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Genomic imprinting mediates dosage compensation in a young plant XY system

Nature Plants volume 4, pages 677–680 (2018)Cite this article

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Abstract

Sex chromosomes have repeatedly evolved from a pair of autosomes. Consequently, X and Y chromosomes initially have similar gene content, but ongoing Y degeneration leads to reduced expression and eventual loss of Y genes1. The resulting imbalance in gene expression between Y genes and the rest of the genome is expected to reduce male fitness, especially when protein networks have components from both autosomes and sex chromosomes. A diverse set of dosage compensating mechanisms that alleviates these negative effects has been described in animals2,3,4. However, the early steps in the evolution of dosage compensation remain unknown, and dosage compensation is poorly understood in plants5. Here, we describe a dosage compensation mechanism in the evolutionarily young XY sex determination system of the plant Silene latifolia. Genomic imprinting results in higher expression from the maternal X chromosome in both males and females. This compensates for reduced Y expression in males, but results in X overexpression in females and may be detrimental. It could represent a transient early stage in the evolution of dosage compensation. Our finding has striking resemblance to the first stage proposed by Ohno6 for the evolution of X inactivation in mammals.

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Fig. 1: Normalized difference (Δ) in allelic expression levels between S. latifolia and the outgroup without sex chromosomes S. vulgaris, in autosomal and sex-linked contigs for the seedling tissue.
Fig. 2: Normalized expression difference between maternal and paternal alleles in S. latifolia females in autosomal and sex-linked SNPs in the seedling tissue.

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Acknowledgements

This project was supported through ANR grant ANR-14-CE19-0021-01 to G.A.B.M, SNSF grant 160123 to A.W. and Czech Science Agency grant 16-08698S to R.H. We thank the EMBL Genomics Core Facility (EMBL, Heidelberg) for Y-chromosome sequencing. We thank B. Gaut, T. Giraud and J. Mank for comments on the manuscript.

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Author notes

  1. These authors contributed equally: Aline Muyle, Niklaus Zemp.

Authors and Affiliations

  1. Laboratoire “Biométrie et Biologie Evolutive”, CNRS/Université Lyon 1, Lyon, France

    Aline Muyle, Cécile Fruchard, Raquel Tavares, Franck Picard & Gabriel A. B. Marais

  2. Genetic Diversity Centre (GDC), ETH Zurich, Zurich, Switzerland

    Niklaus Zemp

  3. Institute of Integrative Biology, ETH Zurich, Zurich, Switzerland

    Niklaus Zemp & Alex Widmer

  4. Institute of Biophysics of the Czech Academy of Sciences, Brno, Czech Republic

    Radim Cegan & Roman Hobza

  5. Institute of Experimental Botany, Center of the Hana Region for Biotechnological and Agricultural Research, Olomouc, Czech Republic

    Jan Vrana & Roman Hobza

  6. Center for Bioinformatics in Rhônes-Alpes (PRABI), Lyon, France

    Clothilde Deschamps

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Contributions

A.M., N.Z., A.W. and G.A.B.M. conceived the study and experimental design. N.Z. and A.W. prepared and sequenced the plant material. A.M. ran SEX-DETector on the RNA-seq datasets for the three tissues, analysed the data, prepared tables and figures, and wrote the Supplementary Information with input from the other authors. N.Z. generated the X-chromosome genetic map. R.C., J.V. and R.H. did the Y-chromosome flow cytometry sorting and sequencing. C.D. did the first assembly of the sorted Y chromosome and improved it with RNA-seq data with the help of C.F. A.M. did the blasts to validate the inferences of SEX-DETector. R.T. did the GO term analysis. A.M. and F.P. did the statistical analyses of the data. G.A.B.M. and A.M. wrote the main text of the manuscript with input from the other authors.

Corresponding author

Correspondence to Aline Muyle.

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The authors declare no competing interests.

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Supplementary Information

Supplementary Information

Supplementary Text, Supplementary References, Supplementary Figures 1–16, and Supplementary Tables 1 and 3.

Reporting Summary

Supplementary Table 2

Mapping statistics. Library sizes (number of reads) and percentage of mapped reads of each individual.

Supplementary Table 4

Known sex-linked genes in S. latifolia. Gene names, transcripts and associated literature references are listed.

Supplementary Table 5

GO-terms and expression levels of seedling sex-linked transcripts. For each sex-linked transcript in seedlings, the mean Y over X expression ratio in males is given followed by the mean male over female expression, the mean paternal allele expression in females, the mean maternal allele expression in females and in males, the mean Y allele expression and the mean outgroup expression (S. vulgaris). This is followed by GO analysis output: number of hits, GO names, Enzyme names and InterPro GO names.

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Muyle, A., Zemp, N., Fruchard, C. et al. Genomic imprinting mediates dosage compensation in a young plant XY system. Nature Plants 4, 677–680 (2018). https://doi.org/10.1038/s41477-018-0221-y

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