Evolution of Yin and Yang isoforms of a chromatin remodeling subunit precedes the creation of two genes

Genes can encode multiple isoforms, broadening their functions and providing a molecular substrate to evolve phenotypic diversity. Evolution of isoform function is a potential route to adapt to new environments. Here we show that de novo, beneficial alleles in the nurf-1 gene became fixed in two lab...

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Detalhes bibliográficos
Autores: Xu, Wen, Long, Lijiang, Zhao, Yuehui, Stevens, Lewis, Felipe, Irene, Munoz, Javier, Ellis, Ronald E, McGrath, Patrick T
Formato: artículo
Fecha de publicación:2019
País:España
Recursos:Instituto de Salud Carlos III (ISCIII)
Repositorio:Repisalud
Idioma:inglés
OAI Identifier:oai:repisalud.isciii.es:20.500.12105/9335
Acesso em linha:http://hdl.handle.net/20.500.12105/9335
Access Level:acceso abierto
Palavra-chave:Animals
Caenorhabditis elegans
Caenorhabditis elegans Proteins
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spelling Evolution of Yin and Yang isoforms of a chromatin remodeling subunit precedes the creation of two genesXu, WenLong, LijiangZhao, YuehuiStevens, LewisFelipe, IreneMunoz, JavierEllis, Ronald EMcGrath, Patrick TAnimalsCaenorhabditis elegansCaenorhabditis elegans ProteinsGenes can encode multiple isoforms, broadening their functions and providing a molecular substrate to evolve phenotypic diversity. Evolution of isoform function is a potential route to adapt to new environments. Here we show that de novo, beneficial alleles in the nurf-1 gene became fixed in two laboratory lineages of C. elegans after isolation from the wild in 1951, before methods of cryopreservation were developed. nurf-1 encodes an ortholog of BPTF, a large (>300 kD) multidomain subunit of the NURF chromatin remodeling complex. Using CRISPR-Cas9 genome editing and transgenic rescue, we demonstrate that in C. elegans, nurf-1 has split into two, largely non-overlapping isoforms (NURF-1.D and NURF-1.B, which we call Yin and Yang, respectively) that share only two of 26 exons. Both isoforms are essential for normal gametogenesis but have opposite effects on male/female gamete differentiation. Reproduction in hermaphrodites, which involves production of both sperm and oocytes, requires a balance of these opposing Yin and Yang isoforms. Transgenic rescue and genetic position of the fixed mutations suggest that different isoforms are modified in each laboratory strain. In a related clade of Caenorhabditis nematodes, the shared exons have duplicated, resulting in the split of the Yin and Yang isoforms into separate genes, each containing approximately 200 amino acids of duplicated sequence that has undergone accelerated protein evolution following the duplication. Associated with this duplication event is the loss of two additional nurf-1 transcripts, including the long-form transcript and a newly identified, highly expressed transcript encoded by the duplicated exons. We propose these lost transcripts are non-functional side products necessary to transcribe the Yin and Yang transcripts in the same cells. Our work demonstrates how gene sharing, through the production of multiple isoforms, can precede the creation of new, independent genes.eLife Sciences PublicationsUnited States Department of Health and Human Services20202020-03-2520192019-09-0920192019-09-09journal articlehttp://purl.org/coar/resource_type/c_6501VoRhttp://purl.org/coar/version/c_970fb48d4fbd8a85info:eu-repo/semantics/articleapplication/pdfhttp://hdl.handle.net/20.500.12105/9335reponame:Repisaludinstname:Instituto de Salud Carlos III (ISCIII)Inglésengopen accesshttp://purl.org/coar/access_right/c_abf2Atribución-NoComercial-CompartirIgual 4.0 Internacionalhttp://creativecommons.org/licenses/by-nc-sa/4.0/info:eu-repo/semantics/openAccessoai:repisalud.isciii.es:20.500.12105/93352026-06-12T12:43:37Z
dc.title.none.fl_str_mv Evolution of Yin and Yang isoforms of a chromatin remodeling subunit precedes the creation of two genes
title Evolution of Yin and Yang isoforms of a chromatin remodeling subunit precedes the creation of two genes
spellingShingle Evolution of Yin and Yang isoforms of a chromatin remodeling subunit precedes the creation of two genes
Xu, Wen
Animals
Caenorhabditis elegans
Caenorhabditis elegans Proteins
title_short Evolution of Yin and Yang isoforms of a chromatin remodeling subunit precedes the creation of two genes
