Triptychon-like regulates aspects of both fruit flavor and color in citrus

Authors: HE, JIAXIAN - Huazhong Agricultural University; XU, YUANTAO - Huazhong Agricultural University; HUANG, DING - Huazhong Agricultural University; FU, JIALING - Huazhong Agricultural University; LIU, ZHANG - Huazhong Agricultural University; WANG, LUN - Huazhong Agricultural University; ZHANG, YIN - Huazhong Agricultural University; XU, RANGWEI - Huazhong Agricultural University; Li, Li; DENG, XIUXIN - Huazhong Agricultural University; XU, QIANG - Huazhong Agricultural University

Submitted to: Journal of Experimental Botany
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/18/2022
Publication Date: 3/9/2022
Citation: He, J., Xu, Y., Huang, D., Fu, J., Liu, Z., Wang, L., Zhang, Y., Xu, R., Li, L., Deng, X., Xu, Q. 2022. Triptychon-like regulates aspects of both fruit flavor and color in citrus. Journal of Experimental Botany. 73(11):3610-3624. https://doi.org/10.1093/jxb/erac069.
DOI: https://doi.org/10.1093/jxb/erac069

Interpretive Summary: Understanding the genetic basis underlying some metabolite accumulation is critical for improving fruit quality. This work reveals a citrus gene (CiTRL) acts as a negative regulator to simultaneously control citric acid, proanthocyanidin, and anthocyanin content in citrus fruits via a cross-regulation machinery. The findings provide an opportunity to efficiently manipulate these key traits as a means to produce citrus fruits that are both visually appealing and delicious taste.

Technical Abstract: Deciphering the genetic basis of organoleptic traits is critical for improving the quality of fruits, which greatly shapes their appeal to consumers. Here, we characterize the citrus R3-MYB transcription factor TRIPTYCHON-LIKE (CitTRL), which is closely associated with the levels of citric acid, proanthocyanidins (PAs), and anthocyanins. Overexpression of CitTRL lowered acidity levels and PA contents in citrus calli as well as anthocyanin and PA contents in Arabidopsis leaves and seeds. CitTRL interacts with the two basic helix–loop–helix (bHLH) proteins CitbHLH1 and ANTHOCYANIN 1 (CitAN1) to regulate fruit quality. We show that CitTRL competes with the R2R3-MYB CitRuby1 for binding to CitbHLH1 or CitAN1, thereby repressing their activation of anthocyanin structural genes. CitTRL also competes with a second R2R3-MYB, CitPH4, for binding to CitAN1, thus altering the expression of the vacuolar proton- pump gene PH5 and Leucoanthocyanidin reductase, responsible for vacuolar acidification and proanthocyanidins biosynthesis, respectively. Moreover, CitPH4 activates CitTRL transcription, thus forming an activator–repressor loop to prevent the overaccumulation of citric acid and PAs. Overall, this study demonstrates that CitTRL acts as a repressor of the accumulation of citric acid, PAs, and anthocyanins by a cross-regulation mechanism. Our results provide an opportunity to simultaneously manipulate these key traits as a means to produce citrus fruits that are both visually and organoleptically appealing.