Transcription factors evolve faster than their structural gene targets in theflavonoid pigment pathway

Autores
Wheeler, Lucas C.; Walker, Joseph F.; Ng, Julienne; Deanna, Rocío; Dunbar Wallis, Amy; Backes, Alice; Pezzi, Pedro H.; Palchetti, Maria Virginia; Robertson, Holly M.; Monaghan, Andrew; de Freitas, Loreta Brandão; Barboza, Gloria E.; Moyroud, Edwige; Smith, Stacey Dewitt
Año de publicación
2022
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Dissecting the relationship between gene function and substitution rates is key to understanding genome-wide patterns of molecular evolution. Biochemical pathways provide powerful systems for investigating this relationship because the functional role of each gene is often well characterized. Here, we investigate the evolution of the flavonoid pigment pathway in the colorful Petunieae clade of the tomato family (Solanaceae). This pathway is broadly conserved in plants, both in terms of its structural elements and its MYB, basic helix-loop-helix, and WD40 transcriptional regulators, and its function has been extensively studied, particularly in model species of petunia. We built a phylotranscriptomic data set for 69 species of Petunieae to infer patterns of molecular evolution across pathway genes and across lineages. We found that transcription factors exhibit faster rates of molecular evolution (dN/dS) than their targets, with the highly specialized MYB genes evolving fastest. Using the largest comparative data set to date, we recovered little support for the hypothesis that upstream enzymes evolve slower than those occupying more downstream positions, although expression levels do predict molecular evolutionary rates. Although shifts in floral pigmentation were only weakly related to changes affecting coding regions, we found a strong relationship with the presence/absence patterns of MYB transcripts. Intensely pigmented species express all three main MYB anthocyanin activators in petals, whereas pale or white species express few or none. Our findings reinforce the notion that pathway regulators have a dynamic history, involving higher rates of molecular evolution than structural components, along with frequent changes in expression during color transitions.
Fil: Wheeler, Lucas C.. State University of Colorado at Boulder; Estados Unidos
Fil: Walker, Joseph F.. University of Cambridge; Reino Unido. University of Illinois; Estados Unidos
Fil: Ng, Julienne. State University of Colorado at Boulder; Estados Unidos
Fil: Deanna, Rocío. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto Multidisciplinario de Biología Vegetal. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas Físicas y Naturales. Instituto Multidisciplinario de Biología Vegetal; Argentina. University of Colorado; Estados Unidos
Fil: Dunbar Wallis, Amy. State University of Colorado at Boulder; Estados Unidos
Fil: Backes, Alice. Universidade Federal do Rio Grande do Sul; Brasil
Fil: Pezzi, Pedro H.. Universidade Federal do Rio Grande do Sul; Brasil
Fil: Palchetti, Maria Virginia. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto Multidisciplinario de Biología Vegetal. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas Físicas y Naturales. Instituto Multidisciplinario de Biología Vegetal; Argentina
Fil: Robertson, Holly M.. University of Cambridge; Reino Unido
Fil: Monaghan, Andrew. State University of Colorado at Boulder; Estados Unidos
Fil: de Freitas, Loreta Brandão. Universidade Federal do Rio Grande do Sul; Brasil
Fil: Barboza, Gloria E.. Universidad Nacional de Córdoba; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto Multidisciplinario de Biología Vegetal. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas Físicas y Naturales. Instituto Multidisciplinario de Biología Vegetal; Argentina
Fil: Moyroud, Edwige. University of Cambridge; Reino Unido
Fil: Smith, Stacey Dewitt. State University of Colorado at Boulder; Estados Unidos
Materia
ANTHOCYANINS
FLOWER COLOR
MOLECULAR EVOLUTION
MYB
PETUNIEAE
PHYLOGENOMICS
SOLANACEAE
TRANSCRIPTION FACTORS
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/160655
Acceder
id CONICETDig_557398331bb9a3e0764207613e6c3cdf
oai_identifier_str oai:ri.conicet.gov.ar:11336/160655
