Aethionema arabicum dimorphic seed trait resetting during transition to seedlings

The transition from germinating seeds to emerging seedlings is one of the most vulnerable plant life cycle stages. Heteromorphic diaspores (seed and fruit dispersal units) are an adaptive bet-hedging strategy to cope with spatiotemporally variable environments. While the roles and mechanisms of seed...

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Autores: Arshad, Waheed, Steinbrecher, Tina, Wilhelmsson, Per K I, Fernández-Pozo, Noé, Pérez, Marta, Mérai, Zsuzsanna, Rensing, Stefan A, Chandler, Jake O, Leubner-Metzger, Gerhard
Tipo de recurso: artículo
Estado:Versión aceptada para publicación
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:10261/370456
Acceso en línea:http://hdl.handle.net/10261/370456
https://api.elsevier.com/content/abstract/scopus_id/85188246195
Access Level:acceso abierto
Palabra clave:bet-hedging strategy
diaspore dimorphism
fruit and seed heteromorphism
pericarp-imposed dormancy
pre-emergence growth
seed seedling transition
seedling stress resilience
transcriptome resetting
id ES_e28fd37d8531d922ba3eef2ce9d34b4a
oai_identifier_str oai:digital.csic.es:10261/370456
network_acronym_str ES
network_name_str España
repository_id_str
dc.title.none.fl_str_mv Aethionema arabicum dimorphic seed trait resetting during transition to seedlings
title Aethionema arabicum dimorphic seed trait resetting during transition to seedlings
spellingShingle Aethionema arabicum dimorphic seed trait resetting during transition to seedlings
Arshad, Waheed
bet-hedging strategy
diaspore dimorphism
fruit and seed heteromorphism
pericarp-imposed dormancy
pre-emergence growth
seed seedling transition
seedling stress resilience
transcriptome resetting
title_short Aethionema arabicum dimorphic seed trait resetting during transition to seedlings
title_full Aethionema arabicum dimorphic seed trait resetting during transition to seedlings
title_fullStr Aethionema arabicum dimorphic seed trait resetting during transition to seedlings
title_full_unstemmed Aethionema arabicum dimorphic seed trait resetting during transition to seedlings
title_sort Aethionema arabicum dimorphic seed trait resetting during transition to seedlings
dc.creator.none.fl_str_mv Arshad, Waheed
Steinbrecher, Tina
Wilhelmsson, Per K I
Fernández-Pozo, Noé
Pérez, Marta
Mérai, Zsuzsanna
Rensing, Stefan A
Chandler, Jake O
Leubner-Metzger, Gerhard
author Arshad, Waheed
author_facet Arshad, Waheed
Steinbrecher, Tina
Wilhelmsson, Per K I
Fernández-Pozo, Noé
Pérez, Marta
Mérai, Zsuzsanna
Rensing, Stefan A
Chandler, Jake O
Leubner-Metzger, Gerhard
author_role author
author2 Steinbrecher, Tina
Wilhelmsson, Per K I
Fernández-Pozo, Noé
Pérez, Marta
Mérai, Zsuzsanna
Rensing, Stefan A
Chandler, Jake O
Leubner-Metzger, Gerhard
author2_role author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Biotechnology and Biological Sciences Research Council (UK)
Natural Environment Research Council (UK)
German Research Foundation
Ministerio de Ciencia e Innovación (España)
European Commission
National Research Data Infrastructure (Germany)
0000-0002-9413-2279
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv bet-hedging strategy
diaspore dimorphism
fruit and seed heteromorphism
pericarp-imposed dormancy
pre-emergence growth
seed seedling transition
seedling stress resilience
transcriptome resetting
topic bet-hedging strategy
diaspore dimorphism
fruit and seed heteromorphism
pericarp-imposed dormancy
pre-emergence growth
seed seedling transition
seedling stress resilience
transcriptome resetting
description The transition from germinating seeds to emerging seedlings is one of the most vulnerable plant life cycle stages. Heteromorphic diaspores (seed and fruit dispersal units) are an adaptive bet-hedging strategy to cope with spatiotemporally variable environments. While the roles and mechanisms of seedling traits have been studied in monomorphic species, which produce one type of diaspore, very little is known about seedlings in heteromorphic species. Using the dimorphic diaspore model Aethionema arabicum (Brassicaceae), we identified contrasting mechanisms in the germination responses to different temperatures of the mucilaginous seeds (M+ seed morphs), the dispersed indehiscent fruits (IND fruit morphs), and the bare non-mucilaginous M- seeds obtained from IND fruits by pericarp (fruit coat) removal. What follows the completion of germination is the pre-emergence seedling growth phase, which we investigated by comparative growth assays of early seedlings derived from the M+ seeds, bare M- seeds, and IND fruits. The dimorphic seedlings derived from M+ and M- seeds did not differ in their responses to ambient temperature and water potential. The phenotype of seedlings derived from IND fruits differed in that they had bent hypocotyls and their shoot and root growth was slower, but the biomechanical hypocotyl properties of 15-day-old seedlings did not differ between seedlings derived from germinated M+ seeds, M- seeds, or IND fruits. Comparison of the transcriptomes of the natural dimorphic diaspores, M+ seeds and IND fruits, identified 2,682 differentially expressed genes (DEGs) during late germination. During the subsequent 3 days of seedling pre-emergence growth, the number of DEGs was reduced 10-fold to 277 root DEGs and 16-fold to 164 shoot DEGs. Among the DEGs in early seedlings were hormonal regulators, in particular for auxin, ethylene, and gibberellins. Furthermore, DEGs were identified for water and ion transporters, nitrate transporter and assimilation enzymes, and cell wall remodeling protein genes encoding enzymes targeting xyloglucan and pectin. We conclude that the transcriptomes of seedlings derived from the dimorphic diaspores, M+ seeds and IND fruits, undergo transcriptional resetting during the post-germination pre-emergence growth transition phase from germinated diaspores to growing seedlings.
