<p>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, <i>THERMOSENSITIVE PARTHENOCARPY 4a</i> (<i>TSP4a</i>) and <i>TSP4b</i>, which encode the transcriptional regulators IAA9 and AINTEGUMENTA (ANT), respectively, to control thermosensitive parthenocarpy. <i>TSP4a</i> and <i>TSP4b</i> form a positive feedback loop upon heat stress to repress auxin signaling in ovaries. Natural <i>TSP4a</i> and <i>TSP4b</i> 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 <i>TSP4a</i> promoter and <i>TSP4b</i> 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.</p>

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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 van der Knaap,
  • Xia Cui

摘要

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.