1727)

  • J Mark Cock

Interreg Program France -England (Marinexus)

  • J Mark Cock

University Pierre and Marie Curie

  • Alok Arun
  • Susana M Coelho
  • Akira F Peters
  • Simon Bourdareau
  • Laurent Pérès
  • Delphine Scornet
  • Martina Strittmatter
  • Agnieszka P Lipinska
  • Haiqin Yao
  • Olivier Godfroy
  • Gabriel J Montecinos
  • Komlan Avia
  • Nicolas Macaisne
  • J Mark Cock

European Research Council (638240)

  • Susana M Coelho

European Erasmus Mundus program

  • J Mark Cock

China Scholarship Council

  • J Mark Cock

Agence Nationale de la Recherche (ANR-10-BTBR-04-01)

  • J Mark Cock

Agence Nationale de la Recherche (ANR-10-LABX-40)

  • Abdelhafid Bendahmane

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Sheila McCormick, University of California, Berkeley, United States

Publication history

  1. Received: October 24, 2018
  2. Accepted: January 13, 2019
  3. Accepted Manuscript published: January 15, 2019 (version 1)
  4. Version of Record published: February 8, 2019 (version 2)
  5. Version of Record updated: March 18, 2019 (version 3)

Copyright

© 2019, Arun et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Alok Arun
  2. Susana M Coelho
  3. Akira F Peters
  4. Simon Bourdareau
  5. Laurent Pérès
  6. Delphine Scornet
  7. Martina Strittmatter
  8. Agnieszka P Lipinska
  9. Haiqin Yao
  10. Olivier Godfroy
  11. Gabriel J Montecinos
  12. Komlan Avia
  13. Nicolas Macaisne
  14. Christelle Troadec
  15. Abdelhafid Bendahmane
  16. J Mark Cock
(2019)
Convergent recruitment of TALE homeodomain life cycle regulators to direct sporophyte development in land plants and brown algae
eLife 8:e43101.
https://doi.org/10.7554/eLife.43101
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