CsAPRR2 regulates cucumber immature fruit color by coordinating chloroplast biogenesis and photosynthesis-related gene expression

Immature fruit color (IFC) of cucumber (Cucumis sativus L.) is an important marketability trait affecting consumer preferences. We previously identified a single-base insertion (−/G) in CsAPRR2 that introduces a premature stop codon, leading to loss of the conserved C-terminal GCT box that is essential for protein–protein interactions. This mutation is strongly associated with reduced CsAPRR2 expression and white IFC. RNA interference (RNAi) and transgenic overexpression confirmed the critical role of CsAPRR2 in regulating IFC. Chromatin immunoprecipitation sequencing analysis and transcriptome profiling identified 225 candidate targets of CsAPRR2, many of which encode thylakoid membrane proteins or key enzymes in chlorophyll biosynthesis. Knockdown of CsAPRR2 expression in RNAi plants significantly reduced the expression of these genes, resulting in impaired thylakoid development, lower chloroplast numbers, and reduced pigment content. CsAPRR2 physically interacts with transcription factors CsTCP15 and CsTCP20B in a GCT box–dependent manner, supporting a model in which these interactions contribute to CsAPRR2-mediated regulation of chloroplast development. Notably, a CsTCP20B variant identified in a wild cucumber with light green immature skin and white mature skin supports its involvement in skin color regulation. Together, this work establishes CsAPRR2 as a central regulator of chloroplast biogenesis and immature fruit pigmentation in cucumber and underscores the importance of transcription factor interactions in modulating photosynthesis-related gene expression.