Cold weather cause severe crop losses. Climate change exacerbates the unpredictability and frequency of such weather events, highlighting the need for cold-resilient crops1. Cold-induced pollen abortion and reproductive failure during flowering are major causes of yield losses2,3, yet the molecular mechanisms and signalling pathways that underlie cold resilience in pollen development remain unknown. Here we identify a subset of cold-responsive small signalling peptides in the RGF–GLV–CLEL family, SlRGF9 and SlRGF10, that control cold resilience in tomato pollen. After loss of function of SlRGF9 and SlRGF10, tomato plants (Solanum lycopersicum) showed no defects under normal conditions, but pollen abortion was observed after cold stress. The leucine-rich repeat receptor-like kinases, SlRGFR6 and SlSERK proteins, form cell-surface receptor complexes that bind to these cold-induced SlRGFs. Furthermore, SlRGF–SlRGFR6 signalling activates calcium influx through cyclic-nucleotide-gated channels, counteracting cold-delayed programmed cell death and ensuring tapetum degradation to support microspore development. Upregulating SlRGF9 and SlRGF10 in tomato plants prevents cold-induced yield losses by up to 52%. This cold-responsive peptide signalling pathway is conserved across dicots and monocots. For example, upregulation of RGF homologues in rice (Oryza sativa) boosts cold resilience in pollen and recovers 18.3% of grain yield loss. Our findings uncover a core peptide signalling axis that governs cold resilience in pollen and has broad potential for safeguarding crop productivity against cold stress.
