βC1 protein encoded in geminivirus satellite concertedly targets MKK2 and MPK4 to counter host defense.

Tao Hu,Changjun Huang,Yuting He,Xiuren Zhang,Xueping Zhou,Claudia Castillo-González,Xiaojian Gui,Yaqin Wang,Savithramma P Dinesh-Kumar

doi:10.1371/journal.ppat.1007728

Abstract

Plant viruses have evolved multiple strategies to overcome host defense to establish an infection. Here, we identified two components of a host mitogen-activated protein kinase (MAPK) cascade, MKK2 and MPK4, as bona fide targets of the βC1 protein encoded by the betasatellite of tomato yellow leaf curl China virus (TYLCCNV). βC1 interacts with the kinase domain of MKK2 and inhibits its activity. In vivo, βC1 suppresses flagellin-induced MAPK activation and downstream responses by targeting MKK2. Furthermore, βC1 also interacts with MPK4 and inhibits its kinase activity. TYLCCNV infection induces the activation of the MAPK cascade, mutation in MKK2 or MPK4 renders the plant more susceptible to TYLCCNV, and can complement the lack of βC1. This work shows for the first time that a plant virus both activates and suppresses a MAPK cascade, and the discovery of the ability of βC1 to selectively interfere with the host MAPK activation illustrates a novel virulence function and counter-host defense mechanism of geminiviruses.

Highlights

Plants have evolved multiple layers of effective strategies to defend themselves from invading pathogens [1]
We identified a plant Mitogen-Activated Protein Kinases (MAPK) cascade that contributes to the defense against geminiviruses
The βC1 protein of geminivirus betasatellite interacts with mitogen-activated protein kinase kinase 2 (MKK2) and mitogen-activated protein kinase 4 (MPK4) and inhibits their kinase activity

Summary

Introduction

Plants have evolved multiple layers of effective strategies to defend themselves from invading pathogens [1]. The first layer of immune response depends on the recognition of pathogen- or microbe-associated molecular patterns (PAMPs or MAMPs) by cell membrane-associated pattern recognition receptors (PRRs). Multiple PTI readouts are produced downstream of PRR activation, including activation of cascades of Mitogen-Activated Protein Kinases (MAPK) and the subsequent up-regulation of defense gene expression. The second layer of immune response is triggered by the recognition of pathogen effectors in a direct or indirect manner, and is called effector triggered immunity (ETI) [1]. In Arabidopsis thaliana, MAPK cascades can be rapidly activated by the recognition of PAMPs/MAMPs by their cognate PRRs, as has been demonstrated for bacterial flagellin, bacterial EF-Tu, or fungal chitin [6,7,8], and at least one bacterial effector, namely AvrRpt, has been shown to strongly activate two of the Arabidopsis MAPKs, AtMPK3 and AtMPK6 [9]

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Discussion

Conclusion