CsbZIP1-CsMYB12 mediates the production of bitter-tasting flavonols in tea plants (Camellia sinensis) through a coordinated activator\u2013repressor network

Xuecheng Zhao,Shuwei Yu,Jian Zhao,Xiangsheng Zeng,Alisdair R Fernie,Ning Lin

doi:10.1038/s41438-021-00545-8

Abstract

Under high light conditions or UV radiation, tea plant leaves produce more flavonols, which contribute to the bitter taste of tea; however, neither the flavonol biosynthesis pathways nor the regulation of their production are well understood. Intriguingly, tea leaf flavonols are enhanced by UV-B but reduced by shading treatment. CsFLS, CsUGT78A14, CsMYB12, and CsbZIP1 were upregulated by UV-B radiation and downregulated by shading. CsMYB12 and CsbZIP1 bound to the promoters of CsFLS and CsUGT78A14, respectively, and activated their expression individually. CsbZIP1 positively regulated CsMYB12 and interacted with CsMYB12, which specifically activated flavonol biosynthesis. Meanwhile, CsPIF3 and two MYB repressor genes, CsMYB4 and CsMYB7, displayed expression patterns opposite to that of CsMYB12. CsMYB4 and CsMYB7 bound to CsFLS and CsUGT78A14 and repressed their CsMYB12-activated expression. While CsbZIP1 and CsMYB12 regulated neither CsMYB4 nor CsMYB7, CsMYB12 interacted with CsbZIP1, CsMYB4, and CsMYB7, but CsbZIP1 did not physically interact with CsMYB4 or CsMYB7. Finally, CsPIF3 bound to and activated CsMYB7 under shading to repress flavonol biosynthesis. These combined results suggest that UV activation and shading repression of flavonol biosynthesis in tea leaves are coordinated through a complex network involving CsbZIP1 and CsPIF3 as positive MYB activators and negative MYB repressors, respectively. The study thus provides insight into the regulatory mechanism underlying the production of bitter-tasting flavonols in tea plants.

Highlights

Tea plants (Camellia sinensis) synthesize diverse flavonoids, such as catechins, flavonols, and anthocyanins and their derivatives, at significant levels in tender tissues, such as apical buds and young leaves
To understand the molecular regulatory mechanisms underlying the regulation of flavonol synthesis by light exposure, we conducted both UV-B radiation and shading treatment experiments on tea plant seedlings hydroponically grown in SK nutrient solution and on tea plants grown in tea gardens
Two structural genes and a MYB transcription factors (TFs) (Fig. 1d) of the flavonol biosynthetic pathway, namely, CsFLS, CsUGT78A14, and CsMYB12, were revealed by Quantitative real-time PCR (qRT-PCR) analysis to be significantly activated by UV-B radiation (Fig. 1c, e)

Summary

Introduction

Tea plants (Camellia sinensis) synthesize diverse flavonoids, such as catechins, flavonols, and anthocyanins and their derivatives, at significant levels in tender tissues, such as apical buds and young leaves. These flavonoids, together with caffeine and theanine, constitute the major bioactive secondary metabolites in teas, contributing to their pleasant flavors, rich tastes, and multiple health benefits, features that are of vast importance given that tea is the most consumed nonalcohol beverage in the world[1,2,3].

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Conclusion