ClSnRK2.3 negatively regulates watermelon fruit ripening and sugar accumulation

Abstract

Watermelon (Citrullus lanatus) as non‐climacteric fruit is domesticated from the ancestors with inedible fruits. We previously revealed that the abscisic acid (ABA) signaling pathway gene ClSnRK2.3 might influence watermelon fruit ripening. However, the molecular mechanisms are unclear. Here, we found that the selective variation of ClSnRK2.3 resulted in lower promoter activity and gene expression level in cultivated watermelons than ancestors, which indicated ClSnRK2.3 might be a negative regulator in fruit ripening. Overexpression (OE) of ClSnRK2.3 significantly delayed watermelon fruit ripening and suppressed the accumulation of sucrose, ABA and gibberellin GA4. Furthermore, we determined that the pyrophosphate‐dependent phosphofructokinase (ClPFP1) in sugar metabolism pathway and GA biosynthesis enzyme GA20 oxidase (ClGA20ox) could be phosphorylated by ClSnRK2.3 and thereby resulting in accelerated protein degradation in OE lines and finally led to low levels of sucrose and GA4. Besides that, ClSnRK2.3 phosphorylated homeodomain‐leucine zipper protein (ClHAT1) and protected it from degradation to suppress the expression of the ABA biosynthesis gene 9’‐cis‐epoxycarotenoid dioxygenase 3 (ClNCED3). These results indicated that ClSnRK2.3 negatively regulated watermelon fruit ripening by manipulating the biosynthesis of sucrose, ABA and GA4. Altogether, these findings revealed a novel regulatory mechanism in non‐climacteric fruit development and ripening.

Sucrose promotes cone enlargement via the TgNGA1‐TgWRKY47‐TgEXPA2 module in Torreya grandis

“…Sucrose is recognized for its critical roles in providing carbon skeletons and energy during the enlargement of plant reproductive organs (Fan et al ., 2021; Ko et al ., 2021). In addition, sucrose may modulate a wide range of metabolic processes and gene expression, thus functioning in fruit enlargement in angiosperms (Chen et al ., 2022; Wang et al ., 2023). The changes in sucrose and hexose levels in fruits are closely related to the sizes of sink organs in angiosperms (Li et al ., 2020).…”

Abscisic acid biosynthesis, metabolism and signaling in ripening fruit

“…Contrarily, the transcription of FaABI1 encoding PP2Cs decreases rapidly during strawberry fruit ripening; The silencing of this gene affects the transcripts of many ABA-responsive genes, and accelerates ripening process, which confirmed its negative role in ABA signaling ( Jia et al., 2013 ). Recently, ClSnRK2.3 has been found to directly phosphorylate the pyrophosphate-dependent phosphofructokinase ClPFP1, which is involved in sugar metabolism pathway, to accelerate its degradation and this process finally results in low sucrose content in watermelon fruit ( Wang et al., 2023 ), indicating that ABA signaling may be transmitted without AREB/ABFs and the intermediate components such as PP2Cs and SnRK2 may directly regulate target genes related to fruit ripening. However, extensive studies have revealed that ABA signals are mainly transmitted to downstream target genes through AREB/ABFs.…”

“…Moreover, gibberellic acid (GA) can activate the removal of ABA through FveCYP707A4a-induced metabolism, indicating that down-regulation of GA may result in ABA accumulation and promote fruit ripening ( Liao et al., 2018 ). However, ABA signaling component ClSnRK2.3 phosphorylates GA biosynthesis enzyme ClGA20ox to accelerate its degradation, which results in low GA level and negatively regulates watermelon fruit ripening ( Wang et al., 2023 ).…”