Sugar starvation activates the OsSnRK1a-OsbHLH111/OsSGI1-OsTPP7 module to mediate growth inhibition of rice

Sugar deficiency is the persistent challenge for plants during development. Trehalose-6-phosphate (T6P) is recognized as a key regulator in balancing plant sugar homeostasis. However, the underlying mechanisms by which sugar starvation limits plant development are unclear. Here, a basic helix-loop-helix (bHLH) transcription factor (OsbHLH111) was named starvation-associated growth inhibitor 1 (OsSGI1) and the focus is on the sugar shortage of rice. The transcript and protein levels of OsSGI1 were markedly increased during sugar starvation. The knockout mutants sgi1-1/2/3 exhibited increased grain size and promoted seed germination and vegetative growth, which were opposite to those of overexpression lines. The direct binding of OsSGI1 to sucrose non-fermenting-1 (SNF1)-related protein kinase 1a (OsSnRK1a) was enhanced during sugar shortage. Subsequently, OsSnRK1a-dependent phosphorylation of OsSGI1 enhanced the direct binding to the E-box of trehalose 6-phosphate phosphatase 7 (OsTPP7) promoter, thus rose the transcription inhibition on OsTPP7, then elevated trehalose 6-phosphate (Tre6P) content but decreased sucrose content. Meanwhile, OsSnRK1a degraded phosphorylated-OsSGI1 by proteasome pathway to prevent the cumulative toxicity of OsSGI1. Overall, we established the OsSGI1-OsTPP7-Tre6P loop with OsSnRK1a as center and OsSGI1 as forward, which is activated by sugar starvation to regulate sugar homeostasis and thus inhibits rice growth.