Variation in responses to N limitation in Solanum lycopersicum var. cerasiforme and S. pimpinellifolium accessions and hybrids reveals genetic potential for improving nitrogen use efficiency (NUE) in tomato breeding

Enhancing nitrogen use efficiency (NUE) is critical in reducing the environmental footprint of agriculture. Wild relatives represent valuable underexploited genetic resources for improving NUE and ensuring sustainable tomato (Solanum lycopersicum L.) production in response to global demand. This stu...

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Autores: Gil-Villar, Daniel, Arrones, Andrea, Gramazio, Pietro, Vilanova, Santiago, Jiménez-Benavente, Eva, Plazas, Mariola, Arbona, Vicent, Granell, Antonio, Medina, Joaquín, Molina, Rosa Victoria, Prohens, Jaime, Nebauer, Sergio G.
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2025
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/406827
Acceso en línea:http://hdl.handle.net/10261/406827
https://api.elsevier.com/content/abstract/scopus_id/105014296216
Access Level:acceso abierto
Palabra clave:Breeding
Low-input agriculture
NUE
Nitrogen
Partition
Tomato
Uptake
Yield
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repository_id_str
dc.title.none.fl_str_mv Variation in responses to N limitation in Solanum lycopersicum var. cerasiforme and S. pimpinellifolium accessions and hybrids reveals genetic potential for improving nitrogen use efficiency (NUE) in tomato breeding
title Variation in responses to N limitation in Solanum lycopersicum var. cerasiforme and S. pimpinellifolium accessions and hybrids reveals genetic potential for improving nitrogen use efficiency (NUE) in tomato breeding
spellingShingle Variation in responses to N limitation in Solanum lycopersicum var. cerasiforme and S. pimpinellifolium accessions and hybrids reveals genetic potential for improving nitrogen use efficiency (NUE) in tomato breeding
Gil-Villar, Daniel
Breeding
Low-input agriculture
NUE
Nitrogen
Partition
Tomato
Uptake
Yield
title_short Variation in responses to N limitation in Solanum lycopersicum var. cerasiforme and S. pimpinellifolium accessions and hybrids reveals genetic potential for improving nitrogen use efficiency (NUE) in tomato breeding
title_full Variation in responses to N limitation in Solanum lycopersicum var. cerasiforme and S. pimpinellifolium accessions and hybrids reveals genetic potential for improving nitrogen use efficiency (NUE) in tomato breeding
title_fullStr Variation in responses to N limitation in Solanum lycopersicum var. cerasiforme and S. pimpinellifolium accessions and hybrids reveals genetic potential for improving nitrogen use efficiency (NUE) in tomato breeding
title_full_unstemmed Variation in responses to N limitation in Solanum lycopersicum var. cerasiforme and S. pimpinellifolium accessions and hybrids reveals genetic potential for improving nitrogen use efficiency (NUE) in tomato breeding
title_sort Variation in responses to N limitation in Solanum lycopersicum var. cerasiforme and S. pimpinellifolium accessions and hybrids reveals genetic potential for improving nitrogen use efficiency (NUE) in tomato breeding
dc.creator.none.fl_str_mv Gil-Villar, Daniel
Arrones, Andrea
Gramazio, Pietro
Vilanova, Santiago
Jiménez-Benavente, Eva
Plazas, Mariola
Arbona, Vicent
Granell, Antonio
Medina, Joaquín
Molina, Rosa Victoria
Prohens, Jaime
Nebauer, Sergio G.
author Gil-Villar, Daniel
author_facet Gil-Villar, Daniel
Arrones, Andrea
Gramazio, Pietro
Vilanova, Santiago
Jiménez-Benavente, Eva
Plazas, Mariola
Arbona, Vicent
Granell, Antonio
Medina, Joaquín
Molina, Rosa Victoria
Prohens, Jaime
Nebauer, Sergio G.
author_role author
author2 Arrones, Andrea
Gramazio, Pietro
Vilanova, Santiago
Jiménez-Benavente, Eva
Plazas, Mariola
Arbona, Vicent
Granell, Antonio
Medina, Joaquín
Molina, Rosa Victoria
Prohens, Jaime
Nebauer, Sergio G.
author2_role author
author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv European Commission
Agencia Estatal de Investigación (España)
Ministerio de Ciencia e Innovación (España)
Generalitat Valenciana
Gil-Villar, Daniel [0000-0003-0051-7037]
Arrones, Andrea [0000-0003-3926-0291]
Gramazio, Pietro [0000-0003-2226-7999]
Vilanova, Santiago [0000-0003-4939-9713]
Plazas, Mariola [0000-0001-8090-7312]
Arbona, Vicent [0000-0003-2232-106X]
Granell, Antonio [0000-0003-4266-9581]
Medina, Joaquín [0000-0002-1735-330X]
Prohens, Jaime [0000-0003-1181-9065]
Nebauer, Sergio G. [0000-0001-7978-6680]
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Breeding
Low-input agriculture
NUE
Nitrogen
Partition
Tomato
Uptake
Yield
topic Breeding
Low-input agriculture
NUE
Nitrogen
Partition
Tomato
Uptake
Yield
description Enhancing nitrogen use efficiency (NUE) is critical in reducing the environmental footprint of agriculture. Wild relatives represent valuable underexploited genetic resources for improving NUE and ensuring sustainable tomato (Solanum lycopersicum L.) production in response to global demand. This study presents an integrative physiological and transcriptomic analysis of four genetically and geographically diverse accessions of S. lycopersicum var. cerasiforme (SLC) and S. pimpinellifolium (SP), along with four interspecific F1 hybrids grown under optimal and sub-optimal N supply levels. These materials were evaluated for their long-term responses, and specific adaptations to N limitation were identified across materials. Specifically, SLC3 displayed high NUE under sub-optimal N supply, primarily due to efficient N partitioning to the fruit, and transcriptional activation of genes associated with photosynthesis and responses to light. Furthermore, SP1 and SP3 accessions presented the highest N uptake efficiency across both N levels, likely linked to differential regulation of genes related to amino acid transport in SP1 and root cell wall growth responses in SP3. Transcriptomic analyses revealed distinct sets of root- and leaf-expressed genes among accessions regulated in response to N availability. Specific combinations of genes involved in N transport, like NPF, NRT2, and amino acid permease families, and C/N metabolism were identified. These results emphasize the potential of SLC and SP accessions as sources of NUE-related alleles, highlighting that their successful incorporation as founders in multiparent MAGIC populations could accelerate breeding for high-yielding, N-efficient tomato cultivars.
