A feedback loop at the THERMOSENSITIVE PARTHENOCARPY 4 locus controls tomato fruit set under heat stress
Abstract High temperatures compromise crop productivity worldwide, but breeding bottlenecks slow the delivery of climate-resilient crops. By investigating tomato fruit set under high temperatures, we discover a module comprising two linked genes, THERMOSENSITIVE PARTHENOCARPY 4a (TSP4a) and TSP4b, w...
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Nature Portfolio
2025-05-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-025-59522-7 |
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| author | Xiaonan Lu Jianxin Wu QianQian Shi Shuai Sun Yuan Cheng Guozhi Zhou Ren Li Huanzhong Wang Esther van der Knaap Xia Cui |
| author_facet | Xiaonan Lu Jianxin Wu QianQian Shi Shuai Sun Yuan Cheng Guozhi Zhou Ren Li Huanzhong Wang Esther van der Knaap Xia Cui |
| author_sort | Xiaonan Lu |
| collection | DOAJ |
| description | Abstract High temperatures compromise crop productivity worldwide, but breeding bottlenecks slow the delivery of climate-resilient crops. By investigating tomato fruit set under high temperatures, we discover a module comprising two linked genes, THERMOSENSITIVE PARTHENOCARPY 4a (TSP4a) and TSP4b, which encode the transcriptional regulators IAA9 and AINTEGUMENTA (ANT), respectively, to control thermosensitive parthenocarpy. TSP4a and TSP4b form a positive feedback loop upon heat stress to repress auxin signaling in ovaries. Natural TSP4a and TSP4b alleles bear regulatory-region polymorphisms and are differentially expressed to overcome the trade-off between fruit set and wider plant development. Gene editing of the TSP4a promoter and TSP4b 3’ UTR in open-chromatin regions results in expression down-regulation, increased parthenocarpy without yield penalties and maintenance of fruit-sugar levels without broad auxin-related pleiotropic defects in greenhouse-grown plants. These mechanistic insights into heat-induced parthenocarpy and auxin signaling in reproductive organs demonstrate breeding utility to safeguard tomato yield under warming scenarios. |
| format | Article |
| id | doaj-art-88e80d6e29a64a2fb87399bdde16907c |
| institution | Kabale University |
| issn | 2041-1723 |
| language | English |
| publishDate | 2025-05-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj-art-88e80d6e29a64a2fb87399bdde16907c2025-08-20T03:53:13ZengNature PortfolioNature Communications2041-17232025-05-0116111610.1038/s41467-025-59522-7A feedback loop at the THERMOSENSITIVE PARTHENOCARPY 4 locus controls tomato fruit set under heat stressXiaonan Lu0Jianxin Wu1QianQian Shi2Shuai Sun3Yuan Cheng4Guozhi Zhou5Ren Li6Huanzhong Wang7Esther van der Knaap8Xia Cui9State Key Laboratory of Vegetable Biobreeding, Sino–Dutch Joint Laboratory of Horticultural Genomics, Institute of Vegetables and Flowers, Chinese Academy of Agricultural SciencesState Key Laboratory of Vegetable Biobreeding, Sino–Dutch Joint Laboratory of Horticultural Genomics, Institute of Vegetables and Flowers, Chinese Academy of Agricultural SciencesState Key Laboratory of Vegetable Biobreeding, Sino–Dutch Joint Laboratory of Horticultural Genomics, Institute of Vegetables and Flowers, Chinese Academy of Agricultural SciencesState Key Laboratory of Vegetable Biobreeding, Sino–Dutch Joint Laboratory of Horticultural Genomics, Institute of Vegetables and Flowers, Chinese Academy of Agricultural SciencesState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Institute of Vegetables, Zhejiang Academy of Agricultural SciencesState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Institute of Vegetables, Zhejiang Academy of Agricultural SciencesState Key Laboratory of Vegetable Biobreeding, Sino–Dutch Joint Laboratory of Horticultural Genomics, Institute of Vegetables and Flowers, Chinese Academy of Agricultural SciencesDepartment of Plant Science and Landscape Architecture, University of ConnecticutDepartment of Horticulture and Institute of Plant Breeding, Genetics & Genomics University of GeorgiaState Key Laboratory of Vegetable Biobreeding, Sino–Dutch Joint Laboratory of Horticultural Genomics, Institute of Vegetables and Flowers, Chinese Academy of Agricultural SciencesAbstract High temperatures compromise crop productivity worldwide, but breeding bottlenecks slow the delivery of climate-resilient crops. By investigating tomato fruit set under high temperatures, we discover a module comprising two linked genes, THERMOSENSITIVE PARTHENOCARPY 4a (TSP4a) and TSP4b, which encode the transcriptional regulators IAA9 and AINTEGUMENTA (ANT), respectively, to control thermosensitive parthenocarpy. TSP4a and TSP4b form a positive feedback loop upon heat stress to repress auxin signaling in ovaries. Natural TSP4a and TSP4b alleles bear regulatory-region polymorphisms and are differentially expressed to overcome the trade-off between fruit set and wider plant development. Gene editing of the TSP4a promoter and TSP4b 3’ UTR in open-chromatin regions results in expression down-regulation, increased parthenocarpy without yield penalties and maintenance of fruit-sugar levels without broad auxin-related pleiotropic defects in greenhouse-grown plants. These mechanistic insights into heat-induced parthenocarpy and auxin signaling in reproductive organs demonstrate breeding utility to safeguard tomato yield under warming scenarios.https://doi.org/10.1038/s41467-025-59522-7 |
| spellingShingle | Xiaonan Lu Jianxin Wu QianQian Shi Shuai Sun Yuan Cheng Guozhi Zhou Ren Li Huanzhong Wang Esther van der Knaap Xia Cui A feedback loop at the THERMOSENSITIVE PARTHENOCARPY 4 locus controls tomato fruit set under heat stress Nature Communications |
| title | A feedback loop at the THERMOSENSITIVE PARTHENOCARPY 4 locus controls tomato fruit set under heat stress |
| title_full | A feedback loop at the THERMOSENSITIVE PARTHENOCARPY 4 locus controls tomato fruit set under heat stress |
| title_fullStr | A feedback loop at the THERMOSENSITIVE PARTHENOCARPY 4 locus controls tomato fruit set under heat stress |
| title_full_unstemmed | A feedback loop at the THERMOSENSITIVE PARTHENOCARPY 4 locus controls tomato fruit set under heat stress |
| title_short | A feedback loop at the THERMOSENSITIVE PARTHENOCARPY 4 locus controls tomato fruit set under heat stress |
| title_sort | feedback loop at the thermosensitive parthenocarpy 4 locus controls tomato fruit set under heat stress |
| url | https://doi.org/10.1038/s41467-025-59522-7 |
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