Yerba mate (Ilex paraguariensis) genome provides new insights into convergent evolution of caffeine biosynthesis

Autores
Vignale, Federico Agustín; García Hernández, Andrea Lorena; Modenutti, Carlos Pablo; Sosa, Ezequiel J.; Defelipe, Lucas Alfredo; Oliveira, Renato; Nunes, Gisele L; Acevedo, Raúl Maximiliano; Burguener, German F; Rossi, Sebastian M; Zapata, Pedro Dario; Marti, Dardo A; Sansberro, Pedro Alfonso; Oliveira, Guilherme; Catania, Emily M; Smith, Madeline N; Dubs, Nicole M; Nair, Satish; Barkman, Todd J.; Turjanski, Adrian
Año de publicación
2025
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Yerba mate (YM, Ilex paraguariensis) is an economically important crop marketed for the elaboration of mate, the third-most widely consumed caffeine-containing infusion worldwide. Here, we report the first genome assembly of this species, which has a total length of 1.06 Gb and contains 53,390 protein-coding genes. Comparative analyses revealed that the large YM genome size is partly due to a whole-genome duplication (Ip-α) during the early evolutionary history of Ilex, in addition to the hexaploidization event (γ) shared by core eudicots. Characterization of the genome allowed us to clone the genes encoding methyltransferase enzymes that catalyse multiple reactions required for caffeine production. To our surprise, this species has converged upon a different biochemical pathway compared to that of coffee and tea. In order to gain insight into the structural basis for the convergent enzyme activities, we obtained a crystal structure for the terminal enzyme in the pathway that forms caffeine. The structure reveals that convergent solutions have evolved for substrate positioning because different amino acid residues facilitate a different substrate orientation such that efficient methylation occurs in the independently evolved enzymes in YM and coffee. While our results show phylogenomic constraint limits the genes coopted for convergence of caffeine biosynthesis, the X-ray diffraction data suggest structural constraints are minimal for the convergent evolution of individual reactions.
Fil: Vignale, Federico Agustín. European Molecular Biology Laboratory; Alemania. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: García Hernández, Andrea Lorena. University of Illinois; Estados Unidos
Fil: Modenutti, Carlos Pablo. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Sosa, Ezequiel J.. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina
Fil: Defelipe, Lucas Alfredo. European Molecular Biology Laboratory; Alemania
Fil: Oliveira, Renato. Instituto Tecnológico Vale; Brasil
Fil: Nunes, Gisele L. Instituto Tecnológico Vale; Brasil
Fil: Acevedo, Raúl Maximiliano. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Nordeste. Instituto de Botánica del Nordeste. Universidad Nacional del Nordeste. Facultad de Ciencias Agrarias. Instituto de Botánica del Nordeste; Argentina
Fil: Burguener, German F. California State University; Estados Unidos
Fil: Rossi, Sebastian M. Universidad Nacional de Misiones. Facultad de Ciencias Exactas, Químicas y Naturales; Argentina
Fil: Zapata, Pedro Dario. Universidad Nacional de Misiones. Facultad de Ciencias Exactas, Químicas y Naturales; Argentina
Fil: Marti, Dardo A. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Nordeste. Instituto de Biología Subtropical. Universidad Nacional de Misiones. Instituto de Biología Subtropical; Argentina
Fil: Sansberro, Pedro Alfonso. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Nordeste. Instituto de Botánica del Nordeste. Universidad Nacional del Nordeste. Facultad de Ciencias Agrarias. Instituto de Botánica del Nordeste; Argentina
Fil: Oliveira, Guilherme. Instituto Tecnológico Vale.; Brasil
Fil: Catania, Emily M. University of Michigan; Estados Unidos
Fil: Smith, Madeline N. Michigan State University; Estados Unidos
Fil: Dubs, Nicole M. Michigan State University; Estados Unidos
Fil: Nair, Satish. University of Illinois. Urbana - Champaign; Estados Unidos
Fil: Barkman, Todd J.. Michigan State University; Estados Unidos
Fil: Turjanski, Adrian. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina
Materia
ILEX PARAGUARIENSIS
GENOME
CAFFEINE BIOSYNTHESIS
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:11336/284860
Acceder
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network_name_str CONICET Digital (CONICET)
spelling Yerba mate (Ilex paraguariensis) genome provides new insights into convergent evolution of caffeine biosynthesisVignale, Federico AgustínGarcía Hernández, Andrea LorenaModenutti, Carlos PabloSosa, Ezequiel J.Defelipe, Lucas AlfredoOliveira, RenatoNunes, Gisele LAcevedo, Raúl MaximilianoBurguener, German FRossi, Sebastian MZapata, Pedro DarioMarti, Dardo ASansberro, Pedro AlfonsoOliveira, GuilhermeCatania, Emily MSmith, Madeline NDubs, Nicole MNair, SatishBarkman, Todd J.Turjanski, AdrianILEX PARAGUARIENSISGENOMECAFFEINE BIOSYNTHESIShttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Yerba mate (YM, Ilex paraguariensis) is an economically important crop marketed for the elaboration of mate, the third-most widely consumed caffeine-containing infusion worldwide. Here, we report the first genome assembly of this species, which has a total length of 1.06 Gb and contains 53,390 protein-coding genes. Comparative analyses