N-hydroxy-pipecolic acid (NHP) activates plant systemic acquired resistance (SAR). Enhanced defense responses are typically accompanied by deficiency in plant development and reproduction. Despite of extensive studies on SAR induction, the effects of NHP metabolism on plant growth remain largely unclear. In this study, we discovered that NHP glycosylation is a critical factor that fine-tunes the tradeoff between SAR defense and plant growth. We demonstrated that a UDP-glycosyltransferase (UGT76B1) forming NHP glycoside (NHPG) controls the NHP to NHPG ratio. Consistently, the ugt76b1 mutant exhibits enhanced SAR response and an inhibitory effect on plant growth, while UGT76B1 overexpression attenuates SAR response, promotes growth, and delays senescence, indicating that NHP levels are dependent on UGT76B1 function in the course of SAR. Furthermore, our results suggested that, upon pathogen attack, UGT76B1-mediated NHP glycosylation forms a “hand brake” on NHP accumulation by attenuating the positive regulation of NHP biosynthetic pathway genes, highlighting the complexity of SAR-associated networks. In addition, we showed that UGT76B1-mediated NHP glycosylation in the local site is important for fine-tuning SAR response. Our results implicate that engineering plant immunity through manipulating the NHP/NHPG ratio is a promising method to balance growth and defense response in crops.

N-羟基-哌啶酸 (NHP) 激活植物系统获得性抗性 (SAR)。增强的防御反应通常伴随着植物发育和繁殖的缺陷。尽管对 SAR 诱导进行了广泛的研究，但 NHP 代谢对植物生长的影响在很大程度上仍不清楚。在这项研究中，我们发现 NHP 糖基化是微调 SAR 防御和植物生长之间权衡的关键因素。我们证明了形成 NHP 糖苷 (NHPG) 的 UDP-糖基转移酶 (UGT76B1) 控制 NHP 与 NHPG 的比率。一致地，ugt76b1突变体表现出增强的 SAR 响应和对植物生长的抑制作用，而UGT76B1过表达减弱 SAR 反应、促进生长和延缓衰老，表明 NHP 水平在 SAR 过程中依赖于 UGT76B1 功能。此外，我们的结果表明，在病原体攻击时，UGT76B1 介导的 NHP 糖基化通过减弱 NHP 生物合成途径基因的正调控，对 NHP 积累形成“手刹”，突出了 SAR 相关网络的复杂性。此外，我们发现 UGT76B1 介导的局部位点 NHP 糖基化对于微调 SAR 反应很重要。我们的结果表明，通过操纵 NHP/NHPG 比率来改造植物免疫是平衡作物生长和防御反应的一种很有前途的方法。