Cutin formation in tomato is controlled by a multipartite module of synergistic and antagonistic transcription factors

Summary: Cuticles protect plants from water loss and pathogen attack. We address here the functional significance of SlGRAS9, SlZHD17, and SlMBP3 in regulating cutin formation in tomato fruit. The study unveils the role of the multipartite “SlGRAS9-SlZHD17-SlMBP3-SlMIXTA-like” transcription factor m...

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Main Authors: Yuan Shi, Changhao Deng, Xiangyin Lu, Yan Wang, Yaowen Pan, Deding Su, Wang Lu, Yuxiang Lin, Rui Li, Junnan Han, Yanwei Hao, Yi Chen, Ghassen Abid, Julien Pirrello, Mondher Bouzayen, Yudong Liu, Zhengguo Li, Baowen Huang
Format: Article
Language:English
Published: Elsevier 2025-02-01
Series:Cell Reports
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Online Access:http://www.sciencedirect.com/science/article/pii/S2211124725000294
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author Yuan Shi
Changhao Deng
Xiangyin Lu
Yan Wang
Yaowen Pan
Deding Su
Wang Lu
Yuxiang Lin
Rui Li
Junnan Han
Yanwei Hao
Yi Chen
Ghassen Abid
Julien Pirrello
Mondher Bouzayen
Yudong Liu
Zhengguo Li
Baowen Huang
author_facet Yuan Shi
Changhao Deng
Xiangyin Lu
Yan Wang
Yaowen Pan
Deding Su
Wang Lu
Yuxiang Lin
Rui Li
Junnan Han
Yanwei Hao
Yi Chen
Ghassen Abid
Julien Pirrello
Mondher Bouzayen
Yudong Liu
Zhengguo Li
Baowen Huang
author_sort Yuan Shi
collection DOAJ
description Summary: Cuticles protect plants from water loss and pathogen attack. We address here the functional significance of SlGRAS9, SlZHD17, and SlMBP3 in regulating cutin formation in tomato fruit. The study unveils the role of the multipartite “SlGRAS9-SlZHD17-SlMBP3-SlMIXTA-like” transcription factor module in cutin biosynthesis. Plants deficient in SlGRAS9, SlZHD17, or SlMBP3 exhibit thickened cuticles and a higher accumulation of cutin monomers, conferring extended fruit shelf life and higher tolerance to postharvest fungal infection. SlGRAS9 regulation of cutin is mediated by SlZHD17, a negative regulator of SlCYP86A69. SlZHD17 acts synergistically with SlMBP3 to repress SlCYP86A69, and its interaction with SlMIXTA-like prevents the binding to the SlCYP86A69 promoter, thereby releasing the repression of cutin biosynthesis. SlZHD17 and SlMBP3 synergistically repress cutin biosynthesis, while SlMIXTA-like and SlCD2 act antagonistically to SlZHD17 and SlMBP3 on this metabolic pathway. The study defines targets for breeding strategies aimed at improving cuticle-associated traits in tomato and potentially other crops.
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spelling doaj-art-0f813fbbf04d4f4886430240faead68e2025-02-02T05:27:06ZengElsevierCell Reports2211-12472025-02-01442115258Cutin formation in tomato is controlled by a multipartite module of synergistic and antagonistic transcription factorsYuan Shi0Changhao Deng1Xiangyin Lu2Yan Wang3Yaowen Pan4Deding Su5Wang Lu6Yuxiang Lin7Rui Li8Junnan Han9Yanwei Hao10Yi Chen11Ghassen Abid12Julien Pirrello13Mondher Bouzayen14Yudong Liu15Zhengguo Li16Baowen Huang17Key Laboratory of Plant Hormones Regulation and Molecular Breeding of Chongqing, School of Life Sciences, Chongqing University, Chongqing 401331, China; Center of Plant Functional Genomics and Synthetic Biology, Institute of Advanced Interdisciplinary Studies, Chongqing University, Chongqing 401331, ChinaKey Laboratory of Plant Hormones Regulation and Molecular Breeding of Chongqing, School of Life Sciences, Chongqing University, Chongqing 401331, China; Center of Plant Functional Genomics and Synthetic Biology, Institute of Advanced Interdisciplinary Studies, Chongqing University, Chongqing 401331, ChinaKey Laboratory of Plant Hormones Regulation and Molecular Breeding of Chongqing, School of Life Sciences, Chongqing University, Chongqing 401331, China; Center of Plant Functional Genomics and Synthetic Biology, Institute of Advanced Interdisciplinary Studies, Chongqing University, Chongqing 401331, ChinaKey Laboratory of Plant Hormones Regulation and Molecular Breeding of Chongqing, School of Life Sciences, Chongqing University, Chongqing 401331, China; Center of Plant Functional Genomics and Synthetic Biology, Institute of Advanced Interdisciplinary Studies, Chongqing University, Chongqing 401331, ChinaKey Laboratory of Plant Hormones Regulation and Molecular Breeding of Chongqing, School of Life Sciences, Chongqing University, Chongqing 401331, China; Center of Plant Functional Genomics and Synthetic Biology, Institute of Advanced Interdisciplinary Studies, Chongqing University, Chongqing 401331, ChinaKey Laboratory of Plant Hormones Regulation and Molecular Breeding of Chongqing, School of Life Sciences, Chongqing University, Chongqing 401331, China; Center of Plant Functional Genomics and Synthetic Biology, Institute of Advanced Interdisciplinary Studies, Chongqing University, Chongqing 401331, ChinaKey Laboratory of Plant Hormones Regulation and Molecular Breeding of Chongqing, School of Life Sciences, Chongqing University, Chongqing 401331, China; Center of Plant Functional Genomics and Synthetic Biology, Institute of Advanced Interdisciplinary Studies, Chongqing University, Chongqing 