Two Phytophthora effectors mitigate plant immunity by manipulating intracellular pH through interaction with V-ATPase in potato.

Abstract

Plant V-ATPase serves as a primary active proton pump of the endomembrane system and is crucial for the stress response. However, the role of the C subunit of V-ATPase (VHA-C) in effector-triggered immunity remains poorly understood. Here, we reveal that Phytophthora infestans evolved a pair of RxLR effectors, AL3 and Avr2, which are expressed sequentially and both target the host VHA-C (StATP6V1C1) and StBSL1. In the early stage of P. infestans infection, AL3 promotes the assembly of StATP6V1C1 with subunits G and E, leading to increased V-ATPase activity and cytoplasmic acidification. Subsequently, Avr2 inhibits the StWNK10-catalyzed Ser-261 phosphorylation of StATP6V1C1, thereby retarding V-ATPase activity and causing intracellular alkalinization. In cultivars absence of two immune receptors, this pH shift facilitates the interactions of the two effectors with downstream susceptibility factors of StBSL1 at various stages of infection, which may promote the onset and development of the disease. As coping strategy, plants independently evolve two NLRs, R2 and Rpi-mcq1, guard both StATP6V1C1 and StBSLs to perceive effectors thereby mitigating the risk of late blight. Our findings establish a new arms race battlefield between plants and oomycetes, highlighting the role of intracellular pH homeostasis in both effector-triggered susceptibility (ETS) and effector-triggered immunity (ETI).