publishDate 2024
dc.date.none.fl_str_mv 2024
2024
2024
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Postprint
info:eu-repo/semantics/acceptedVersion
format article
status_str acceptedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/370456
https://api.elsevier.com/content/abstract/scopus_id/85188246195
url http://hdl.handle.net/10261/370456
https://api.elsevier.com/content/abstract/scopus_id/85188246195
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
#PLACEHOLDER_PARENT_METADATA_VALUE#
info:eu-repo/grantAgreement/AEI//RYC2020-030219-I
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/PID2021-125805OA-I00
Frontiers in plant science
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv Frontiers Media
publisher.none.fl_str_mv Frontiers Media
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)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
repository.mail.fl_str_mv
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spelling Aethionema arabicum dimorphic seed trait resetting during transition to seedlingsArshad, WaheedSteinbrecher, TinaWilhelmsson, Per K IFernández-Pozo, NoéPérez, MartaMérai, ZsuzsannaRensing, Stefan AChandler, Jake OLeubner-Metzger, Gerhardbet-hedging strategydiaspore dimorphismfruit and seed heteromorphismpericarp-imposed dormancypre-emergence growthseed seedling transitionseedling stress resiliencetranscriptome resettingThe transition from germinating seeds to emerging seedlings is one of the most vulnerable plant life cycle stages. Heteromorphic diaspores (seed and fruit dispersal units) are an adaptive bet-hedging strategy to cope with spatiotemporally variable environments. While the roles and mechanisms of seedling traits have been studied in monomorphic species, which produce one type of diaspore, very little is known about seedlings in heteromorphic species. Using the dimorphic diaspore model Aethionema arabicum (Brassicaceae), we identified contrasting mechanisms in the germination responses to different temperatures of the mucilaginous seeds (M+ seed morphs), the dispersed indehiscent fruits (IND fruit morphs), and the bare non-mucilaginous M- seeds obtained from IND fruits by pericarp (fruit coat) removal. What follows the completion of germination is the pre-emergence seedling growth phase, which we investigated by comparative growth assays of early seedlings derived from the M+ seeds, bare M- seeds, and IND fruits. The dimorphic seedlings derived from M+ and M- seeds did not differ in their responses to ambient temperature and water potential. The phenotype of seedlings derived from IND fruits differed in that they had bent hypocotyls and their shoot and root growth was slower, but the biomechanical hypocotyl properties of 15-day-old seedlings did not differ between seedlings derived from germinated M+ seeds, M- seeds, or IND fruits. Comparison of the transcriptomes of the natural dimorphic diaspores, M+ seeds and IND fruits, identified 2,682 differentially expressed genes (DEGs) during late germination. During the subsequent 3 days of seedling pre-emergence growth, the number of DEGs was reduced 10-fold to 277 root DEGs and 16-fold to 164 shoot DEGs. Among the DEGs in early seedlings were hormonal regulators, in particular for auxin, ethylene, and gibberellins. Furthermore, DEGs were identified for water and ion transporters, nitrate transporter and assimilation enzymes, and cell wall remodeling protein genes encoding enzymes targeting xyloglucan and pectin. We conclude that the transcriptomes of seedlings derived from the dimorphic diaspores, M+ seeds and IND fruits, undergo transcriptional resetting during the post-germination pre-emergence growth transition phase from germinated diaspores to growing seedlings.This work is part of the ERA-CAPS “SeedAdapt” consortium project which was led Arshad et al. 10.3389/fpls.2024.1358312 by GL-M, and funded by grants from the Biotechnology and Biological Sciences Research Council (BBSRC) to GL-M (BB/M00192X/1), from the Natural Environment Research Council (NERC) through a Doctoral Training Grant to WA (NE/L002485/1), from the Deutsche Forschungsgemeinschaft (DFG) SR (RE 1697/8-1),from Ministerio de Ciencia e Innovación (MCIN/AEI/10.13039/501100011033) and the European Social Fund to NFP (RYC2020-030219-I and PID2021- 125805OA-I00), from the Austrian Science Fund (FWF) to ZM (FWF I3979-B25). We also acknowledge the support of DataPLANT to SAR (NFDI 7/1 -42077441) as part of the German National Research Data Infrastructure.Peer reviewedFrontiers MediaBiotechnology and Biological Sciences Research Council (UK)Natural Environment Research Council (UK)German Research FoundationMinisterio de Ciencia e Innovación (España)European CommissionNational Research Data Infrastructure (Germany)0000-0002-9413-2279Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202420242024info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Postprintinfo:eu-repo/semantics/acceptedVersionhttp://hdl.handle.net/10261/370456https://api.elsevier.com/content/abstract/scopus_id/85188246195reponame: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//RYC2020-030219-Iinfo:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/PID2021-125805OA-I00Frontiers in plant scienceSíinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3704562026-05-22T06:33:51Z
score 15,812455

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