401331, ChinaKey Laboratory of Plant Hormones Regulation and Molecular Breeding of Chongqing, School of Life Sciences, Chongqing University, Chongqing 401331, China; Center of Plant Functional Genomics and Synthetic Biology, Institute of Advanced Interdisciplinary Studies, Chongqing University, Chongqing 401331, ChinaKey Laboratory of Plant Hormones Regulation and Molecular Breeding of Chongqing, School of Life Sciences, Chongqing University, Chongqing 401331, China; Center of Plant Functional Genomics and Synthetic Biology, Institute of Advanced Interdisciplinary Studies, Chongqing University, Chongqing 401331, ChinaKey Laboratory of Plant Hormones Regulation and Molecular Breeding of Chongqing, School of Life Sciences, Chongqing University, Chongqing 401331, China; Center of Plant Functional Genomics and Synthetic Biology, Institute of Advanced Interdisciplinary Studies, Chongqing University, Chongqing 401331, ChinaCollege of Horticulture, South China Agricultural University, Guangzhou 510642, ChinaZhejiang Key Laboratory of Intelligent Food Logistic and Processing, State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Zhejiang-Malaysia Joint Research Laboratory for Agricultural Product Processing and Nutrition, College of Food Science and Engineering, Ningbo University, Ningbo 315800, ChinaCentre of Biotechnology of Borj-Cedria, Laboratory of Legumes and Sustainable Agrosystems, P.B. 901, Hammam-Lif 2050, TunisiaLaboratoire de Recherche en Sciences Vegetales - Genomique et Biotechnologie des Fruits - UMR5546, Toulouse-INP, CNRS, UPS, Universite de Toulouse, Toulouse, FranceCenter of Plant Functional Genomics and Synthetic Biology, Institute of Advanced Interdisciplinary Studies, Chongqing University, Chongqing 401331, China; Laboratoire de Recherche en Sciences Vegetales - Genomique et Biotechnologie des Fruits - UMR5546, Toulouse-INP, CNRS, UPS, Universite de Toulouse, Toulouse, France; Corresponding authorSchool of Agricultural Sciences, Zhengzhou University, Zhengzhou 450001, China; Corresponding authorKey Laboratory of Plant Hormones Regulation and Molecular Breeding of Chongqing, School of Life Sciences, Chongqing University, Chongqing 401331, China; Center of Plant Functional Genomics and Synthetic Biology, Institute of Advanced Interdisciplinary Studies, Chongqing University, Chongqing 401331, China; Corresponding authorKey Laboratory of Plant Hormones Regulation and Molecular Breeding of Chongqing, School of Life Sciences, Chongqing University, Chongqing 401331, China; Center of Plant Functional Genomics and Synthetic Biology, Institute of Advanced Interdisciplinary Studies, Chongqing University, Chongqing 401331, China; Corresponding authorSummary: Cuticles protect plants from water loss and pathogen attack. We address here the functional significance of SlGRAS9, SlZHD17, and SlMBP3 in regulating cutin formation in tomato fruit. The study unveils the role of the multipartite “SlGRAS9-SlZHD17-SlMBP3-SlMIXTA-like” transcription factor module in cutin biosynthesis. Plants deficient in SlGRAS9, SlZHD17, or SlMBP3 exhibit thickened cuticles and a higher accumulation of cutin monomers, conferring extended fruit shelf life and higher tolerance to postharvest fungal infection. SlGRAS9 regulation of cutin is mediated by SlZHD17, a negative regulator of SlCYP86A69. SlZHD17 acts synergistically with SlMBP3 to repress SlCYP86A69, and its interaction with SlMIXTA-like prevents the binding to the SlCYP86A69 promoter, thereby releasing the repression of cutin biosynthesis. SlZHD17 and SlMBP3 synergistically repress cutin biosynthesis, while SlMIXTA-like and SlCD2 act antagonistically to SlZHD17 and SlMBP3 on this metabolic pathway. The study defines targets for breeding strategies aimed at improving cuticle-associated traits in tomato and potentially other crops.http://www.sciencedirect.com/science/article/pii/S2211124725000294CP: Plants
spellingShingle Yuan Shi
Changhao Deng
Xiangyin Lu
Yan Wang
Yaowen Pan
Deding Su
Wang Lu
Yuxiang Lin
Rui Li
Junnan Han
Yanwei Hao
Yi Chen
Ghassen Abid
Julien Pirrello
Mondher Bouzayen
Yudong Liu
Zhengguo Li
Baowen Huang
Cutin formation in tomato is controlled by a multipartite module of synergistic and antagonistic transcription factors
Cell Reports
CP: Plants
title Cutin formation in tomato is controlled by a multipartite module of synergistic and antagonistic transcription factors
title_full Cutin formation in tomato is controlled by a multipartite module of synergistic and antagonistic transcription factors
title_fullStr Cutin formation in tomato is controlled by a multipartite module of synergistic and antagonistic transcription factors
title_full_unstemmed Cutin formation in tomato is controlled by a multipartite module of synergistic and antagonistic transcription factors
title_short Cutin formation in tomato is controlled by a multipartite module of synergistic and antagonistic transcription factors
title_sort cutin formation in tomato is controlled by a multipartite module of synergistic and antagonistic transcription factors
topic CP: Plants
url http://www.sciencedirect.com/science/article/pii/S2211124725000294
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