Coat proteins of necroviruses target 14-3-3a to subvert MAPKKK\u03b1-mediated antiviral immunity in plants

Zongyu Gao,Qianshen Zhang,Savithramma P Dinesh-Kumar,Xiaoling Wang,Dawei Li,Yongliang Zhang,Dingliang Zhang,Zhiyan Wen,Xin Zhang

doi:10.1038/s41467-022-28395-5

Zongyu Gao, Qianshen Zhang + Show 7 more

Open Access

https://doi.org/10.1038/s41467-022-28395-5

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Abstract

Mitogen-activated protein kinase (MAPK) cascades play an important role in innate immunity against various pathogens in plants and animals. However, we know very little about the importance of MAPK cascades in plant defense against viral pathogens. Here, we used a positive-strand RNA necrovirus, beet black scorch virus (BBSV), as a model to investigate the relationship between MAPK signaling and virus infection. Our findings showed that BBSV infection activates MAPK signaling, whereas viral coat protein (CP) counteracts MAPKKKα-mediated antiviral defense. CP does not directly target MAPKKKα, instead it competitively interferes with the binding of 14-3-3a to MAPKKKα in a dose-dependent manner. This results in the instability of MAPKKKα and subversion of MAPKKKα-mediated antiviral defense. Considering the conservation of 14-3-3-binding sites in the CPs of diverse plant viruses, we provide evidence that 14-3-3-MAPKKKα defense signaling module is a target of viral effectors in the ongoing arms race of defense and viral counter-defense.

Highlights

Mitogen-activated protein kinase (MAPK) cascades play an important role in innate immunity against various pathogens in plants and animals
We demonstrate that MAPKKKα-mediated defense against beet black scorch virus (BBSV) infection in N. benthamiana is correlated with the expression of a series of defense-related genes such as PROTEIN 1A (PR1A), ETHYLENERESPONSIVE TRANSCRIPTION FACTOR 1B (ERF1B), and HYPERSENSITIVE-INDUCED RESPONSE PROTEIN 1 (HIR1), whereas viral coat protein (CP) can subvert MAPKKKαmediated antiviral innate immune response by targeting 14-3-3a
We knocked down the expression of MAPKKKα by using intron spliced hairpin RNAi vector-mediated gene silencing[38], and observed increased GFP fluorescence and CP accumulation in MAPKKKα-RNAi leaves compared with the empty vector (EV) control (Fig. 1b, c)

Summary

Introduction

Mitogen-activated protein kinase (MAPK) cascades play an important role in innate immunity against various pathogens in plants and animals. CP does not directly target MAPKKKα, instead it competitively interferes with the binding of 14-3-3a to MAPKKKα in a dose-dependent manner This results in the instability of MAPKKKα and subversion of MAPKKKα-mediated antiviral defense. Microbe-associated molecular patterns (PAMPs/MAMPs), triggering a series of downstream defense responses, including calcium flux, production of reactive oxygen species (ROS), activation of mitogen-activated protein kinase (MAPK) cascades and upregulation of defense genes. This perception of PAMPs/ MAMPs constitutes the first layer of plant protection against pathogen attack and is referred to as pattern-triggered immunity (PTI)[2,3]. Over the past decade, a growing body of evidence suggests that plants deploy PTI to limit virus infection

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