CsCPC, an R3‐MYB transcription factor, acts as a negative regulator of citric acid accumulation in Citrus

• Published in: The Plant journal : for cell and molecular biology Vol. 121; no. 1; pp. e17189 - n/a
• Main Authors: Wang, Ting‐Ting, Song, Xin, Zhang, Miao, Fan, Yan‐Jie, Ren, Jie, Duan, Yao‐Yuan, Guan, Shu‐ping, Luo, Xin, Yang, Wen‐Hui, Cao, Hui‐Xiang, Wu, Xiao‐Meng, Guo, Wen‐Wu, Xie, Kai‐Dong
• Format: Journal Article
• Language: English
• Published: England Blackwell Publishing Ltd 01.01.2025
• Subjects: Accumulation; Acids; Callus; Citric acid; Citric Acid - metabolism; Citrus; Citrus - genetics; Citrus - metabolism; Citrus fruits; Feedback loops; Fruit - genetics; Fruit - growth & development; Fruit - metabolism; fruit quality; Fruits; Gene Expression Regulation, Plant; genetically modified organisms; Germplasm; Hybrids; kumquats; lemons; Molecular modelling; Organic acids; Plant Proteins - genetics; Plant Proteins - metabolism; Plants, Genetically Modified; R3‐MYB transcription factor; Regulatory mechanisms (biology); Ripening; RNA-mediated interference; Transcription factors; Transcription Factors - genetics; Transcription Factors - metabolism; Transcriptomes; transcriptomics; triploid hybrids; triploidy; vacuoles; Citrus; citric acid; triploid hybrids; R3‐MYB transcription factor
• ISSN: 0960-7412; 1365-313X; 1365-313X
• DOI: 10.1111/tpj.17189

SUMMARY The citric acid accumulation during fruit ripening determines the quality of fleshy fruits. However, the molecular mechanism underlying citric acid accumulation is not clearly understood yet in citrus due to the scarcity of paired germplasm that exhibits significant difference in organic acid accumulation. Two citrus triploid hybrids with distinct citric acid content in their mature fruits were herein identified from a previously conducted interploidy cross in our group, providing an ideal paired material for studying acid accumulation in citrus. Through a comparative transcriptome analysis of the pulps of the above two triploid hybrids, an R3‐MYB transcription factor, CAPRICE (CsCPC), was identified to be a regulator of citric acid accumulation in citrus fruits. Through transgenic experiments involving overexpression (in callus and kumquat fruits) and RNAi (in lemon leaves), we demonstrated that CsCPC suppresses citric acid accumulation by negatively regulating the expression of CsPH1 and CsPH5. Moreover, CsCPC competed with an R2R3‐MYB CsPH4 for binding to ANTHOCYANIN1 (CsAN1) and thus disturbed the activation of CsPH1 and CsPH5 that encode vacuolar P‐ATPase, which eventually led to a decrease in citric acid content. CsPH4 activated the expression of CsCPC and thus formed an activator–repressor feedback loop, which ultimately inhibited citric acid accumulation in citrus fruit. In summary, this study reveals a new regulatory mechanism of CsCPC‐mediated inhibition of citric acid accumulation in citrus fruits, which would support the improvement of citrus fruit quality. Significance Statement This study uncovers a complex regulatory loop controlling citric acid levels in citrus fruit, where two proteins, CsCPC and CsPH4, coordinate the accumulation of citric acid. These findings provide a deeper understanding of the genetic mechanisms behind fruit acidity, which could help improve citrus quality in agricultural breeding.