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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Main Authors: Xiaonan Lu, Jianxin Wu, QianQian Shi, Shuai Sun, Yuan Cheng, Guozhi Zhou, Ren Li, Huanzhong Wang, Esther van der Knaap, Xia Cui
Format: Article
Language:English
Published: Nature Portfolio 2025-05-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-59522-7
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Summary: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.
ISSN:2041-1723