Direct coupling of PSK peptide signaling to ROS generation by PSKR1-RBOHB safeguards pollen thermotolerance in tomato.

Abstract

Heat stress poses a major threat to global crop productivity, with the male gametophyte being the most thermosensitive stage. While peptide hormones are known orchestrators of plant vegetative adaptation, their roles in reproductive thermotolerance remain largely undefined. Here, we show that phytosulfokine (PSK) signaling determines tomato pollen thermotolerance, as heat-induced anther PSK precursor expression correlates with pollen germination, and exogenous PSK application mitigates heat-induced pollen abortion. Loss of the PSK receptor (PSKR) PSKR1 or the NADPH oxidase Respiratory burst oxidase homolog B (RBOHB) compromises reactive oxygen species (ROS) homeostasis and pollen thermotolerance, causing severe yield losses under both controlled and natural field heat-stress conditions. Mechanistically, genetic rescue experiments establish that RBOHB-dependent ROS signaling functions downstream of PSK perception driven by PSKR1-mediated phosphorylation of RBOHB at threonine-266 and serine-340 in pollen grains, which triggers protective ROS bursts to activate the downstream heat shock transcription factor/heat shock protein pathway. Genetic complementation with phospho-mimic variants confirms that phosphorylation at these residues is sufficient to enhance pollen thermotolerance. Our findings define a PSK peptide-ROS signaling axis that safeguards male thermotolerance, providing both genetic targets and peptide-based strategies for sustaining crop yields in a warming climate.