RNA-Seq-based analysis of transcriptomic signatures elicited by mutations conferring salt tolerance in Cucurbita pepo

Salinity is a major determinant of plant growth and crop productivity, resulting in significant economic losses in agriculture. Improving salinity tolerance in plant breeding programs requires not only donor tolerant genotypes but also a thorough knowledge of the genes controlling the trait. Taking...

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Main Authors: Keshav Gautam, Sonsoles Alonso, Alicia García, María Segura, Álvaro Benítez, Cecilia Martínez, Manuel Jamilena
Format: Article
Language:English
Published: Elsevier 2025-03-01
Series:Plant Stress
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Online Access:http://www.sciencedirect.com/science/article/pii/S2667064X25000405
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author Keshav Gautam
Sonsoles Alonso
Alicia García
María Segura
Álvaro Benítez
Cecilia Martínez
Manuel Jamilena
author_facet Keshav Gautam
Sonsoles Alonso
Alicia García
María Segura
Álvaro Benítez
Cecilia Martínez
Manuel Jamilena
author_sort Keshav Gautam
collection DOAJ
description Salinity is a major determinant of plant growth and crop productivity, resulting in significant economic losses in agriculture. Improving salinity tolerance in plant breeding programs requires not only donor tolerant genotypes but also a thorough knowledge of the genes controlling the trait. Taking advantage of two recently identified salinity-tolerant EMS mutants of squash (sal-1 and sal-2), this study aimed to analyse whether these two sources of salt tolerance are associated with similar transcriptomic changes in leaves. RNA sequencing revealed that the two mutants have a very distinct transcriptomic response to salt stress compared to the WT, with 154 and 1068 salt-tolerance-associated differentially expressed genes (DEGs) in sal-1 and sal-2, respectively. GO and KEGG enrichment analyses revealed the importance of several phytohormone biosynthesis, signalling and transport genes (CpAUX22B/22D, CpSAUR32–2, CpARR5/12, CpAHK2/3, CpBZR1, CpTCH4, CpNCED1, CpCYP707A1, CpPP2C, CpSnRK1/2, CpLOX2 and CpACX) in the salt tolerance response. MAPK genes (CpMPK3 and CpMEKK1) and the Ca²⁺ signalling network (CpCPK26/28/34, CpCML31/36/48, CpPBP1, CpCBL1 and CpRBOHD) were also specifically activated in salt-tolerant mutants, indicating their contribution to salt tolerance. Genes for antioxidant enzymes (PP2, POD, CAT, PRX, GST and GRX) and cell wall metabolism were also up-regulated in salt-tolerant mutants, reducing oxidative stress and maintaining the integrity of membranes and other cellular structures. Genes for ion transporters were significantly up-regulated in response to salt stress in sal-2, probably involved in maintaining ion homeostasis. Several genes encoding transcription factors of the ERF, C3H, Dof, HD-ZIP, MYB, HSF, NAC, knotted and WRKY families, as well as long non-coding RNA, were also found to positively or negatively regulate salt stress tolerance in the sal-1 and sal-2 mutants. Overall, the results highlight the complexity of the molecular response involved in salt stress tolerance in C. pepo and prioritise further investigation of specific genes that contribute to the resilience of crops under saline conditions.