revealed that the large YM genome size is partly due to a whole-genome duplication (Ip-α) during the early evolutionary history of Ilex, in addition to the hexaploidization event (γ) shared by core eudicots. Characterization of the genome allowed us to clone the genes encoding methyltransferase enzymes that catalyse multiple reactions required for caffeine production. To our surprise, this species has converged upon a different biochemical pathway compared to that of coffee and tea. In order to gain insight into the structural basis for the convergent enzyme activities, we obtained a crystal structure for the terminal enzyme in the pathway that forms caffeine. The structure reveals that convergent solutions have evolved for substrate positioning because different amino acid residues facilitate a different substrate orientation such that efficient methylation occurs in the independently evolved enzymes in YM and coffee. While our results show phylogenomic constraint limits the genes coopted for convergence of caffeine biosynthesis, the X-ray diffraction data suggest structural constraints are minimal for the convergent evolution of individual reactions.Fil: Vignale, Federico Agustín. European Molecular Biology Laboratory; Alemania. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: García Hernández, Andrea Lorena. University of Illinois; Estados UnidosFil: Modenutti, Carlos Pablo. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Sosa, Ezequiel J.. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; ArgentinaFil: Defelipe, Lucas Alfredo. European Molecular Biology Laboratory; AlemaniaFil: Oliveira, Renato. Instituto Tecnológico Vale; BrasilFil: Nunes, Gisele L. Instituto Tecnológico Vale; BrasilFil: Acevedo, Raúl Maximiliano. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Nordeste. Instituto de Botánica del Nordeste. Universidad Nacional del Nordeste. Facultad de Ciencias Agrarias. Instituto de Botánica del Nordeste; ArgentinaFil: Burguener, German F. California State University; Estados UnidosFil: Rossi, Sebastian M. Universidad Nacional de Misiones. Facultad de Ciencias Exactas, Químicas y Naturales; ArgentinaFil: Zapata, Pedro Dario. Universidad Nacional de Misiones. Facultad de Ciencias Exactas, Químicas y Naturales; ArgentinaFil: Marti, Dardo A. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Nordeste. Instituto de Biología Subtropical. Universidad Nacional de Misiones. Instituto de Biología Subtropical; ArgentinaFil: Sansberro, Pedro Alfonso. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Nordeste. Instituto de Botánica del Nordeste. Universidad Nacional del Nordeste. Facultad de Ciencias Agrarias. Instituto de Botánica del Nordeste; ArgentinaFil: Oliveira, Guilherme. Instituto Tecnológico Vale.; BrasilFil: Catania, Emily M. University of Michigan; Estados UnidosFil: Smith, Madeline N. Michigan State University; Estados UnidosFil: Dubs, Nicole M. Michigan State University; Estados UnidosFil: Nair, Satish. University of Illinois. Urbana - Champaign; Estados UnidosFil: Barkman, Todd J.. Michigan State University; Estados UnidosFil: Turjanski, Adrian. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; ArgentinaeLife Sciences Publications Ltd.2025-01info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfapplication/pdfapplication/pdfapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/284860Vignale, Federico Agustín; García Hernández, Andrea Lorena; Modenutti, Carlos Pablo; Sosa, Ezequiel J.; Defelipe, Lucas Alfredo; et al.; Yerba mate (Ilex paraguariensis) genome provides new insights into convergent evolution of caffeine biosynthesis; eLife Sciences Publications Ltd.; eLife; 13; e104759; 1-2025; 1-412050-084XCONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://elifesciences.org/articles/104759info:eu-repo/semantics/altIdentifier/doi/10.7554/eLife.104759info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2026-08-25T14:33:54Zoai:ri.conicet.gov.ar:11336/284860instacron: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:34982026-08-25 14:33:55.193CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Yerba mate (Ilex paraguariensis) genome provides new insights into convergent evolution of caffeine biosynthesis
title Yerba mate (Ilex paraguariensis) genome provides new insights into convergent evolution of caffeine biosynthesis
spellingShingle Yerba mate (Ilex paraguariensis) genome provides new insights into convergent evolution of caffeine biosynthesis
Vignale, Federico Agustín
ILEX PARAGUARIENSIS
GENOME
CAFFEINE BIOSYNTHESIS
title_short Yerba mate (Ilex paraguariensis) genome provides new insights into convergent evolution of caffeine biosynthesis
title_full Yerba mate (Ilex paraguariensis) genome provides new insights into convergent evolution of caffeine biosynthesis
title_fullStr Yerba mate (Ilex paraguariensis) genome provides new insights into convergent evolution of caffeine biosynthesis
title_full_unstemmed Yerba mate (Ilex paraguariensis) genome provides new insights into convergent evolution of caffeine biosynthesis
title_sort Yerba mate (Ilex paraguariensis) genome provides new insights into convergent evolution of caffeine biosynthesis
dc.creator.none.fl_str_mv Vignale, Federico Agustín
García Hernández, Andrea Lorena
Modenutti, Carlos Pablo
Sosa, Ezequiel J.
