The trichome pattern diversity of Cardamine shares genetic mechanisms with Arabidopsis but differs in environmental drivers

Natural variation in trichome pattern (amount and distribution) is prominent among populations of many angiosperms. However, the degree of parallelism in the genetic mechanisms underlying this diversity and its environmental drivers in different species remain unclear. To address these questions, we...

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Autores: Fuster-Pons, Alberto, Murillo-Sánchez, Alba, Méndez-Vigo, Belén, Marcer, Arnald, Pieper, Bjorn, Torres-Pérez, Rafael, Oliveros, Juan Carlos, Tsiantis, Miltos, Picó, F. Xavier, Alonso-Blanco, Carlos
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2024
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/375929
Acceso en línea:http://hdl.handle.net/10261/375929
https://api.elsevier.com/content/abstract/scopus_id/85210986813
Access Level:acceso abierto
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spelling The trichome pattern diversity of Cardamine shares genetic mechanisms with Arabidopsis but differs in environmental driversFuster-Pons, AlbertoMurillo-Sánchez, AlbaMéndez-Vigo, BelénMarcer, ArnaldPieper, BjornTorres-Pérez, RafaelOliveros, Juan CarlosTsiantis, MiltosPicó, F. XavierAlonso-Blanco, CarlosNatural variation in trichome pattern (amount and distribution) is prominent among populations of many angiosperms. However, the degree of parallelism in the genetic mechanisms underlying this diversity and its environmental drivers in different species remain unclear. To address these questions, we analyzed the genomic and environmental bases of leaf trichome pattern diversity in Cardamine hirsuta, a relative of Arabidopsis (Arabidopsis thaliana). We characterized 123 wild accessions for their genomic diversity, leaf trichome patterns at different temperatures, and environmental adjustments. Nucleotide diversities and biogeographical distribution models identified two major genetic lineages with distinct demographic and adaptive histories. Additionally, C. hirsuta showed substantial variation in trichome pattern and plasticity to temperature. Trichome amount in C. hirsuta correlated positively with spring precipitation but negatively with temperature, which is opposite to climatic patterns in A. thaliana. Contrastingly, genetic analysis of C. hirsuta glabrous accessions indicated that, like for A. thaliana, glabrousness is caused by null mutations in ChGLABRA1 (ChGL1). Phenotypic genome-wide association studies (GWAS) further identified a ChGL1 haplogroup associated with low trichome density and ChGL1 expression. Therefore, a ChGL1 series of null and partial loss-of-function alleles accounts for the parallel evolution of leaf trichome pattern in C. hirsuta and A. thaliana. Finally, GWAS also detected other candidate genes (e.g. ChETC3, ChCLE17) that might affect trichome pattern. Accordingly, the evolution of this trait in C. hirsuta and A. thaliana shows partially conserved genetic mechanisms but is likely involved in adaptation to different environments.A.F.-P. and A.M.-S. were recipients of PhD fellowships BES-2017-080063 and PRE2020-094891, respectively, from the Ministerio de Ciencia e Innovación (MCIN) of Spain. This work has been funded by grant PID2022-136893NB-I00 from the MCIN/AEI/10.13039/501100011033 and FEDER (EU) to C.A.-B., the Max Planck Society (core grant to M.T.), and the Deutsche Forschungsgemeinschaft (DFG) (CRC TRR 341 Plant Ecological Genetics project A3 to M.T.).Peer reviewedUniversity of OxfordMinisterio de Ciencia e Innovación (España)Max Planck SocietyFuster-Pons, Alberto [0000-0002-9248-4377]Murillo-Sánchez, Alba [0000-0001-6441-5297]Méndez-Vigo, Belén [0000-0002-9850-536X]Torres-Pérez, Rafael [0000-0002-3696-4720]Oliveros, Juan Carlos [0000-0002-4520-0853]Picó, F Xavier [0000-0003-2849-4922]Alonso-Blanco, Carlos [0000-0002-4738-5556]Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202520252024info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/375929https://api.elsevier.com/content/abstract/scopus_id/85210986813reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/BES-2017-080063info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/PID2022-136893NB-I00Plant physiologyapplication/pdfhttps://doi.org/10.1093/plphys/kiae213Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3759292026-05-22T06:33:51Z
dc.title.none.fl_str_mv The trichome pattern diversity of Cardamine shares genetic mechanisms with Arabidopsis but differs in environmental drivers
title The trichome pattern diversity of Cardamine shares genetic mechanisms with Arabidopsis but differs in environmental drivers
