<scp>JA</scp> Regulates Caffeine Biosynthesis in Tea Leaf for Resistance Against Fungal Infection and Antagonises With <scp>GA</scp> to Balance the Defence–Growth Trade‐Off via <scp>CsDELLA</scp> ‐ <scp>JAZ</scp> ‐ <scp>MYC2</scp> ‐ <scp>MYB184</scp> ‐ <scp>TCS1</scp> Module
Zhili Ye, Ziqing Zheng, Jinsong Wang, Qinyu Zhong, Xiaoyu Mu, Zhoufang Yuan, Yin Huang, Zainab Ghazala, Hao Zuo, Yaling Li, Xiaoyu Liang, Yuchen Qi, Xiongyuan Si, Yanrui Zhang, Enhua Xia, Jian Zhao, Penghui Li
Abstract
Caffeine is a defensive alkaloid primarily accumulated in tea leaves to defend against pathogens. But the regulatory mechanism for caffeine biosynthesis in response to fungal infection and the trade-off between specialised metabolite and plant growth remain elusive. Here, we report that jasmonic acid (JA)-regulated CsMYB184 is the key for caffeine biosynthesis in tea leaves. Exogenous MeJA promoted caffeine biosynthesis in tea leaves and enhanced the resistance against fungal pathogens. JASMONATE ZIM-domain proteins (JAZs) interacted with CsMYB184 to repress CsMYB184 transactivation of TCS1. Meanwhile, JA effector CsMYC2 directly bound to and activated CsMYB184 transcription, but inhibited plant growth by directly modulating GA inactivation through gibberellin 2-oxidase 4 (CsGA2ox4). By contrast, gibberellins (GA) stimulated tea plant growth and inhibited caffeine biosynthesis, rendering tea plants more susceptible to fungal pathogens, via competitive DELLA proteins interacting with JAZs to relieve JAZ inhibition of CsMYB184. CsDELLA-JAZ-MYC2-MYB184-TCS1 formed an activation-repression loop to regulate developmental and hormonal control of caffeine biosynthesis in response to fungal pathogens, which balance the tea plant growth and defence response trade-offs. The study reveals JA-GA antagonistic regulation of caffeine biosynthesis as one of the innate immunity defences, meanwhile balancing the growth and defence of tea plants via crosstalk between JA and GA signalling.