1. Developmental Biology
  2. Evolutionary Biology
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Gamete expression of TALE class HD genes activates the diploid sporophyte program in Marchantia polymorpha

  1. Tom Dierschke
  2. Eduardo Flores-Sandoval
  3. Madlen I Rast-Somssich
  4. Felix Althoff
  5. Sabine Zachgo
  6. John L Bowman  Is a corresponding author
  1. Monash University, Australia
  2. University of Osnabrück, Germany
Research Article
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Cite this article as: eLife 2021;10:e57088 doi: 10.7554/eLife.57088

Abstract

Eukaryotic life cycles alternate between haploid and diploid phases and in phylogenetically diverse unicellular eukaryotes, expression of paralogous homeodomain genes in gametes primes the haploid-to-diploid transition. In the unicellular Chlorophyte alga Chlamydomonas KNOX and BELL TALE-homeodomain genes mediate this transition. We demonstrate that in the liverwort Marchantia polymorpha paternal (sperm) expression of three of five phylogenetically diverse BELL genes, MpBELL234, and maternal (egg) expression of both MpKNOX1 and MpBELL34 mediate the haploid-to-diploid transition. Loss-of-function alleles of MpKNOX1 result in zygotic arrest, whereas loss of either maternal or paternal MpBELL234 results in variable zygotic and early embryonic arrest. Expression of MpKNOX1 and MpBELL34 during diploid sporophyte development is consistent with a later role for these genes in patterning the sporophyte. These results indicate that the ancestral mechanism to activate diploid gene expression was retained in early diverging land plants and subsequently co-opted during evolution of the diploid sporophyte body.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files.

Article and author information

Author details

  1. Tom Dierschke

    School of Biological Sciences, Monash University, Melbourne, Australia
    Competing interests
    The authors declare that no competing interests exist.
  2. Eduardo Flores-Sandoval

    School of Biological Sciences, Monash University, Melbourne, Australia
    Competing interests
    The authors declare that no competing interests exist.
  3. Madlen I Rast-Somssich

    School of Biological Sciences, Monash University, Melbourne, Australia
    Competing interests
    The authors declare that no competing interests exist.
  4. Felix Althoff

    Botany Department, University of Osnabrück, Osnabrück, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Sabine Zachgo

    Botany Department, University of Osnabrück, Osnabrück, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. John L Bowman

    School of Biological Sciences, Monash University, Melbourne, Australia
    For correspondence
    John.Bowman@monash.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7347-3691

Funding

Australian Research Council (FF0551326)

  • Tom Dierschke
  • Eduardo Flores-Sandoval
  • John L Bowman

Australian Research Council (DP130100177)

  • Tom Dierschke
  • Eduardo Flores-Sandoval
  • John L Bowman

Australian Research Council (DP170100049)

  • Tom Dierschke
  • Eduardo Flores-Sandoval
  • Madlen I Rast-Somssich
  • John L Bowman

Deutsche Forschungsgemeinschaft (SFB944,P13)

  • Tom Dierschke
  • Felix Althoff
  • Sabine Zachgo

Australian Research Council (DP210101423)

  • Tom Dierschke
  • John L Bowman

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: March 20, 2020
  2. Preprint posted: April 7, 2020 (view preprint)
  3. Accepted: September 15, 2021
  4. Accepted Manuscript published: September 17, 2021 (version 1)
  5. Accepted Manuscript updated: September 20, 2021 (version 2)
  6. Version of Record published: September 27, 2021 (version 3)

Copyright

© 2021, Dierschke 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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