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Heterosis and inbreeding depression of epigenetic Arabidopsis hybrids

Nature Plants volume 1, Article number: 15092 (2015) Cite this article

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Abstract

We have addressed the possible epigenetic contribution to heterosis using epigenetic inbred lines (epiRILs) with varying levels and distributions of DNA methylation. One line consistently displayed parent-of-origin heterosis for growth-related traits. Genome-wide transcription profiling followed by a candidate gene approach revealed 33 genes with altered regulation in crosses of this line that could contribute to the observed heterosis. Although none of the candidate genes could explain hybrid vigour, we detected intriguing, hybrid-specific transcriptional regulation of the RPP5 gene, encoding a growth suppressor. RPP5 displayed intermediate transcript levels in heterotic hybrids; surprisingly however, with global loss of fitness of their F2 progeny, we observed striking under-representation of the hybrid-like intermediate levels. Thus, in addition to genetic factors contributing to heterosis, our results strongly suggest that epigenetic diversity and epigenetic regulation of transcription play a role in hybrid vigour and inbreeding depression, and also in the absence of parental genetic diversity.

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Figure 1: Heterosis of epi31 test crosses.
Figure 2: Developmental kinetics during vegetative growth.
Figure 3: Genome-wide transcription profiles of the heterotic epi31 × WT hybrids and candidate gene approach.
Figure 4: Model of heterosis and inbreeding depression of epigenetic hybrids.

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Acknowledgements

We thank all members of the Paszkowski and the LEPSE laboratory, as well as Patrick Descombes for expression profiling assistance and P. King for editing the manuscript. This work was supported by EVOBREED ERC grant 322621 and Gatsby Fellowship AT3273/GLE.

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Author notes

  1. Jon Reinders & Etienne Bucher

    Present address: †Present addresses: DuPont Pioneer, Johnston, Iowa, USA (J.R.); Université d'Angers, UMR1345 Institut de Recherche en Horticulture et Semences, Beaucouzé 49071, France (E.B.).,

Authors and Affiliations

  1. Department of Plant Biology, University of Geneva, Sciences III, Geneva 4, CH-1211, Switzerland

    Mélanie Dapp, Jon Reinders, Etienne Bucher, Gregory Theiler & Jerzy Paszkowski

  2. LEPSE unit, Campus INRA/Montpellier SupAgro, 34060, Montpellier, France

    Alexis Bédiée, Crispulo Balsera & Christine Granier

  3. The Sainsbury Laboratory, University of Cambridge, CB2 1LR, Cambridge, UK

    Jerzy Paszkowski

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Contributions

M.D., J.R. and J.P. designed the research, with the help of C.G. for the design of the phenotyping experimentations. M.D. performed the experiments, with the help of A.B., C.B. and C.G. for the phenotyping, G.T. for the statistical tests on phenotyping, and J.R. and E.B. for genome-wide annotation, expression and in silico DNA methylation analyses. M.D. and J.P. wrote the manuscript.

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Correspondence to Jerzy Paszkowski.

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The authors declare no competing financial interests.

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Dapp, M., Reinders, J., Bédiée, A. et al. Heterosis and inbreeding depression of epigenetic Arabidopsis hybrids. Nature Plants 1, 15092 (2015). https://doi.org/10.1038/nplants.2015.92

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