Defelipe, Lucas Alfredo
Oliveira, Renato
Nunes, Gisele L
Acevedo, Raúl Maximiliano
Burguener, German F
Rossi, Sebastian M
Zapata, Pedro Dario
Marti, Dardo A
Sansberro, Pedro Alfonso
Oliveira, Guilherme
Catania, Emily M
Smith, Madeline N
Dubs, Nicole M
Nair, Satish
Barkman, Todd J.
Turjanski, Adrian
author Vignale, Federico Agustín
author_facet Vignale, Federico Agustín
García Hernández, Andrea Lorena
Modenutti, Carlos Pablo
Sosa, Ezequiel J.
Defelipe, Lucas Alfredo
Oliveira, Renato
Nunes, Gisele L
Acevedo, Raúl Maximiliano
Burguener, German F
Rossi, Sebastian M
Zapata, Pedro Dario
Marti, Dardo A
Sansberro, Pedro Alfonso
Oliveira, Guilherme
Catania, Emily M
Smith, Madeline N
Dubs, Nicole M
Nair, Satish
Barkman, Todd J.
Turjanski, Adrian
author_role author
author2 García Hernández, Andrea Lorena
Modenutti, Carlos Pablo
Sosa, Ezequiel J.
Defelipe, Lucas Alfredo
Oliveira, Renato
Nunes, Gisele L
Acevedo, Raúl Maximiliano
Burguener, German F
Rossi, Sebastian M
Zapata, Pedro Dario
Marti, Dardo A
Sansberro, Pedro Alfonso
Oliveira, Guilherme
Catania, Emily M
Smith, Madeline N
Dubs, Nicole M
Nair, Satish
Barkman, Todd J.
Turjanski, Adrian
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv ILEX PARAGUARIENSIS
GENOME
CAFFEINE BIOSYNTHESIS
topic ILEX PARAGUARIENSIS
GENOME
CAFFEINE BIOSYNTHESIS
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Yerba mate (YM, Ilex paraguariensis) is an economically important crop marketed for the elaboration of mate, the third-most widely consumed caffeine-containing infusion worldwide. Here, we report the first genome assembly of this species, which has a total length of 1.06 Gb and contains 53,390 protein-coding genes. Comparative analyses revealed that the large YM genome size is partly due to a whole-genome duplication (Ip-α) during the early evolutionary history of Ilex, in addition to the hexaploidization event (γ) shared by core eudicots. Characterization of the genome allowed us to clone the genes encoding methyltransferase enzymes that catalyse multiple reactions required for caffeine production. To our surprise, this species has converged upon a different biochemical pathway compared to that of coffee and tea. In order to gain insight into the structural basis for the convergent enzyme activities, we obtained a crystal structure for the terminal enzyme in the pathway that forms caffeine. The structure reveals that convergent solutions have evolved for substrate positioning because different amino acid residues facilitate a different substrate orientation such that efficient methylation occurs in the independently evolved enzymes in YM and coffee. While our results show phylogenomic constraint limits the genes coopted for convergence of caffeine biosynthesis, the X-ray diffraction data suggest structural constraints are minimal for the convergent evolution of individual reactions.
