Rapid Y degeneration and dosage compensation in plant sex chromosomes

The nonrecombining regions of animal Y chromosomes are known to undergo genetic degeneration, but previous work has failed to reveal large-scale gene degeneration on plant Y chromosomes. Here, we uncover rapid and extensive degeneration of Y-linked genes in a plant species,Silene latifolia, that evo...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 112; no. 42; pp. 13021 - 13026
Main Authors Papadopulos, Alexander S. T., Chester, Michael, Ridout, Kate, Filatov, Dmitry A.
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 20.10.2015
National Acad Sciences
Subjects
Biological Sciences
Chromosomes
Chromosomes, Plant
Dosage Compensation, Genetic
Flowers & plants
Gene expression
Genetic Linkage
Genetics
Genomes
Plants - genetics
Sex Chromosomes
Silene - genetics
Silene latifolia
Transcription factors
Y degeneration
plants
sex chromosome evolution
dosage compensation
gene expression
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Summary:The nonrecombining regions of animal Y chromosomes are known to undergo genetic degeneration, but previous work has failed to reveal large-scale gene degeneration on plant Y chromosomes. Here, we uncover rapid and extensive degeneration of Y-linked genes in a plant species,Silene latifolia, that evolved sex chromosomes de novo in the last 10 million years. Previous transcriptome-based studies of this species missed unexpressed, degenerate Y-linked genes. To identify sex-linked genes, regardless of their expression, we sequenced male and female genomes ofS. latifoliaand integrated the genomic contigs with a high-density genetic map. This revealed that 45% of Y-linked genes are not expressed, and 23% are interrupted by premature stop codons. This contrasts with X-linked genes, in which only 1.3% of genes contained stop codons and 4.3% of genes were not expressed in males. Loss of functional Y-linked genes is partly compensated for by gene-specific up-regulation of X-linked genes. Our results demonstrate that the rate of genetic degeneration of Y-linked genes inS. latifoliais as fast as in animals, and that the evolutionary trajectories of sex chromosomes are similar in the two kingdoms.
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Edited by James A. Birchler, University of Missouri-Columbia, Columbia, MO, and approved September 9, 2015 (received for review April 30, 2015)
2Present address: Royal Botanic Gardens, Kew, Richmond TW9 3AB, United Kingdom.
Author contributions: D.A.F. designed research; A.S.T.P., M.C., K.R., and D.A.F. performed research; A.S.T.P., M.C., and D.A.F. analyzed data; and A.S.T.P., M.C., and D.A.F. wrote the paper.
1A.S.T.P. and M.C. contributed equally to this work.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.1508454112