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Transcription factors evolve faster than their structural gene targets in theflavonoid pigment pathwayWheeler, Lucas C.Walker, Joseph F.Ng, JulienneDeanna, RocíoDunbar Wallis, AmyBackes, AlicePezzi, Pedro H.Palchetti, Maria VirginiaRobertson, Holly M.Monaghan, Andrewde Freitas, Loreta BrandãoBarboza, Gloria E.Moyroud, EdwigeSmith, Stacey DewittANTHOCYANINSFLOWER COLORMOLECULAR EVOLUTIONMYBPETUNIEAEPHYLOGENOMICSSOLANACEAETRANSCRIPTION FACTORShttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Dissecting the relationship between gene function and substitution rates is key to understanding genome-wide patterns of molecular evolution. Biochemical pathways provide powerful systems for investigating this relationship because the functional role of each gene is often well characterized. Here, we investigate the evolution of the flavonoid pigment pathway in the colorful Petunieae clade of the tomato family (Solanaceae). This pathway is broadly conserved in plants, both in terms of its structural elements and its MYB, basic helix-loop-helix, and WD40 transcriptional regulators, and its function has been extensively studied, particularly in model species of petunia. We built a phylotranscriptomic data set for 69 species of Petunieae to infer patterns of molecular evolution across pathway genes and across lineages. We found that transcription factors exhibit faster rates of molecular evolution (dN/dS) than their targets, with the highly specialized MYB genes evolving fastest. Using the largest comparative data set to date, we recovered little support for the hypothesis that upstream enzymes evolve slower than those occupying more downstream positions, although expression levels do predict molecular evolutionary rates. Although shifts in floral pigmentation were only weakly related to changes affecting coding regions, we found a strong relationship with the presence/absence patterns of MYB transcripts. Intensely pigmented species express all three main MYB anthocyanin activators in petals, whereas pale or white species express few or none. Our findings reinforce the notion that pathway regulators have a dynamic history, involving higher rates of molecular evolution than structural components, along with frequent changes in expression during color transitions.Fil: Wheeler, Lucas C.. State University of Colorado at Boulder; Estados UnidosFil: Walker, Joseph F.. University of Cambridge; Reino Unido. University of Illinois; Estados UnidosFil: Ng, Julienne. State University of Colorado at Boulder; Estados UnidosFil: Deanna, Rocío. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto Multidisciplinario de Biología Vegetal. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas Físicas y Naturales. Instituto Multidisciplinario de Biología Vegetal; Argentina. University of Colorado; Estados UnidosFil: Dunbar Wallis, Amy. State University of Colorado at Boulder; Estados UnidosFil: Backes, Alice. Universidade Federal do Rio Grande do Sul; BrasilFil: Pezzi, Pedro H.. Universidade Federal do Rio Grande do Sul; BrasilFil: Palchetti, Maria Virginia. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto Multidisciplinario de Biología Vegetal. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas Físicas y Naturales. Instituto Multidisciplinario de Biología Vegetal; ArgentinaFil: Robertson, Holly M.. University of Cambridge; Reino UnidoFil: Monaghan, Andrew. State University of Colorado at Boulder; Estados UnidosFil: de Freitas, Loreta Brandão. Universidade Federal do Rio Grande do Sul; BrasilFil: Barboza, Gloria E.. Universidad Nacional de Córdoba; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto Multidisciplinario de Biología Vegetal. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas Físicas y Naturales. Instituto Multidisciplinario de Biología Vegetal; ArgentinaFil: Moyroud, Edwige. University of Cambridge; Reino UnidoFil: Smith, Stacey Dewitt. State University of Colorado at Boulder; Estados UnidosOxford University Press2022-03info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/160655Wheeler, Lucas C.; Walker, Joseph F.; Ng, Julienne; Deanna, Rocío; Dunbar Wallis, Amy; et al.; Transcription factors evolve faster than their structural gene targets in theflavonoid pigment pathway; Oxford University Press; Molecular Biology and Evolution; 39; 3; 3-2022; 1-150737-40381537-1719CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.1093/molbev/msac044info:eu-repo/semantics/altIdentifier/url/https://academic.oup.com/mbe/article/39/3/msac044/6536971info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T09:42:42Zoai:ri.conicet.gov.ar:11336/160655instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-29 09:42:43.154CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Transcription factors evolve faster than their structural gene targets in theflavonoid pigment pathway
title Transcription factors evolve faster than their structural gene targets in theflavonoid pigment pathway
spellingShingle Transcription factors evolve faster than their structural gene targets in theflavonoid pigment pathway
Wheeler, Lucas C.
