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

Xiaonan Lu, Jianxin Wu, QianQian Shi, Shuai Sun, Yuan Cheng, Guozhi Zhou, Ren Li, Huanzhong Wang, Esther Knaap and Xia Cui ()
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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

Nature Communications, 2025, vol. 16, issue 1, 1-16

Abstract: 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.

Date: 2025
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DOI: 10.1038/s41467-025-59522-7

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