Gamete fertility and ovule number variation in selfed reciprocal F1 hybrid triploid plants are heritable and display epigenetic parent-of-origin effects

Authors

  • Dorota Duszynska,

    1. Plant and AgriBiosciences Centre (PABC), School of Natural Sciences, National University of Ireland Galway, Galway, Ireland
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    • These authors contributed equally to this work.
  • Peter C. McKeown,

    1. Plant and AgriBiosciences Centre (PABC), School of Natural Sciences, National University of Ireland Galway, Galway, Ireland
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    • These authors contributed equally to this work.
  • Thomas E. Juenger,

    1. Section of Integrative Biology & Institute for Cellular and Molecular Biology, University of Texas, Austin, TX, USA
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  • Anna Pietraszewska-Bogiel,

    1. Plant and AgriBiosciences Centre (PABC), School of Natural Sciences, National University of Ireland Galway, Galway, Ireland
    2. Molecular Cytology, Swammerdam Institute for Life Sciences (SILS), University of Amsterdam, Amsterdam, the Netherlands
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  • Danny Geelen,

    1. Department of Plant Production, Faculty of Bioscience Engineering, University of Ghent, Ghent, Belgium
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  • Charles Spillane

    Corresponding author
    • Plant and AgriBiosciences Centre (PABC), School of Natural Sciences, National University of Ireland Galway, Galway, Ireland
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Author for correspondence:

Charles Spillane

Tel: +353 91 494148

Email: charles.spillane@nuigalway.ie

Summary

  • Polyploidy and hybridization play major roles in plant evolution and reproduction. To investigate the reproductive effects of polyploidy and hybridization in Arabidopsis thaliana, we analyzed fertility of reciprocal pairs of F1 hybrid triploids, generated by reciprocally crossing 89 diploid accessions to a tetraploid Ler-0 line.
  • All F1 hybrid triploid genotypes exhibited dramatically reduced ovule fertility, while variation in ovule number per silique was observed across different F1 triploid genotypes. These two reproductive traits were negatively correlated suggesting a trade-off between increased ovule number and ovule fertility. Furthermore, the ovule fertility of the F1 hybrid triploids displayed both hybrid dysgenesis and hybrid advantage (heterosis) effects.
  • Strikingly, both reproductive traits (ovule fertility, ovule number) displayed epigenetic parent-of-origin effects between genetically identical reciprocal F1 hybrid triploid pairs. In some F1 triploid genotypes, the maternal genome excess F1 hybrid triploid was more fertile, whilst for other accessions the paternal genome excess F1 hybrid triploid was more fertile.
  • Male gametogenesis was not significantly disrupted in F1 triploids. Fertility variation in the F1 triploid A. thaliana is mainly the result of disrupted ovule development. Overall, we demonstrate that in F1 triploid plants both ovule fertility and ovule number are subject to parent-of-origin effects that are genome dosage-dependent.

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