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spelling doaj-art-cda4669b5a1f4f8096c6a40c443144982025-08-20T02:55:52ZengElsevierPlant Stress2667-064X2025-03-011510077510.1016/j.stress.2025.100775RNA-Seq-based analysis of transcriptomic signatures elicited by mutations conferring salt tolerance in Cucurbita pepoKeshav Gautam0Sonsoles Alonso1Alicia García2María Segura3Álvaro Benítez4Cecilia Martínez5Manuel Jamilena6Department of Biology and Geology. Agri-food Campus of International Excellence (CeiA3) and Research Center CIAIMBITAL, University of Almería, 04120, Almería, SpainDepartment of Biology and Geology. Agri-food Campus of International Excellence (CeiA3) and Research Center CIAIMBITAL, University of Almería, 04120, Almería, SpainDepartment of Biology and Geology. Agri-food Campus of International Excellence (CeiA3) and Research Center CIAIMBITAL, University of Almería, 04120, Almería, SpainDepartment of Biology and Geology. Agri-food Campus of International Excellence (CeiA3) and Research Center CIAIMBITAL, University of Almería, 04120, Almería, SpainDepartment of Biology and Geology. Agri-food Campus of International Excellence (CeiA3) and Research Center CIAIMBITAL, University of Almería, 04120, Almería, SpainCorresponding authors.; Department of Biology and Geology. Agri-food Campus of International Excellence (CeiA3) and Research Center CIAIMBITAL, University of Almería, 04120, Almería, SpainCorresponding authors.; Department of Biology and Geology. Agri-food Campus of International Excellence (CeiA3) and Research Center CIAIMBITAL, University of Almería, 04120, Almería, SpainSalinity is a major determinant of plant growth and crop productivity, resulting in significant economic losses in agriculture. Improving salinity tolerance in plant breeding programs requires not only donor tolerant genotypes but also a thorough knowledge of the genes controlling the trait. Taking advantage of two recently identified salinity-tolerant EMS mutants of squash (sal-1 and sal-2), this study aimed to analyse whether these two sources of salt tolerance are associated with similar transcriptomic changes in leaves. RNA sequencing revealed that the two mutants have a very distinct transcriptomic response to salt stress compared to the WT, with 154 and 1068 salt-tolerance-associated differentially expressed genes (DEGs) in sal-1 and sal-2, respectively. GO and KEGG enrichment analyses revealed the importance of several phytohormone biosynthesis, signalling and transport genes (CpAUX22B/22D, CpSAUR32–2, CpARR5/12, CpAHK2/3, CpBZR1, CpTCH4, CpNCED1, CpCYP707A1, CpPP2C, CpSnRK1/2, CpLOX2 and CpACX) in the salt tolerance response. MAPK genes (CpMPK3 and CpMEKK1) and the Ca²⁺ signalling network (CpCPK26/28/34, CpCML31/36/48, CpPBP1, CpCBL1 and CpRBOHD) were also specifically activated in salt-tolerant mutants, indicating their contribution to salt tolerance. Genes for antioxidant enzymes (PP2, POD, CAT, PRX, GST and GRX) and cell wall metabolism were also up-regulated in salt-tolerant mutants, reducing oxidative stress and maintaining the integrity of membranes and other cellular structures. Genes for ion transporters were significantly up-regulated in response to salt stress in sal-2, probably involved in maintaining ion homeostasis. Several genes encoding transcription factors of the ERF, C3H, Dof, HD-ZIP, MYB, HSF, NAC, knotted and WRKY families, as well as long non-coding RNA, were also found to positively or negatively regulate salt stress tolerance in the sal-1 and sal-2 mutants. Overall, the results highlight the complexity of the molecular response involved in salt stress tolerance in C. pepo and prioritise further investigation of specific genes that contribute to the resilience of crops under saline conditions.http://www.sciencedirect.com/science/article/pii/S2667064X25000405RNA-seqTranscription FactorCucurbita pepoPhytohormonesSalt stress
spellingShingle Keshav Gautam
Sonsoles Alonso
Alicia García
María Segura
Álvaro Benítez
Cecilia Martínez
Manuel Jamilena
RNA-Seq-based analysis of transcriptomic signatures elicited by mutations conferring salt tolerance in Cucurbita pepo
Plant Stress
RNA-seq
Transcription Factor
Cucurbita pepo
Phytohormones
Salt stress
title RNA-Seq-based analysis of transcriptomic signatures elicited by mutations conferring salt tolerance in Cucurbita pepo
title_full RNA-Seq-based analysis of transcriptomic signatures elicited by mutations conferring salt tolerance in Cucurbita pepo
title_fullStr RNA-Seq-based analysis of transcriptomic signatures elicited by mutations conferring salt tolerance in Cucurbita pepo
title_full_unstemmed RNA-Seq-based analysis of transcriptomic signatures elicited by mutations conferring salt tolerance in Cucurbita pepo
title_short RNA-Seq-based analysis of transcriptomic signatures elicited by mutations conferring salt tolerance in Cucurbita pepo
title_sort rna seq based analysis of transcriptomic signatures elicited by mutations conferring salt tolerance in cucurbita pepo
topic RNA-seq
Transcription Factor
Cucurbita pepo
Phytohormones
Salt stress
url http://www.sciencedirect.com/science/article/pii/S2667064X25000405
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