A gradual process of recombination restriction in the evolutionary history of the sex chromosomes in dioecious plants.

To help understand the evolution of suppressed recombination between sex chromosomes, and its consequences for evolution of the sequences of Y-linked genes, we have studied four X-Y gene pairs, including one gene not previously characterized, in plants in a group of closely related dioecious species...

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Main Authors: Michael Nicolas, Gabriel Marais, Vladka Hykelova, Bohuslav Janousek, Valérie Laporte, Boris Vyskot, Dominique Mouchiroud, Ioan Negrutiu, Deborah Charlesworth, Françoise Monéger
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2005-01-01
Series:PLoS Biology
Online Access:http://europepmc.org/articles/PMC536007?pdf=render
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spelling doaj-97291440cce04dfd9f850f5e882ba33f2021-07-02T02:27:38ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852005-01-0131e410.1371/journal.pbio.0030004A gradual process of recombination restriction in the evolutionary history of the sex chromosomes in dioecious plants.Michael NicolasGabriel MaraisVladka HykelovaBohuslav JanousekValérie LaporteBoris VyskotDominique MouchiroudIoan NegrutiuDeborah CharlesworthFrançoise MonégerTo help understand the evolution of suppressed recombination between sex chromosomes, and its consequences for evolution of the sequences of Y-linked genes, we have studied four X-Y gene pairs, including one gene not previously characterized, in plants in a group of closely related dioecious species of Silene which have an X-Y sex-determining system (S. latifolia, S. dioica, and S. diclinis). We used the X-linked copies to build a genetic map of the X chromosomes, with a marker in the pseudoautosomal region (PAR) to orient the map. The map covers a large part of the X chromosomes--at least 50 centimorgans. Except for a recent rearrangement in S. dioica, the gene order is the same in the X chromosomes of all three species. Silent site divergence between the DNA sequences of the X and Y copies of the different genes increases with the genes' distances from the PAR, suggesting progressive restriction of recombination between the X and Y chromosomes. This was confirmed by phylogenetic analyses of the four genes, which also revealed that the least-diverged X-Y pair could have ceased recombining independently in the dioecious species after their split. Analysis of amino acid replacements vs. synonymous changes showed that, with one possible exception, the Y-linked copies appear to be functional in all three species, but there are nevertheless some signs of degenerative processes affecting the genes that have been Y-linked for the longest times. Although the X-Y system evolved quite recently in Silene (less than 10 million years ago) compared to mammals (about 320 million years ago), our results suggest that similar processes have been at work in the evolution of sex chromosomes in plants and mammals, and shed some light on the molecular mechanisms suppressing recombination between X and Y chromosomes.http://europepmc.org/articles/PMC536007?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Michael Nicolas
Gabriel Marais
Vladka Hykelova
Bohuslav Janousek
Valérie Laporte
Boris Vyskot
Dominique Mouchiroud
Ioan Negrutiu
Deborah Charlesworth
Françoise Monéger
spellingShingle Michael Nicolas
Gabriel Marais
Vladka Hykelova
Bohuslav Janousek
Valérie Laporte
Boris Vyskot
Dominique Mouchiroud
Ioan Negrutiu
Deborah Charlesworth
Françoise Monéger
A gradual process of recombination restriction in the evolutionary history of the sex chromosomes in dioecious plants.
PLoS Biology
author_facet Michael Nicolas
Gabriel Marais
Vladka Hykelova
Bohuslav Janousek
Valérie Laporte
Boris Vyskot
Dominique Mouchiroud
Ioan Negrutiu
Deborah Charlesworth
Françoise Monéger
author_sort Michael Nicolas
title A gradual process of recombination restriction in the evolutionary history of the sex chromosomes in dioecious plants.
title_short A gradual process of recombination restriction in the evolutionary history of the sex chromosomes in dioecious plants.
title_full A gradual process of recombination restriction in the evolutionary history of the sex chromosomes in dioecious plants.
title_fullStr A gradual process of recombination restriction in the evolutionary history of the sex chromosomes in dioecious plants.
title_full_unstemmed A gradual process of recombination restriction in the evolutionary history of the sex chromosomes in dioecious plants.
title_sort gradual process of recombination restriction in the evolutionary history of the sex chromosomes in dioecious plants.
publisher Public Library of Science (PLoS)
series PLoS Biology
issn 1544-9173
1545-7885
publishDate 2005-01-01
description To help understand the evolution of suppressed recombination between sex chromosomes, and its consequences for evolution of the sequences of Y-linked genes, we have studied four X-Y gene pairs, including one gene not previously characterized, in plants in a group of closely related dioecious species of Silene which have an X-Y sex-determining system (S. latifolia, S. dioica, and S. diclinis). We used the X-linked copies to build a genetic map of the X chromosomes, with a marker in the pseudoautosomal region (PAR) to orient the map. The map covers a large part of the X chromosomes--at least 50 centimorgans. Except for a recent rearrangement in S. dioica, the gene order is the same in the X chromosomes of all three species. Silent site divergence between the DNA sequences of the X and Y copies of the different genes increases with the genes' distances from the PAR, suggesting progressive restriction of recombination between the X and Y chromosomes. This was confirmed by phylogenetic analyses of the four genes, which also revealed that the least-diverged X-Y pair could have ceased recombining independently in the dioecious species after their split. Analysis of amino acid replacements vs. synonymous changes showed that, with one possible exception, the Y-linked copies appear to be functional in all three species, but there are nevertheless some signs of degenerative processes affecting the genes that have been Y-linked for the longest times. Although the X-Y system evolved quite recently in Silene (less than 10 million years ago) compared to mammals (about 320 million years ago), our results suggest that similar processes have been at work in the evolution of sex chromosomes in plants and mammals, and shed some light on the molecular mechanisms suppressing recombination between X and Y chromosomes.
url http://europepmc.org/articles/PMC536007?pdf=render
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