ANTHOCYANINS
FLOWER COLOR
MOLECULAR EVOLUTION
MYB
PETUNIEAE
PHYLOGENOMICS
SOLANACEAE
TRANSCRIPTION FACTORS
title_short Transcription factors evolve faster than their structural gene targets in theflavonoid pigment pathway
title_full Transcription factors evolve faster than their structural gene targets in theflavonoid pigment pathway
title_fullStr Transcription factors evolve faster than their structural gene targets in theflavonoid pigment pathway
title_full_unstemmed Transcription factors evolve faster than their structural gene targets in theflavonoid pigment pathway
title_sort Transcription factors evolve faster than their structural gene targets in theflavonoid pigment pathway
dc.creator.none.fl_str_mv Wheeler, Lucas C.
Walker, Joseph F.
Ng, Julienne
Deanna, Rocío
Dunbar Wallis, Amy
Backes, Alice
Pezzi, Pedro H.
Palchetti, Maria Virginia
Robertson, Holly M.
Monaghan, Andrew
de Freitas, Loreta Brandão
Barboza, Gloria E.
Moyroud, Edwige
Smith, Stacey Dewitt
author Wheeler, Lucas C.
author_facet Wheeler, Lucas C.
Walker, Joseph F.
Ng, Julienne
Deanna, Rocío
Dunbar Wallis, Amy
Backes, Alice
Pezzi, Pedro H.
Palchetti, Maria Virginia
Robertson, Holly M.
Monaghan, Andrew
de Freitas, Loreta Brandão
Barboza, Gloria E.
Moyroud, Edwige
Smith, Stacey Dewitt
author_role author
author2 Walker, Joseph F.
Ng, Julienne
Deanna, Rocío
Dunbar Wallis, Amy
Backes, Alice
Pezzi, Pedro H.
Palchetti, Maria Virginia
Robertson, Holly M.
Monaghan, Andrew
de Freitas, Loreta Brandão
Barboza, Gloria E.
Moyroud, Edwige
Smith, Stacey Dewitt
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv ANTHOCYANINS
FLOWER COLOR
MOLECULAR EVOLUTION
MYB
PETUNIEAE
PHYLOGENOMICS
SOLANACEAE
TRANSCRIPTION FACTORS
topic ANTHOCYANINS
FLOWER COLOR
MOLECULAR EVOLUTION
MYB
PETUNIEAE
PHYLOGENOMICS
SOLANACEAE
TRANSCRIPTION FACTORS
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Dissecting the relationship between gene function and substitution rates is key to understanding genome-wide patterns of molecular evolution. Biochemical pathways provide powerful systems for investigating this relationship because the functional role of each gene is often well characterized. Here, we investigate the evolution of the flavonoid pigment pathway in the colorful Petunieae clade of the tomato family (Solanaceae). This pathway is broadly conserved in plants, both in terms of its structural elements and its MYB, basic helix-loop-helix, and WD40 transcriptional regulators, and its function has been extensively studied, particularly in model species of petunia. We built a phylotranscriptomic data set for 69 species of Petunieae to infer patterns of molecular evolution across pathway genes and across lineages. We found that transcription factors exhibit faster rates of molecular evolution (dN/dS) than their targets, with the highly specialized MYB genes evolving fastest. Using the largest comparative data set to date, we recovered little support for the hypothesis that upstream enzymes evolve slower than those occupying more downstream positions, although expression levels do predict molecular evolutionary rates. Although shifts in floral pigmentation were only weakly related to changes affecting coding regions, we found a strong relationship with the presence/absence patterns of MYB transcripts. Intensely pigmented species express all three main MYB anthocyanin activators in petals, whereas pale or white species express few or none. Our findings reinforce the notion that pathway regulators have a dynamic history, involving higher rates of molecular evolution than structural components, along with frequent changes in expression during color transitions.
