Abscisic acid controls sugar accumulation essential to strawberry fruit ripening via the FaRIPK1‐FaTCP7‐FaSTP13/FaSPT module

Abstract

SUMMARYStrawberry is considered as a model plant for studying the ripening of abscisic acid (ABA)‐regulated non‐climacteric fruits, a process in which sugar plays a fundamental role, while how ABA regulates sugar accumulation remains unclear. This study provides a direct line of physiological, biochemical, and molecular evidence that ABA signaling regulates sugar accumulation via the FaRIPK1‐FaTCP7‐FaSTP13/FaSPT signaling pathway. Herein, FaRIPK1, a red‐initial protein kinase 1 previously identified in strawberry fruit, not only interacted with the transcription factor FaTCP7 (TEOSINTE BRANCHEN 1, CYCLOIDEA, and PCF) but also phosphorylated the critical Ser89 and Thr93 sites of FaTCP7, which negatively regulated strawberry fruit ripening, as evidenced by the transient overexpression (OE) and virus‐induced gene silencing transgenic system. Furthermore, the DAP‐seq experiments revealed that FvTCP7 bound the motif “GTGGNNCCCNC” in the promoters of two sugar transporter genes, FaSTP13 (sugar transport protein 13) and FaSPT (sugar phosphate/phosphate translocator), inhibiting their transcription activities as determined by the electrophoretic mobility shift assay, yeast one‐hybrid, and dual‐luciferase reporter assays. The downregulated FaSTP13 and FaSPT transcripts in the FaTCP7‐OE fruit resulted in a reduction in soluble sugar content. Consistently, the yeast absorption test revealed that the two transporters had hexose transport activity. Especially, the phosphorylation‐inhibited binding of FaTCP7 to the promoters of FaSTP13 and FaSPT could result in the release of their transcriptional activities. In addition, the phosphomimetic form FaTCP7S89D or FaTCP7T93D could rescue the phenotype of FaTCP7‐OE fruits. Importantly, exogenous ABA treatment enhanced the FaRIPK1–FaTCP7 interaction. Overall, we found direct evidence that ABA signaling controls sugar accumulation during strawberry fruit ripening via the “FaRIPK1‐FaTCP7‐FaSTP13/FaSPT” module.