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Genome assembly of the basket willow, Salix viminalis, reveals earliest stages of sex chromosome expansion

Almeida, Pedro and Proux-Wera, Estelle and Churcher, Allison and Soler, Lucile and Dainat, Jacques and Pucholt, Pascal and Nordlund, Jessica and Martin, Tom and Rönnberg Wästljung, Ann-Christin and Nystedt, Björn and Berlin, Sofia and Mank, Judith E. (2020). Genome assembly of the basket willow, Salix viminalis, reveals earliest stages of sex chromosome expansion. BMC Biology. 18 , 78 , 1-18
[Journal article]

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Abstract

Background: Sex chromosomes have evolved independently multiple times in eukaryotes and are therefore considered a prime example of convergent genome evolution. Sex chromosomes are known to emerge after recombination is halted between a homologous pair of chromosomes, and this leads to a range of non-adaptive modifications causing gradual degeneration and gene loss on the sex-limited chromosome. However, the proximal causes of recombination suppression and the pace at which degeneration subsequently occurs remain unclear.
Results: Here, we use long- and short-read single-molecule sequencing approaches to assemble and annotate a draft genome of the basket willow, Salix viminalis, a species with a female heterogametic system at the earliest stages of sex chromosome emergence. Our single-molecule approach allowed us to phase the emerging Z and W haplotypes in a female, and we detected very low levels of Z/W single-nucleotide divergence in the non-recombining region. Linked-read sequencing of the same female and an additional male (ZZ) revealed the presence of two evolutionary strata supported by both divergence between the Z and W haplotypes and by haplotype phylogenetic trees. Gene order is still largely conserved between the Z and W homologs, although the W-linked region contains genes involved in cytokinin signaling regulation that are not syntenic with the Z homolog. Furthermore, we find no support across multiple lines of evidence for inversions, which have long been assumed to halt recombination between the sex chromosomes.
Conclusions: Our data suggest that selection against recombination is a more gradual process at the earliest stages of sex chromosome formation than would be expected from an inversion and may result instead from the accumulation of transposable elements. Our results present a cohesive understanding of the earliest genomic consequences of recombination suppression as well as valuable insights into the initial stages of sex chromosome formation and regulation of sex differentiation.

Authors/Creators:Almeida, Pedro and Proux-Wera, Estelle and Churcher, Allison and Soler, Lucile and Dainat, Jacques and Pucholt, Pascal and Nordlund, Jessica and Martin, Tom and Rönnberg Wästljung, Ann-Christin and Nystedt, Björn and Berlin, Sofia and Mank, Judith E.
Title:Genome assembly of the basket willow, Salix viminalis, reveals earliest stages of sex chromosome expansion
Year of publishing :2020
Volume:18
Article number:78
Number of Pages:18
Publisher:BMC
ISSN:1741-7007
Language:English
Publication Type:Journal article
Article category:Scientific peer reviewed
Version:Published version
Copyright:Creative Commons: Attribution 4.0
Full Text Status:Public
Subjects:(A) Swedish standard research categories 2011 > 4 Agricultural Sciences > 404 Agricultural Biotechnology > Genetics and Breeding
Keywords:Sex chromosomes, W-chromosome, Recombination suppression, Willow, Salix
URN:NBN:urn:nbn:se:slu:epsilon-p-107060
Permanent URL:
http://urn.kb.se/resolve?urn=urn:nbn:se:slu:epsilon-p-107060
Additional ID:
Type of IDID
DOI10.1186/s12915-020-00808-1
ID Code:17378
Faculty:NJ - Fakulteten för naturresurser och jordbruksvetenskap
Department:(NL, NJ) > Dept. of Plant Biology and Forest Genetics (until 131231)
Deposited By: SLUpub Connector
Deposited On:01 Sep 2020 12:49
Metadata Last Modified:01 Sep 2020 12:49

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