Heat stress induces unreduced male gamete formation by targeting meiocyte translation

ABSTRACT Heat stress promotes the formation of unreduced (2n) male gametes through meiotic restitution, a driving force of evolutionary polyploidisation. Here we report that the molecular mechanism underlying heat tolerance of the meiotic division program in Arabidopsis thaliana relies on sustained protein translation of cell cycle genes. By leveraging natural variation in the Arabidopsis population, we identified heat-sensitive and heat-tolerant alleles of TARDY ASYNCHRONOUS MEIOSIS/CYCLINA1;2 (TAM). We show that TAM associates with specialised biomolecular condensates in meiotic cells under high temperatures. Through a mechanism that involves THREE DIVISION MUTANT1 (TDM1), TAM is required to maintain the translation of key meiotic cell cycle genes, including its own, thus preventing premature meiotic exit under heat stress conditions. Boosting TAM translation in heat-sensitive accessions using complementary peptides is sufficient to rescue the heat-induced defects. We propose that this mechanism can play a role in polyploidisation events and plant evolution in the context of the ongoing global climate change.