The potato cyst nematode effector RHA1B is a ubiquitin ligase and uses two distinct mechanisms to suppress plant immune signaling.

Joanna Kud,Wenjie Wang,Yongsheng Liu,Louise-Marie Dandurand,Li Huang,Amanda Gray,Aska Goverse,Yulin Yuan,Youhong Fan,Allan Caplan,Aida Duarte,Joseph C Kuhl,Rachel Gross,Fangming Xiao

doi:10.1371/journal.ppat.1007720

Abstract

Plant pathogens, such as bacteria, fungi, oomycetes and nematodes, rely on wide range of virulent effectors delivered into host cells to suppress plant immunity. Although phytobacterial effectors have been intensively investigated, little is known about the function of effectors of plant-parasitic nematodes, such as Globodera pallida, a cyst nematode responsible for vast losses in the potato and tomato industries. Here, we demonstrate using in vivo and in vitro ubiquitination assays the potato cyst nematode (Globodera pallida) effector RHA1B is an E3 ubiquitin ligase that employs multiple host plant E2 ubiquitin conjugation enzymes to catalyze ubiquitination. RHA1B was able to suppress effector-triggered immunity (ETI), as manifested by suppression of hypersensitive response (HR) mediated by a broad range of nucleotide-binding leucine-rich repeat (NB-LRR) immune receptors, presumably via E3-dependent degradation of the NB-LRR receptors. RHA1B also blocked the flg22-triggered expression of Acre31 and WRKY22, marker genes of pathogen‐associated molecular pattern (PAMP)‐triggered immunity (PTI), but this did not require the E3 activity of RHA1B. Moreover, transgenic potato overexpressing the RHA1B transgene exhibited enhanced susceptibility to G. pallida. Thus, our data suggest RHA1B facilitates nematode parasitism not only by triggering degradation of NB-LRR immune receptors to block ETI signaling but also by suppressing PTI signaling via an as yet unknown E3-independent mechanism.

Highlights

Globodera pallida, a plant-parasitic cyst nematode, is a global threat to agronomically important crops such as potato and tomato
We report identification of a novel G. pallida effector RHA1B as an E3 ubiquitin ligase, which is responsible for ubiquitin-proteasome-mediated protein degradation in general
We found that RHA1B can suppress plant defense signaling via both E3-dependent and -independent manners

Summary

Introduction

A plant-parasitic cyst nematode, is a global threat to agronomically important crops such as potato and tomato This sedentary plant endoparasite penetrates plant root systems to reach the inner cortex where it establishes a permanent feeding site, a multi-nucleate structure termed syncytium [1]. The first layer of plant defense is governed by membrane-associated pattern recognition receptors (PRRs) that recognize pathogen associated molecular patterns (PAMPs) and/or endogenous damage-associated molecular patterns (DAMPs). This is termed PAMP-triggered immunity (PTI) and, to overcome PTI in host plants, pathogens use the secreted effectors to suppress PTI [2]. CEP12, in turn, interferes with PTI signaling, as manifested by blockage of flg22-induced ROS production and PTI marker gene expression [7], and disruption of ETI signaling, as shown by suppression of HR mediated by the NB-LRR receptor Gpa2 [6]

Methods

Results

Discussion

Conclusion