Evolutionary strata on young mating-type chromosomes despite the lack of sexual antagonism
Sex chromosomes can display successive steps of recombination suppression known as “evolutionary strata,” which are thought to result from the successive linkage of sexually antagonistic genes to sex-determining genes. However, there is little evidence to support this explanation. Here we investigat...
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| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2017-07, Vol.114 (27), p.7067-7072 |
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| creator | Branco, Sara Badouin, Hélène de la Vega, Ricardo C. Rodríguez Gouzy, Jérôme Carpentier, Fantin Aguileta, Gabriela Siguenza, Sophie Brandenburg, Jean-Tristan Coelho, Marco A. Hood, Michael E. Giraud, Tatiana |
| description | Sex chromosomes can display successive steps of recombination suppression known as “evolutionary strata,” which are thought to result from the successive linkage of sexually antagonistic genes to sex-determining genes. However, there is little evidence to support this explanation. Here we investigate whether evolutionary strata can evolve without sexual antagonism using fungi that display suppressed recombination extending beyond loci determining mating compatibility despite lack of male/female roles associated with their mating types. By comparing full-length chromosome assemblies from five anther-smut fungi with or without recombination suppression in their mating-type chromosomes, we inferred the ancestral gene order and derived chromosomal arrangements in this group. This approach shed light on the chromosomal fusion underlying the linkage of mating-type loci in fungi and provided evidence for multiple clearly resolved evolutionary strata over a range of ages (0.9–2.1 million years) in mating-type chromosomes. Several evolutionary strata did not include genes involved in mating-type determination. The existence of strata devoid of mating-type genes, despite the lack of sexual antagonism, calls for a unified theory of sex-related chromosome evolution, incorporating, for example, the influence of partially linked deleterious mutations and the maintenance of neutral rearrangement polymorphism due to balancing selection on sexes and mating types. |
| doi_str_mv | 10.1073/pnas.1701658114 |
| format | Article |
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Rodríguez ; Gouzy, Jérôme ; Carpentier, Fantin ; Aguileta, Gabriela ; Siguenza, Sophie ; Brandenburg, Jean-Tristan ; Coelho, Marco A. ; Hood, Michael E. ; Giraud, Tatiana</creator><creatorcontrib>Branco, Sara ; Badouin, Hélène ; de la Vega, Ricardo C. Rodríguez ; Gouzy, Jérôme ; Carpentier, Fantin ; Aguileta, Gabriela ; Siguenza, Sophie ; Brandenburg, Jean-Tristan ; Coelho, Marco A. ; Hood, Michael E. ; Giraud, Tatiana</creatorcontrib><description>Sex chromosomes can display successive steps of recombination suppression known as “evolutionary strata,” which are thought to result from the successive linkage of sexually antagonistic genes to sex-determining genes. However, there is little evidence to support this explanation. Here we investigate whether evolutionary strata can evolve without sexual antagonism using fungi that display suppressed recombination extending beyond loci determining mating compatibility despite lack of male/female roles associated with their mating types. By comparing full-length chromosome assemblies from five anther-smut fungi with or without recombination suppression in their mating-type chromosomes, we inferred the ancestral gene order and derived chromosomal arrangements in this group. This approach shed light on the chromosomal fusion underlying the linkage of mating-type loci in fungi and provided evidence for multiple clearly resolved evolutionary strata over a range of ages (0.9–2.1 million years) in mating-type chromosomes. Several evolutionary strata did not include genes involved in mating-type determination. The existence of strata devoid of mating-type genes, despite the lack of sexual antagonism, calls for a unified theory of sex-related chromosome evolution, incorporating, for example, the influence of partially linked deleterious mutations and the maintenance of neutral rearrangement polymorphism due to balancing selection on sexes and mating types.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.1701658114</identifier><identifier>PMID: 28630332</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Age ; Biochemistry, Molecular Biology ; Biological Evolution ; Biological Sciences ; Chromosomes ; Chromosomes, Fungal ; Evolution ; Evolution, Molecular ; Evolutionary biology ; Fungi ; Fungi - genetics ; Gene order ; Gene Rearrangement ; Genes ; Genes, Mating Type, Fungal ; Genetic Linkage ; Genome, Fungal ; Genomics ; Haploidy ; Heterozygote ; Life Sciences ; Loci ; Mating types ; Microbiology and Parasitology ; Mutation ; Mycology ; Phylogeny ; Plant reproduction ; Polymorphism ; Recombination ; Recombination, Genetic ; Sex ; Sex chromosomes ; Smut ; Strata</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2017-07, Vol.114 (27), p.7067-7072</ispartof><rights>Volumes 1–89 and 106–114, copyright as a collective work only; author(s) retains copyright to individual articles</rights><rights>Copyright National Academy of Sciences Jul 3, 2017</rights><rights>Copyright</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c543t-5cdf2aa2c18eb77041810902324b63662510c428ccd39798969b39212ff51a963</citedby><cites>FETCH-LOGICAL-c543t-5cdf2aa2c18eb77041810902324b63662510c428ccd39798969b39212ff51a963</cites><orcidid>0000-0002-5716-0561 ; 0000-0002-2685-6478 ; 0000-0002-2456-5968 ; 0000-0001-5695-4557</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/26485348$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/26485348$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,723,776,780,799,881,27901,27902,53766,53768,57992,58225</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28630332$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-01547790$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Branco, Sara</creatorcontrib><creatorcontrib>Badouin, Hélène</creatorcontrib><creatorcontrib>de la Vega, Ricardo C. 