SlJRE4-SlTPP1 confers carbon starvation tolerance by inhibiting starch degradation in tomato leaves at night

Abstract Under carbon starvation, plants have evolved a precise regulatory network governing starch degradation rates to avert excessive depletion of starch reserves, thereby sustaining carbon homeostasis and prolonging survival. We previously found that overexpression of the trehalose-6-phosphate phosphatase gene SlTPP1 slows nocturnal starch degradation in tomato leaves under neutral-day conditions; however, its function and regulatory mechanism underlying leaf starch degradation under low light (LL)-induced carbon starvation remain elusive. Here, we demonstrate that SlTPP1 slows nocturnal starch degradation in tomato leaves under carbon starvation. SlTPP1 overexpression suppresses nocturnal starch degradation and inhibits β-amylase activity in tomato leaves under neutral-day, short-day, and LL conditions. LL induces the expression of starch-degrading enzyme genes while concurrently upregulating SlTPP1 transcription in leaves. Furthermore, the jasmonic acid (JA)-responsive ERF transcription factor SlJRE4 directly binds to the GCC-box cis-element in the SlTPP1 promoter and activates its expression. SlJRE4 transcription is also induced by LL. SlJRE4 overexpression similarly slows nocturnal starch degradation and represses β-amylase activity in leaves under neutral-day, short-day, and LL conditions. Additionally, exogenous methyl jasmonate under LL inhibits leaf starch degradation and upregulates the expression of SlJRE4 and SlTPP1. LL upregulates the expression of JA biosynthesis genes and elevates JA levels in tomato leaves. Moreover, SlTPP1 overexpression indirectly enhances SlJRE4 expression in leaves. Collectively, our findings uncover that the SlJRE4–SlTPP1 module acts as a braking mechanism to attenuate the rapid starch degradation in leaves triggered by LL-induced carbon starvation, representing a critical adaptive strategy for plants to improve survival under carbon starvation stress.