Fil: Wheeler, Lucas C.. State University of Colorado at Boulder; Estados Unidos
Fil: Walker, Joseph F.. University of Cambridge; Reino Unido. University of Illinois; Estados Unidos
Fil: Ng, Julienne. State University of Colorado at Boulder; Estados Unidos
Fil: Deanna, Rocío. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto Multidisciplinario de Biología Vegetal. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas Físicas y Naturales. Instituto Multidisciplinario de Biología Vegetal; Argentina. University of Colorado; Estados Unidos
Fil: Dunbar Wallis, Amy. State University of Colorado at Boulder; Estados Unidos
Fil: Backes, Alice. Universidade Federal do Rio Grande do Sul; Brasil
Fil: Pezzi, Pedro H.. Universidade Federal do Rio Grande do Sul; Brasil
Fil: Palchetti, Maria Virginia. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto Multidisciplinario de Biología Vegetal. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas Físicas y Naturales. Instituto Multidisciplinario de Biología Vegetal; Argentina
Fil: Robertson, Holly M.. University of Cambridge; Reino Unido
Fil: Monaghan, Andrew. State University of Colorado at Boulder; Estados Unidos
Fil: de Freitas, Loreta Brandão. Universidade Federal do Rio Grande do Sul; Brasil
Fil: Barboza, Gloria E.. Universidad Nacional de Córdoba; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto Multidisciplinario de Biología Vegetal. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas Físicas y Naturales. Instituto Multidisciplinario de Biología Vegetal; Argentina
Fil: Moyroud, Edwige. University of Cambridge; Reino Unido
Fil: Smith, Stacey Dewitt. State University of Colorado at Boulder; Estados Unidos
description Dissecting the relationship between gene function and substitution rates is key to understanding genome-wide patterns of molecular evolution. Biochemical pathways provide powerful systems for investigating this relationship because the functional role of each gene is often well characterized. Here, we investigate the evolution of the flavonoid pigment pathway in the colorful Petunieae clade of the tomato family (Solanaceae). This pathway is broadly conserved in plants, both in terms of its structural elements and its MYB, basic helix-loop-helix, and WD40 transcriptional regulators, and its function has been extensively studied, particularly in model species of petunia. We built a phylotranscriptomic data set for 69 species of Petunieae to infer patterns of molecular evolution across pathway genes and across lineages. We found that transcription factors exhibit faster rates of molecular evolution (dN/dS) than their targets, with the highly specialized MYB genes evolving fastest. Using the largest comparative data set to date, we recovered little support for the hypothesis that upstream enzymes evolve slower than those occupying more downstream positions, although expression levels do predict molecular evolutionary rates. Although shifts in floral pigmentation were only weakly related to changes affecting coding regions, we found a strong relationship with the presence/absence patterns of MYB transcripts. Intensely pigmented species express all three main MYB anthocyanin activators in petals, whereas pale or white species express few or none. Our findings reinforce the notion that pathway regulators have a dynamic history, involving higher rates of molecular evolution than structural components, along with frequent changes in expression during color transitions.
publishDate 2022
dc.date.none.fl_str_mv 2022-03
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/160655
Wheeler, Lucas C.; Walker, Joseph F.; Ng, Julienne; Deanna, Rocío; Dunbar Wallis, Amy; et al.; Transcription factors evolve faster than their structural gene targets in theflavonoid pigment pathway; Oxford University Press; Molecular Biology and Evolution; 39; 3; 3-2022; 1-15
0737-4038
1537-1719
CONICET Digital
CONICET
url http://hdl.handle.net/11336/160655
identifier_str_mv Wheeler, Lucas C.; Walker, Joseph F.; Ng, Julienne; Deanna, Rocío; Dunbar Wallis, Amy; et al.; Transcription factors evolve faster than their structural gene targets in theflavonoid pigment pathway; Oxford University Press; Molecular Biology and Evolution; 39; 3; 3-2022; 1-15
0737-4038
1537-1719
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/doi/10.1093/molbev/msac044
info:eu-repo/semantics/altIdentifier/url/https://academic.oup.com/mbe/article/39/3/msac044/6536971
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Oxford University Press
publisher.none.fl_str_mv Oxford University Press
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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score 13.070432

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