Leaf senescence, the final stage of leaf development, is influenced by numerous internal and environmental signals. However, how biotic stresses such as pathogen infection regulate leaf senescence remains largely unclear. In this study, we found that the premature leaf senescence in Arabidopsis caused by the soil-borne vascular fungus Verticillium dahliae was impaired by disruption of a protein elicitor from V. dahliae 1 named PevD1. Constitutive or inducible overexpression of PevD1 accelerated Arabidopsis leaf senescence. Interestingly, a senescence-associated NAC transcription factor, ORE1, was targeted by PevD1. PevD1 could interact with and stabilize ORE1 protein by disrupting its interaction with the RING-type ubiquitin E3 ligase NLA. Mutation of ORE1 suppressed the premature senescence caused by overexpressing PevD1, whereas overexpression of ORE1 or PevD1 led to enhanced ethylene production and thereby leaf senescence. We showed that ORE1 directly binds the promoter of ACS6 and promotes its expression for mediating PevD1-induced ethylene biosynthesis. Loss-of-function of ACSs could suppress V. dahliae–induced leaf senescence in ORE1-overexpressing plants. Furthermore, we found thatPevD1 also interacts with Gossypium hirsutum ORE1 (GhORE1) and that virus-induced gene silencing of GhORE1 delays V. dahliae–triggered leaf senescence in cotton, indicating a possibly conserved mechanism in plants. Taken together, these results suggest that V. dahliae induces leaf senescence by secreting the effector PevD1 to manipulate the ORE1-ACS6 cascade, providing new insights into biotic stress-induced senescence in plants.

叶片衰老是叶片发育的最后阶段，受许多内部和环境信号的影响。然而，病原体感染等生物胁迫如何调节叶片衰老仍不清楚。在这项研究中，我们发现由土壤传播的维管菌大丽轮枝菌引起的拟南芥叶片过早衰老受到了来自大丽花1 名为 PevD1的蛋白质诱导子的破坏。PevD1加速拟南芥的组成型或诱导型过表达叶衰老。有趣的是，与衰老相关的 NAC 转录因子 ORE1 被 PevD1 靶向。PevD1 可以通过破坏其与环型泛素 E3 连接酶 NLA 的相互作用来与 ORE1 蛋白相互作用并使其稳定。ORE1的突变抑制了由过表达PevD1引起的过早衰老，而ORE1或PevD1的过表达导致乙烯产量增加，从而导致叶片衰老。我们发现 ORE1 直接结合ACS6的启动子并促进其表达以介导 PevD1 诱导的乙烯生物合成。ACSs的功能丧失可以抑制 V. dahliae诱导的ORE1-叶片衰老过度表达植物。此外，我们发现 PevD1 还与Gossypium hirsutum ORE1 (GhORE1) 相互作用，并且病毒诱导的GhORE1基因沉默延迟了V. dahliae引发的棉花叶片衰老，这表明植物中可能存在保守机制。总之，这些结果表明大丽花通过分泌效应子 PevD1 来操纵 ORE1-ACS6 级联来诱导叶片衰老，从而为生物胁迫诱导的植物衰老提供新的见解。