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Here we investigate whether evolutionary strata can evolve without sexual antagonism using fungi that display suppressed recombination extending beyond loci determining mating compatibility despite lack of male/female roles associated with their mating types. By comparing full-length chromosome assemblies from five anther-smut fungi with or without recombination suppression in their mating-type chromosomes, we inferred the ancestral gene order and derived chromosomal arrangements in this group. This approach shed light on the chromosomal fusion underlying the linkage of mating-type loci in fungi and provided evidence for multiple clearly resolved evolutionary strata over a range of ages (0.9–2.1 million years) in mating-type chromosomes. Several evolutionary strata did not include genes involved in mating-type determination. The existence of strata devoid of mating-type genes, despite the lack of sexual antagonism, calls for a unified theory of sex-related chromosome evolution, incorporating, for example, the influence of partially linked deleterious mutations and the maintenance of neutral rearrangement polymorphism due to balancing selection on sexes and mating types.</description><subject>Age</subject><subject>Biochemistry, Molecular Biology</subject><subject>Biological Evolution</subject><subject>Biological Sciences</subject><subject>Chromosomes</subject><subject>Chromosomes, Fungal</subject><subject>Evolution</subject><subject>Evolution, Molecular</subject><subject>Evolutionary biology</subject><subject>Fungi</subject><subject>Fungi - genetics</subject><subject>Gene order</subject><subject>Gene Rearrangement</subject><subject>Genes</subject><subject>Genes, Mating Type, Fungal</subject><subject>Genetic Linkage</subject><subject>Genome, Fungal</subject><subject>Genomics</subject><subject>Haploidy</subject><subject>Heterozygote</subject><subject>Life Sciences</subject><subject>Loci</subject><subject>Mating types</subject><subject>Microbiology and Parasitology</subject><subject>Mutation</subject><subject>Mycology</subject><subject>Phylogeny</subject><subject>Plant reproduction</subject><subject>Polymorphism</subject><subject>Recombination</subject><subject>Recombination, Genetic</subject><subject>Sex</subject><subject>Sex chromosomes</subject><subject>Smut</subject><subject>Strata</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkc1vEzEQxS0EoqFw5gSyxAUO2874a-0LUlUVihSJC1y4WI7jTTbs2svaG5H_no1SWuhpJM9v3szzI-Q1wgVCzS-H6PIF1oBKakTxhCwQDFZKGHhKFgCsrrRg4oy8yHkHAEZqeE7OmFYcOGcL8uNmn7qptCm68UBzGV1xNEV6SFPc0N6VNm6qchgC9dsx9SmnPmS6DnloS6BlG2jn_E-aGprD78l11MXiNim2uX9JnjWuy-HVXT0n3z_dfLu-rZZfP3-5vlpWXgpeKunXDXOOedRhVdcgUM8egHEmVoorxSSCF0x7v-amNtoos-KGIWsaic4ofk4-nnSHadWHtQ9xdtHZYWz72ZNNrrX_d2K7tZu0t1ICUwizwIeTwPbR2O3V0h7fAKWoawN7nNn3d8vG9GsKudi-zT50nYshTdmiQVTG8Pp417tH6C5NY5y_YqaEEiiMYjN1eaL8mHIeQ3N_AYI9ZmyPGduHjOeJt__6vef_hjoDb07ALpc0PvSV0JILzf8AtJGr1A</recordid><startdate>20170703</startdate><enddate>20170703</enddate><creator>Branco, Sara</creator><creator>Badouin, Hélène</creator><creator>de la Vega, Ricardo C. 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Rodríguez</au><au>Gouzy, Jérôme</au><au>Carpentier, Fantin</au><au>Aguileta, Gabriela</au><au>Siguenza, Sophie</au><au>Brandenburg, Jean-Tristan</au><au>Coelho, Marco A.</au><au>Hood, Michael E.</au><au>Giraud, Tatiana</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Evolutionary strata on young mating-type chromosomes despite the lack of sexual antagonism</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>2017-07-03</date><risdate>2017</risdate><volume>114</volume><issue>27</issue><spage>7067</spage><epage>7072</epage><pages>7067-7072</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><abstract>Sex chromosomes can display successive steps of recombination suppression known as “evolutionary strata,” which are thought to result from the successive linkage of sexually antagonistic genes to sex-determining genes. However, there is little evidence to support this explanation. Here we investigate whether evolutionary strata can evolve without sexual antagonism using fungi that display suppressed recombination extending beyond loci determining mating compatibility despite lack of male/female roles associated with their mating types. By comparing full-length chromosome assemblies from five anther-smut fungi with or without recombination suppression in their mating-type chromosomes, we inferred the ancestral gene order and derived chromosomal arrangements in this group. This approach shed light on the chromosomal fusion underlying the linkage of mating-type loci in fungi and provided evidence for multiple clearly resolved evolutionary strata over a range of ages (0.9–2.1 million years) in mating-type chromosomes. Several evolutionary strata did not include genes involved in mating-type determination. 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| subjects | Age Biochemistry, Molecular Biology Biological Evolution Biological Sciences Chromosomes Chromosomes, Fungal Evolution Evolution, Molecular Evolutionary biology Fungi Fungi - genetics Gene order Gene Rearrangement Genes Genes, Mating Type, Fungal Genetic Linkage Genome, Fungal Genomics Haploidy Heterozygote Life Sciences Loci Mating types Microbiology and Parasitology Mutation Mycology Phylogeny Plant reproduction Polymorphism Recombination Recombination, Genetic Sex Sex chromosomes Smut Strata |
| title | Evolutionary strata on young mating-type chromosomes despite the lack of sexual antagonism |
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