spellingShingle The trichome pattern diversity of Cardamine shares genetic mechanisms with Arabidopsis but differs in environmental drivers
Fuster-Pons, Alberto
title_short The trichome pattern diversity of Cardamine shares genetic mechanisms with Arabidopsis but differs in environmental drivers
title_full The trichome pattern diversity of Cardamine shares genetic mechanisms with Arabidopsis but differs in environmental drivers
title_fullStr The trichome pattern diversity of Cardamine shares genetic mechanisms with Arabidopsis but differs in environmental drivers
title_full_unstemmed The trichome pattern diversity of Cardamine shares genetic mechanisms with Arabidopsis but differs in environmental drivers
title_sort The trichome pattern diversity of Cardamine shares genetic mechanisms with Arabidopsis but differs in environmental drivers
dc.creator.none.fl_str_mv Fuster-Pons, Alberto
Murillo-Sánchez, Alba
Méndez-Vigo, Belén
Marcer, Arnald
Pieper, Bjorn
Torres-Pérez, Rafael
Oliveros, Juan Carlos
Tsiantis, Miltos
Picó, F. Xavier
Alonso-Blanco, Carlos
author Fuster-Pons, Alberto
author_facet Fuster-Pons, Alberto
Murillo-Sánchez, Alba
Méndez-Vigo, Belén
Marcer, Arnald
Pieper, Bjorn
Torres-Pérez, Rafael
Oliveros, Juan Carlos
Tsiantis, Miltos
Picó, F. Xavier
Alonso-Blanco, Carlos
author_role author
author2 Murillo-Sánchez, Alba
Méndez-Vigo, Belén
Marcer, Arnald
Pieper, Bjorn
Torres-Pérez, Rafael
Oliveros, Juan Carlos
Tsiantis, Miltos
Picó, F. Xavier
Alonso-Blanco, Carlos
author2_role author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Ministerio de Ciencia e Innovación (España)
Max Planck Society
Fuster-Pons, Alberto [0000-0002-9248-4377]
Murillo-Sánchez, Alba [0000-0001-6441-5297]
Méndez-Vigo, Belén [0000-0002-9850-536X]
Torres-Pérez, Rafael [0000-0002-3696-4720]
Oliveros, Juan Carlos [0000-0002-4520-0853]
Picó, F Xavier [0000-0003-2849-4922]
Alonso-Blanco, Carlos [0000-0002-4738-5556]
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
description Natural variation in trichome pattern (amount and distribution) is prominent among populations of many angiosperms. However, the degree of parallelism in the genetic mechanisms underlying this diversity and its environmental drivers in different species remain unclear. To address these questions, we analyzed the genomic and environmental bases of leaf trichome pattern diversity in Cardamine hirsuta, a relative of Arabidopsis (Arabidopsis thaliana). We characterized 123 wild accessions for their genomic diversity, leaf trichome patterns at different temperatures, and environmental adjustments. Nucleotide diversities and biogeographical distribution models identified two major genetic lineages with distinct demographic and adaptive histories. Additionally, C. hirsuta showed substantial variation in trichome pattern and plasticity to temperature. Trichome amount in C. hirsuta correlated positively with spring precipitation but negatively with temperature, which is opposite to climatic patterns in A. thaliana. Contrastingly, genetic analysis of C. hirsuta glabrous accessions indicated that, like for A. thaliana, glabrousness is caused by null mutations in ChGLABRA1 (ChGL1). Phenotypic genome-wide association studies (GWAS) further identified a ChGL1 haplogroup associated with low trichome density and ChGL1 expression. Therefore, a ChGL1 series of null and partial loss-of-function alleles accounts for the parallel evolution of leaf trichome pattern in C. hirsuta and A. thaliana. Finally, GWAS also detected other candidate genes (e.g. ChETC3, ChCLE17) that might affect trichome pattern. Accordingly, the evolution of this trait in C. hirsuta and A. thaliana shows partially conserved genetic mechanisms but is likely involved in adaptation to different environments.
publishDate 2024
dc.date.none.fl_str_mv 2024
2025
2025
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/375929
https://api.elsevier.com/content/abstract/scopus_id/85210986813
url http://hdl.handle.net/10261/375929
https://api.elsevier.com/content/abstract/scopus_id/85210986813
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
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info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/BES-2017-080063
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/PID2022-136893NB-I00
Plant physiology
application/pdf
https://doi.org/10.1093/plphys/kiae213
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv University of Oxford
publisher.none.fl_str_mv University of Oxford
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
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