Abstract: Leaf senescence can be triggered by various abiotic stresses. Among these, heat stress emerges as a pivotal environmental factor, particularly in light of the predicted rise in global temperatures. However, the molecular mechanism underlying heat-induced leaf senescence remains largely unexplored. As a cool-season grass species, tall fescue (Festuca arundinacea) is an ideal and imperative material for investigating heat-induced leaf senescence because heat stress easily triggers leaf senescence to influence its forage yield and turf quality. Here, we investigated the role of FaNAC047 in heat-induced leaf senescence. Overexpression of FaNAC047 promoted heat-induced leaf senescence in transgenic tall fescue that was evidenced by a more seriously destructive photosystem and higher accumulation of reactive oxygen species (ROS), whereas knockdown of FaNAC047 delayed leaf senescence. Further protein-DNA interaction assays indicated that FaNAC047 directly activated the transcriptions of NON-YELLOW COLORING 1 (FaNYC1), NYC1-like (FaNOL), and STAY-GREEN (FaSGR) but directly inhibited Catalases 2 (FaCAT2) expression, thereby promoting chlorophyll degradation and ROS accumulation. Subsequently, protein-protein interaction assays revealed that FaNAC047 physically interacted with FaNAC058 to enhance its regulatory effect on FaNYC1, FaNOL, FaSGR, and FaCAT2. Additionally, FaNAC047 could transcriptionally activate FaNAC058 expression to form a regulatory cascade, driving senescence progression. Consistently, the knockdown of FaNAC058 significantly delayed heat-induced leaf senescence. Collectively, our results reveal that FaNAC047-FaNAC058 module coordinately mediates chlorophyll degradation and ROS production to positively regulate heat-induced leaf senescence. The findings illustrate the molecular network of heat-induced leaf senescence for breeding heat-resistant plants.

Key words: chlorophyll catabolic genes, FaCAT2, FaNAC047-FaNAC058 module, heat-induced leaf senescence, ROS production, tall fescue