publishDate 2025
dc.date.none.fl_str_mv 2025
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/10261/406827
https://api.elsevier.com/content/abstract/scopus_id/105014296216
url http://hdl.handle.net/10261/406827
https://api.elsevier.com/content/abstract/scopus_id/105014296216
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
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info:eu-repo/grantAgreement/AEI//TED2021-129296B-I00
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2020-118627RB-I00
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info:eu-repo/grantAgreement/EC/H2020/101000716
The underlying dataset has been published as supplementary material of the article in the publisher platform at DOI https://doi.org/10.1016/j.plaphy.2025.110428
https://doi.org/10.1016/j.plaphy.2025.110428
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
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dc.publisher.none.fl_str_mv Elsevier
publisher.none.fl_str_mv Elsevier
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
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spelling Variation in responses to N limitation in Solanum lycopersicum var. cerasiforme and S. pimpinellifolium accessions and hybrids reveals genetic potential for improving nitrogen use efficiency (NUE) in tomato breedingGil-Villar, DanielArrones, AndreaGramazio, PietroVilanova, SantiagoJiménez-Benavente, EvaPlazas, MariolaArbona, VicentGranell, AntonioMedina, JoaquínMolina, Rosa VictoriaProhens, JaimeNebauer, Sergio G.BreedingLow-input agricultureNUENitrogenPartitionTomatoUptakeYieldEnhancing nitrogen use efficiency (NUE) is critical in reducing the environmental footprint of agriculture. Wild relatives represent valuable underexploited genetic resources for improving NUE and ensuring sustainable tomato (Solanum lycopersicum L.) production in response to global demand. This study presents an integrative physiological and transcriptomic analysis of four genetically and geographically diverse accessions of S. lycopersicum var. cerasiforme (SLC) and S. pimpinellifolium (SP), along with four interspecific F1 hybrids grown under optimal and sub-optimal N supply levels. These materials were evaluated for their long-term responses, and specific adaptations to N limitation were identified across materials. Specifically, SLC3 displayed high NUE under sub-optimal N supply, primarily due to efficient N partitioning to the fruit, and transcriptional activation of genes associated with photosynthesis and responses to light. Furthermore, SP1 and SP3 accessions presented the highest N uptake efficiency across both N levels, likely linked to differential regulation of genes related to amino acid transport in SP1 and root cell wall growth responses in SP3. Transcriptomic analyses revealed distinct sets of root- and leaf-expressed genes among accessions regulated in response to N availability. Specific combinations of genes involved in N transport, like NPF, NRT2, and amino acid permease families, and C/N metabolism were identified. These results emphasize the potential of SLC and SP accessions as sources of NUE-related alleles, highlighting that their successful incorporation as founders in multiparent MAGIC populations could accelerate breeding for high-yielding, N-efficient tomato cultivars.This work has been funded by MICIU/AEI/10.13039/501100011033, by the European union NextGenerationEU/PRTR (TED2021-129296B-I00), MICIU/AEI/10.13039/501100011033 (PID2020-118627RB-I00), MICIU/AEI/10.13039/501100011033 and ERDF/EU (PID2022-13654IOB-I00), Conselleria d’Educació, Cultura, Universitats i Ocupació from Generalitat Valenciana (CIPROM/2021/020 and CIAICO/2023/167), and European Union's Horizon 2020 research and innovation program under grant agreement No 101000716 (HARNESSTOM project). Pietro Gramazio is grateful for the post-doctoral grant RYC2021-031999-I funded by MICIU/AEI/10.13039/501100011033 and the European Union through NextGenerationEU/PRTR.Peer reviewedElsevierEuropean CommissionAgencia Estatal de Investigación (España)Ministerio de Ciencia e Innovación (España)Generalitat ValencianaGil-Villar, Daniel [0000-0003-0051-7037]Arrones, Andrea [0000-0003-3926-0291]Gramazio, Pietro [0000-0003-2226-7999]Vilanova, Santiago [0000-0003-4939-9713]Plazas, Mariola [0000-0001-8090-7312]Arbona, Vicent [0000-0003-2232-106X]Granell, Antonio [0000-0003-4266-9581]Medina, Joaquín [0000-0002-1735-330X]Prohens, Jaime [0000-0003-1181-9065]Nebauer, Sergio G. [0000-0001-7978-6680]Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202520252025info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionapplication/pdfhttp://hdl.handle.net/10261/406827https://api.elsevier.com/content/abstract/scopus_id/105014296216reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/AEI//TED2021-129296B-I00info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2020-118627RB-I00info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/PID2022-136549OB-I00info:eu-repo/grantAgreement/EC/H2020/101000716The underlying dataset has been published as supplementary material of the article in the publisher platform at DOI https://doi.org/10.1016/j.plaphy.2025.110428https://doi.org/10.1016/j.plaphy.2025.110428Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/4068272026-05-22T06:33:51Z
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