ECS1 and ECS2 suppress polyspermy and the formation of haploid plants by promoting double fertilization

Abstract

The current pace of crop plant optimization is insufficient to meet future demands and there is an urgent need for novel breeding strategies. It was previously shown that plants tolerate the generation of triparental polyspermy-derived plants and that polyspermy can bypass hybridization barriers. Polyspermy thus has the potential to harness previously incompatible climate adapted wild varieties for plant breeding. However, factors that influence polyspermy frequencies were not previously known. The endopeptidases ECS1 and ECS2 have been reported to prevent the attraction of supernumerary pollen tubes by cleaving the pollen tube attractant LURE1. Here we show that these genes have an earlier function that is manifested by incomplete double fertilization in plants defective for both genes. In addition to supernumerary pollen tube attraction, ecs1 ecs2 mutants exhibit a delay in synergid disintegration, are susceptible to heterofertilization, and segregate haploid plants that lack a paternal genome contribution. Our results thus uncover ECS1 and ECS2 as the first female factors triggering the induction of maternal haploids. Capitalizing on a high-throughput polyspermy assay, we in addition show that the double mutant exhibits a three-fold increase in polyspermy frequencies. As both haploid induction and polyspermy are valuable breeding aims, our results open new avenues for accelerated generation of climate adapted cultivars.

Data availability

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

Article and author information

Author details

  1. Yanbo Mao

    Centre for Biomolecular Interactions, University of Bremen, Bremen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5520-8202
  2. Thomas Nakel

    Centre for Biomolecular Interactions, University of Bremen, Bremen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9033-5987
  3. Isil Erbasol Serbes

    Centre for Biomolecular Interactions, University of Bremen, Bremen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7854-1243
  4. Saurabh Joshi

    Centre for Biomolecular Interactions, University of Bremen, Bremen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4354-6762
  5. Dawit Girma Tekleyohans

    Centre for Biomolecular Interactions, University of Bremen, Bremen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7383-5971
  6. Thomas Baum

    Centre for Biomolecular Interactions, University of Bremen, Bremen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Rita Groß-Hardt

    Centre for Biomolecular Interactions, University of Bremen, Bremen, Germany
    For correspondence
    gross-hardt@uni-bremen.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1998-0507

Funding

European Research Council (646644)

  • Rita Groß-Hardt

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

Reviewing Editor

  1. Hao Yu, National University of Singapore & Temasek Life Sciences Laboratory, Singapore

Version history

  1. Preprint posted: January 22, 2022 (view preprint)
  2. Received: December 28, 2022
  3. Accepted: July 24, 2023
  4. Accepted Manuscript published: July 25, 2023 (version 1)
  5. Version of Record published: August 11, 2023 (version 2)

Copyright

© 2023, Mao 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. Yanbo Mao
  2. Thomas Nakel
  3. Isil Erbasol Serbes
  4. Saurabh Joshi
  5. Dawit Girma Tekleyohans
  6. Thomas Baum
  7. Rita Groß-Hardt
(2023)
ECS1 and ECS2 suppress polyspermy and the formation of haploid plants by promoting double fertilization
eLife 12:e85832.
https://doi.org/10.7554/eLife.85832

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