Pericentromeric recombination suppression and the ‘large X effect’ in plants

Abstract X chromosome was reported to be a major contributor to isolation between closely related species—the ‘large X’ effect (LXE). The causes of LXE are not clear, but the leading theory is that it is caused by recessive species incompatibilities exposed in the phenotype due to the hemizygosity o...

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Main Authors: Edgar L. Y. Wong, Dmitry A. Filatov
Format: Article
Language:English
Published: Nature Portfolio 2023-12-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-023-48870-3
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author Edgar L. Y. Wong
Dmitry A. Filatov
author_facet Edgar L. Y. Wong
Dmitry A. Filatov
author_sort Edgar L. Y. Wong
collection DOAJ
description Abstract X chromosome was reported to be a major contributor to isolation between closely related species—the ‘large X’ effect (LXE). The causes of LXE are not clear, but the leading theory is that it is caused by recessive species incompatibilities exposed in the phenotype due to the hemizygosity of X-linked genes in the heterogametic sex. However, the LXE was also reported in species with relatively recently evolved sex chromosomes where Y chromosome is not completely degenerate and X-linked genes are not hemizygous, such as the plant Silene latifolia. Recent genome sequencing and detailed genetic mapping in this species revealed a massive (> 330 Mb) non- or rarely-recombining pericentromeric region on the X chromosome (Xpr) that comprises ~ 90% of the chromosome and over 13% of the entire genome. If any of the Xpr genes are involved in species incompatibilities, this would oppose interspecific gene flow for other genes tightly linked in the Xpr. Here we test the hypothesis that the previously reported LXE in S. latifolia is caused by the lack of recombination on most of the X chromosome. Based on genome-wide analysis of DNA polymorphism and gene expression in S. latifolia and its close cross-compatible relative S. dioica, we report that the rarely-recombining regions represent a significant barrier for interspecific gene flow. We found little evidence for any additional factors contributing to the LXE, suggesting that extensive pericentromeric recombination suppression on the X-chromosome is the major if not the only cause of the LXE in S. latifolia and S. dioica.
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spelling doaj.art-d22d4844dcc543278ef1f261224a2b402023-12-10T12:16:00ZengNature PortfolioScientific Reports2045-23222023-12-0113111210.1038/s41598-023-48870-3Pericentromeric recombination suppression and the ‘large X effect’ in plantsEdgar L. Y. Wong0Dmitry A. Filatov1Department of Biology, University of OxfordDepartment of Biology, University of OxfordAbstract X chromosome was reported to be a major contributor to isolation between closely related species—the ‘large X’ effect (LXE). The causes of LXE are not clear, but the leading theory is that it is caused by recessive species incompatibilities exposed in the phenotype due to the hemizygosity of X-linked genes in the heterogametic sex. However, the LXE was also reported in species with relatively recently evolved sex chromosomes where Y chromosome is not completely degenerate and X-linked genes are not hemizygous, such as the plant Silene latifolia. Recent genome sequencing and detailed genetic mapping in this species revealed a massive (> 330 Mb) non- or rarely-recombining pericentromeric region on the X chromosome (Xpr) that comprises ~ 90% of the chromosome and over 13% of the entire genome. If any of the Xpr genes are involved in species incompatibilities, this would oppose interspecific gene flow for other genes tightly linked in the Xpr. Here we test the hypothesis that the previously reported LXE in S. latifolia is caused by the lack of recombination on most of the X chromosome. Based on genome-wide analysis of DNA polymorphism and gene expression in S. latifolia and its close cross-compatible relative S. dioica, we report that the rarely-recombining regions represent a significant barrier for interspecific gene flow. We found little evidence for any additional factors contributing to the LXE, suggesting that extensive pericentromeric recombination suppression on the X-chromosome is the major if not the only cause of the LXE in S. latifolia and S. dioica.https://doi.org/10.1038/s41598-023-48870-3
spellingShingle Edgar L. Y. Wong
Dmitry A. Filatov
Pericentromeric recombination suppression and the ‘large X effect’ in plants
Scientific Reports
title Pericentromeric recombination suppression and the ‘large X effect’ in plants
title_full Pericentromeric recombination suppression and the ‘large X effect’ in plants
title_fullStr Pericentromeric recombination suppression and the ‘large X effect’ in plants
title_full_unstemmed Pericentromeric recombination suppression and the ‘large X effect’ in plants
title_short Pericentromeric recombination suppression and the ‘large X effect’ in plants
title_sort pericentromeric recombination suppression and the large x effect in plants
url https://doi.org/10.1038/s41598-023-48870-3
work_keys_str_mv AT edgarlywong pericentromericrecombinationsuppressionandthelargexeffectinplants
AT dmitryafilatov pericentromericrecombinationsuppressionandthelargexeffectinplants