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A feedback loop at the THERMOSENSITIVE PARTHENOCARPY 4 locus controls tomato fruit set under heat stress

Author

Listed:
  • Xiaonan Lu

    (Chinese Academy of Agricultural Sciences)

  • Jianxin Wu

    (Chinese Academy of Agricultural Sciences)

  • QianQian Shi

    (Chinese Academy of Agricultural Sciences)

  • Shuai Sun

    (Chinese Academy of Agricultural Sciences)

  • Yuan Cheng

    (Zhejiang Academy of Agricultural Sciences)

  • Guozhi Zhou

    (Zhejiang Academy of Agricultural Sciences)

  • Ren Li

    (Chinese Academy of Agricultural Sciences)

  • Huanzhong Wang

    (University of Connecticut)

  • Esther Knaap

    (Genetics & Genomics University of Georgia)

  • Xia Cui

    (Chinese Academy of Agricultural Sciences
    Zhejiang A&F University)

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.

Suggested Citation

  • Xiaonan Lu & Jianxin Wu & QianQian Shi & Shuai Sun & Yuan Cheng & Guozhi Zhou & Ren Li & Huanzhong Wang & Esther Knaap & Xia Cui, 2025. "A feedback loop at the THERMOSENSITIVE PARTHENOCARPY 4 locus controls tomato fruit set under heat stress," Nature Communications, Nature, vol. 16(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-59522-7
    DOI: 10.1038/s41467-025-59522-7
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    References listed on IDEAS

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    1. Ren Li & Shuai Sun & Haijing Wang & Ketao Wang & Hong Yu & Zhen Zhou & Peiyong Xin & Jinfang Chu & Tongmin Zhao & Huanzhong Wang & Jiayang Li & Xia Cui, 2020. "FIS1 encodes a GA2-oxidase that regulates fruit firmness in tomato," Nature Communications, Nature, vol. 11(1), pages 1-12, December.
    2. Shuai Sun & Zhiqiang Liu & Xiaotian Wang & Jia Song & Siyu Fang & Jisheng Kong & Ren Li & Huanzhong Wang & Xia Cui, 2024. "Genetic control of thermomorphogenesis in tomato inflorescences," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
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