SlCSAPlike-PGM interaction modulates starch accumulation to regulate leaf senescence in tomato

SlCSAPlike reduces leaf starch content and drives premature senescence by enhancing PGM enzyme activity to promote the conversion of G1P to G6P. The SlCSAPlike-PGM interaction disrupts carbon balance and triggers chloroplast degradation without relying on transcriptional activation of senescence programs SlCSAPlike is identified as a key regulator of leaf senescence, providing a novel strategy for targeted delay of leaf senescence. Premature leaf senescence significantly impacts tomato yield and quality. Understanding the molecular mechanisms underlying tomato leaf senescence holds important theoretical and practical significance for extending tomato fertility and improving yield and quality. This study identified SlCSAPlike, a DUF1997 protein, as playing a crucial role in regulating leaf senescence. Overexpression of SlCSAPlike accelerated senescence, while knockout of SlCSAPlike delayed the senescence process. SlCSAPlike -OE plants exhibited reduced chlorophyll content, increased reactive oxygen species (ROS) accumulation, and enhanced antioxidant enzyme activity, accompanied by ultrastructural degradation of chloroplasts including thylakoid disassembly and starch granule reduction. Transcriptome analysis revealed that SlCSAPlike-mediated senescence does not rely on the transcriptional activation of the canonical senescence program. Further screening and validation demonstrated that SlCSAPlike interacts with phosphoglucomutase (PGM), enhances its enzymatic activity, and promotes the conversion of G1P to G6P, thereby altering the carbon metabolic balance in leaves, which subsequently influences leaf starch content and accelerates senescence progression. This study reveals a novel mechanism by which SlCSAPlike affects chloroplast stability and senescence progression through regulating PGM-mediated starch accumulation, providing new insights into the molecular mechanisms of leaf senescence and offering potential genetic targets for improving tomato yield by delaying senescence.