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.

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.

Metrics

  • 3,034
    views
  • 392
    downloads
  • 50
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Share this article

https://doi.org/10.7554/eLife.43101

Further reading

    1. Plant Biology
    Zigmunds Orlovskis, Archana Singh ... Saskia A Hogenhout
    Research Article

    Obligate parasites often trigger significant changes in their hosts to facilitate transmission to new hosts. The molecular mechanisms behind these extended phenotypes - where genetic information of one organism is manifested as traits in another - remain largely unclear. This study explores the role of the virulence protein SAP54, produced by parasitic phytoplasmas, in attracting leafhopper vectors. SAP54 is responsible for the induction of leaf-like flowers in phytoplasma-infected plants. However, we previously demonstrated that the insects were attracted to leaves and the leaf-like flowers were not required. Here, we made the surprising discovery that leaf exposure to leafhopper males is required for the attraction phenotype, suggesting a leaf response that distinguishes leafhopper sex in the presence of SAP54. In contrast, this phytoplasma effector alongside leafhopper females discourages further female colonization. We demonstrate that SAP54 effectively suppresses biotic stress response pathways in leaves exposed to the males. Critically, the host plant MADS-box transcription factor short vegetative phase (SVP) emerges as a key element in the female leafhopper preference for plants exposed to males, with SAP54 promoting the degradation of SVP. This preference extends to female colonization of male-exposed svp null mutant plants over those not exposed to males. Our research underscores the dual role of the phytoplasma effector SAP54 in host development alteration and vector attraction - integral to the phytoplasma life cycle. Importantly, we clarify how SAP54, by targeting SVP, heightens leaf vulnerability to leafhopper males, thus facilitating female attraction and subsequent plant colonization by the insects. SAP54 essentially acts as a molecular ‘matchmaker’, helping male leafhoppers more easily locate mates by degrading SVP-containing complexes in leaves. This study not only provides insights into the long reach of single parasite genes in extended phenotypes, but also opens avenues for understanding how transcription factors that regulate plant developmental processes intersect with and influence plant-insect interactions.

    1. Microbiology and Infectious Disease
    2. Plant Biology
    Nyasha Charura, Ernesto Llamas ... Alga Zuccaro
    Research Article

    Programmed cell death occurring during plant development (dPCD) is a fundamental process integral for plant growth and reproduction. Here, we investigate the connection between developmentally controlled PCD and fungal accommodation in Arabidopsis thaliana roots, focusing on the root cap-specific transcription factor ANAC033/SOMBRERO (SMB) and the senescence-associated nuclease BFN1. Mutations of both dPCD regulators increase colonization by the beneficial fungus Serendipita indica, primarily in the differentiation zone. smb-3 mutants additionally exhibit hypercolonization around the meristematic zone and a delay of S. indica-induced root-growth promotion. This demonstrates that root cap dPCD and rapid post-mortem clearance of cellular corpses represent a physical defense mechanism restricting microbial invasion of the root. Additionally, reporter lines and transcriptional analysis revealed that BFN1 expression is downregulated during S. indica colonization in mature root epidermal cells, suggesting a transcriptional control mechanism that facilitates the accommodation of beneficial microbes in the roots.