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Evolution of sex-biased gene expression in a dioecious plant

Nature Plants volume 2, Article number: 16168 (2016) Cite this article

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Abstract

Separate sexes and sex-biased gene expression have repeatedly evolved in animals and plants, but the underlying changes in gene expression remain unknown. Here, we studied a pair of plant species, one in which separate sexes and sex chromosomes evolved recently and one which maintained hermaphrodite flowers resembling the ancestral state, to reconstruct expression changes associated with the evolution of dioecy. We found that sex-biased gene expression has evolved in autosomal and sex-linked genes in the dioecious species. Most expression changes relative to hermaphrodite flowers occurred in females rather than males, with higher and lower expression in females leading to female-biased and male-biased expression, respectively. Expression changes were more common in genes located on the sex chromosomes than the autosomes and led to feminization of the X chromosome and masculinization of the Y chromosome. Our results support a scenario in which sex-biased gene expression evolved during the evolution of dioecy to resolve intralocus sexual conflicts over the allocation of resources.

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Figure 1: Hypothetical scenarios for the evolution of sex-biased gene expression.
Figure 2: Sexual dimorphism and sex-biased gene expression in S. latifolia.
Figure 3: Expression changes in genes with sex-biased expression in S. latifolia.
Figure 4: Evolutionary changes leading to sex-biased gene expression in S. latifolia.
Figure 5: Tertiary expression changes on S. latifolia sex chromosomes.

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Acknowledgements

This work was funded through SNF projects 141260 and 160123 to A.W. and the French National Research Agency ANR-11-BSV7-013-03 to G.A.B.M. We thank C. Michel for laboratory support, S. Zoller from the ETH Zurich Genetic Diversity Centre (GDC) for assembling the reference transcriptome and members of the Plant Ecological Genetics group for insightful discussions. We thank M.C. Fischer for providing pictures of S. latifolia and M. Frei for taking care of all plants. Data produced and analysed in this paper were generated in collaboration with the GDC.

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Authors and Affiliations

  1. ETH Zurich, Institute of Integrative Biology, Universitätstrasse 16, 8092 Zürich, Switzerland

    Niklaus Zemp & Alex Widmer

  2. Université Lyon 1, CNRS, UMR 5558, Laboratoire de Biométrie et Biologie Evolutive, F-69622 Villeurbanne, France

    Raquel Tavares, Aline Muyle & Gabriel A. B. Marais

  3. University of Edinburgh, Institute of Evolutionary Biology, Edinburgh EH9 3JT, UK

    Deborah Charlesworth

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  1. Niklaus Zemp
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Contributions

Designed the experiments and formulated predictions: N.Z., A.W., G.A.B.M., D.C.; performed the experiments: N.Z.; analysed the data: N.Z., R.T., A.M.; wrote the manuscript: N.Z., A.W., D.C., G.A.B.M., R.T., A.M.

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Correspondence to Alex Widmer.

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Supplementary Methods, Supplementary References, Supplementary Figures 1–9, Supplementary Tables 1–3 (PDF 1795 kb)

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Zemp, N., Tavares, R., Muyle, A. et al. Evolution of sex-biased gene expression in a dioecious plant. Nature Plants 2, 16168 (2016). https://doi.org/10.1038/nplants.2016.168

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