title_full Evolution of Yin and Yang isoforms of a chromatin remodeling subunit precedes the creation of two genes
title_fullStr Evolution of Yin and Yang isoforms of a chromatin remodeling subunit precedes the creation of two genes
title_full_unstemmed Evolution of Yin and Yang isoforms of a chromatin remodeling subunit precedes the creation of two genes
title_sort Evolution of Yin and Yang isoforms of a chromatin remodeling subunit precedes the creation of two genes
dc.creator.none.fl_str_mv Xu, Wen
Long, Lijiang
Zhao, Yuehui
Stevens, Lewis
Felipe, Irene
Munoz, Javier
Ellis, Ronald E
McGrath, Patrick T
author Xu, Wen
author_facet Xu, Wen
Long, Lijiang
Zhao, Yuehui
Stevens, Lewis
Felipe, Irene
Munoz, Javier
Ellis, Ronald E
McGrath, Patrick T
author_role author
author2 Long, Lijiang
Zhao, Yuehui
Stevens, Lewis
Felipe, Irene
Munoz, Javier
Ellis, Ronald E
McGrath, Patrick T
author2_role author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv United States Department of Health and Human Services
dc.subject.none.fl_str_mv Animals
Caenorhabditis elegans
Caenorhabditis elegans Proteins
topic Animals
Caenorhabditis elegans
Caenorhabditis elegans Proteins
description Genes can encode multiple isoforms, broadening their functions and providing a molecular substrate to evolve phenotypic diversity. Evolution of isoform function is a potential route to adapt to new environments. Here we show that de novo, beneficial alleles in the nurf-1 gene became fixed in two laboratory lineages of C. elegans after isolation from the wild in 1951, before methods of cryopreservation were developed. nurf-1 encodes an ortholog of BPTF, a large (>300 kD) multidomain subunit of the NURF chromatin remodeling complex. Using CRISPR-Cas9 genome editing and transgenic rescue, we demonstrate that in C. elegans, nurf-1 has split into two, largely non-overlapping isoforms (NURF-1.D and NURF-1.B, which we call Yin and Yang, respectively) that share only two of 26 exons. Both isoforms are essential for normal gametogenesis but have opposite effects on male/female gamete differentiation. Reproduction in hermaphrodites, which involves production of both sperm and oocytes, requires a balance of these opposing Yin and Yang isoforms. Transgenic rescue and genetic position of the fixed mutations suggest that different isoforms are modified in each laboratory strain. In a related clade of Caenorhabditis nematodes, the shared exons have duplicated, resulting in the split of the Yin and Yang isoforms into separate genes, each containing approximately 200 amino acids of duplicated sequence that has undergone accelerated protein evolution following the duplication. Associated with this duplication event is the loss of two additional nurf-1 transcripts, including the long-form transcript and a newly identified, highly expressed transcript encoded by the duplicated exons. We propose these lost transcripts are non-functional side products necessary to transcribe the Yin and Yang transcripts in the same cells. Our work demonstrates how gene sharing, through the production of multiple isoforms, can precede the creation of new, independent genes.
publishDate 2019
dc.date.none.fl_str_mv 2019
2019-09-09
2019
2019-09-09
2020
2020-03-25
dc.type.none.fl_str_mv journal article
http://purl.org/coar/resource_type/c_6501
VoR
http://purl.org/coar/version/c_970fb48d4fbd8a85
dc.type.openaire.fl_str_mv info:eu-repo/semantics/article
format article
dc.identifier.none.fl_str_mv http://hdl.handle.net/20.500.12105/9335
url http://hdl.handle.net/20.500.12105/9335
dc.language.none.fl_str_mv Inglés
eng
language_invalid_str_mv Inglés
language eng
dc.rights.none.fl_str_mv open access
http://purl.org/coar/access_right/c_abf2
Atribución-NoComercial-CompartirIgual 4.0 Internacional
http://creativecommons.org/licenses/by-nc-sa/4.0/
dc.rights.openaire.fl_str_mv info:eu-repo/semantics/openAccess
rights_invalid_str_mv open access
http://purl.org/coar/access_right/c_abf2
Atribución-NoComercial-CompartirIgual 4.0 Internacional
http://creativecommons.org/licenses/by-nc-sa/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv eLife Sciences Publications
publisher.none.fl_str_mv eLife Sciences Publications
dc.source.none.fl_str_mv reponame:Repisalud
instname:Instituto de Salud Carlos III (ISCIII)
instname_str Instituto de Salud Carlos III (ISCIII)
reponame_str Repisalud
collection Repisalud
repository.name.fl_str_mv
repository.mail.fl_str_mv
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score 15.811543

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