Fil: Vignale, Federico Agustín. European Molecular Biology Laboratory; Alemania. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: García Hernández, Andrea Lorena. University of Illinois; Estados Unidos
Fil: Modenutti, Carlos Pablo. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Sosa, Ezequiel J.. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina
Fil: Defelipe, Lucas Alfredo. European Molecular Biology Laboratory; Alemania
Fil: Oliveira, Renato. Instituto Tecnológico Vale; Brasil
Fil: Nunes, Gisele L. Instituto Tecnológico Vale; Brasil
Fil: Acevedo, Raúl Maximiliano. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Nordeste. Instituto de Botánica del Nordeste. Universidad Nacional del Nordeste. Facultad de Ciencias Agrarias. Instituto de Botánica del Nordeste; Argentina
Fil: Burguener, German F. California State University; Estados Unidos
Fil: Rossi, Sebastian M. Universidad Nacional de Misiones. Facultad de Ciencias Exactas, Químicas y Naturales; Argentina
Fil: Zapata, Pedro Dario. Universidad Nacional de Misiones. Facultad de Ciencias Exactas, Químicas y Naturales; Argentina
Fil: Marti, Dardo A. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Nordeste. Instituto de Biología Subtropical. Universidad Nacional de Misiones. Instituto de Biología Subtropical; Argentina
Fil: Sansberro, Pedro Alfonso. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Nordeste. Instituto de Botánica del Nordeste. Universidad Nacional del Nordeste. Facultad de Ciencias Agrarias. Instituto de Botánica del Nordeste; Argentina
Fil: Oliveira, Guilherme. Instituto Tecnológico Vale.; Brasil
Fil: Catania, Emily M. University of Michigan; Estados Unidos
Fil: Smith, Madeline N. Michigan State University; Estados Unidos
Fil: Dubs, Nicole M. Michigan State University; Estados Unidos
Fil: Nair, Satish. University of Illinois. Urbana - Champaign; Estados Unidos
Fil: Barkman, Todd J.. Michigan State University; Estados Unidos
Fil: Turjanski, Adrian. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina
description Yerba mate (YM, Ilex paraguariensis) is an economically important crop marketed for the elaboration of mate, the third-most widely consumed caffeine-containing infusion worldwide. Here, we report the first genome assembly of this species, which has a total length of 1.06 Gb and contains 53,390 protein-coding genes. Comparative analyses revealed that the large YM genome size is partly due to a whole-genome duplication (Ip-α) during the early evolutionary history of Ilex, in addition to the hexaploidization event (γ) shared by core eudicots. Characterization of the genome allowed us to clone the genes encoding methyltransferase enzymes that catalyse multiple reactions required for caffeine production. To our surprise, this species has converged upon a different biochemical pathway compared to that of coffee and tea. In order to gain insight into the structural basis for the convergent enzyme activities, we obtained a crystal structure for the terminal enzyme in the pathway that forms caffeine. The structure reveals that convergent solutions have evolved for substrate positioning because different amino acid residues facilitate a different substrate orientation such that efficient methylation occurs in the independently evolved enzymes in YM and coffee. While our results show phylogenomic constraint limits the genes coopted for convergence of caffeine biosynthesis, the X-ray diffraction data suggest structural constraints are minimal for the convergent evolution of individual reactions.
publishDate 2025
dc.date.none.fl_str_mv 2025-01
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/11336/284860
Vignale, Federico Agustín; García Hernández, Andrea Lorena; Modenutti, Carlos Pablo; Sosa, Ezequiel J.; Defelipe, Lucas Alfredo; et al.; Yerba mate (Ilex paraguariensis) genome provides new insights into convergent evolution of caffeine biosynthesis; eLife Sciences Publications Ltd.; eLife; 13; e104759; 1-2025; 1-41
2050-084X
CONICET Digital
CONICET
url http://hdl.handle.net/11336/284860
identifier_str_mv Vignale, Federico Agustín; García Hernández, Andrea Lorena; Modenutti, Carlos Pablo; Sosa, Ezequiel J.; Defelipe, Lucas Alfredo; et al.; Yerba mate (Ilex paraguariensis) genome provides new insights into convergent evolution of caffeine biosynthesis; eLife Sciences Publications Ltd.; eLife; 13; e104759; 1-2025; 1-41
2050-084X
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
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info:eu-repo/semantics/altIdentifier/doi/10.7554/eLife.104759
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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
application/pdf
application/pdf
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dc.publisher.none.fl_str_mv eLife Sciences Publications Ltd.
publisher.none.fl_str_mv eLife Sciences Publications Ltd.
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repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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