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Review
. 2019 Sep;20(9):1211-1216.
doi: 10.1111/mpp.12852. Epub 2019 Aug 9.

Autophagy-virus interplay in plants: from antiviral recognition to proviral manipulation

Nirbhay Kumar Kushwaha  1 , Anders Hafrén  1 , Daniel Hofius  1
Affiliations
Review

Autophagy-virus interplay in plants: from antiviral recognition to proviral manipulation

Nirbhay Kumar Kushwaha et al. Mol Plant Pathol. 2019 Sep.

Abstract

Autophagy is a conserved self-cleaning and renewal system required for cellular homeostasis and stress tolerance. Autophagic processes are also implicated in the response to 'non-self' such as viral pathogens, yet the functions and mechanisms of autophagy during plant virus infection have only recently started to be revealed. Compelling evidence now indicates that autophagy is an integral part of antiviral immunity in plants. It can promote the hypersensitive cell death response upon incompatible viral infections or mediate the selective elimination of entire particles and individual proteins from compatible viruses in a pathway similar to xenophagy in animals. Several viruses, however, have evolved measures to antagonize xenophagic degradation or utilize autophagy to suppress disease-associated cell death and other defence pathways like RNA silencing. Here, we highlight the current advances and gaps in our understanding of the complex autophagy-virus interplay and its consequences for host immunity and viral pathogenesis in plants.

Keywords: ATG8; autophagy; innate immunity; plants; selective cargo receptor; virus; xenophagy.

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Figures

Figure 1
Figure 1
Anti‐ and proviral roles of autophagy in plants. Autophagy has emerged as a central component of antiviral immunity. During infection with an avirulent strain of Tobacco mosaic virus (TMV), autophagy is activated upon N gene‐mediated recognition of the viral p50 protein and contributes to the hypersensitive response (HR). The mechanistic details and autophagic targets underlying the death‐promoting activity of autophagy in effector‐triggered immunity are still unknown. During virulent virus infection, selective autophagy employs the cargo receptor NBR1 to mediate the degradation of non‐assembled capsid protein (P4) and particles of Cauliflower mosaic virus (CaMV). CaMV evades xenophagy by sequestering P4 and particles in autophagy‐resistant inclusions formed by the viral protein P6. NBR1 targets the RNA silencing suppressor HCpro of Turnip mosaic virus (TuMV) in association with potyvirus‐induced RNA granules, but the viral proteins VPg and to a lesser extent 6K2 are able to block NBR1 flux by as yet unknown mechanisms. NBR1 targeting of viral proteins occurs in an ubiquitin‐dependent (TuMV HCpro) or ‐independent manner (CaMV P4). The RNA‐dependent RNA polymerase (RdRp) of TuMV is inhibited via direct interaction with ATG6/Beclin1, which is proposed to act as cargo receptor for RdRp degradation. Other viral proteins subjected to autophagic destruction include the Cucumber mosaic virus (CMV) silencing suppressor 2b, potentially involving the host protein rgs‐CaM, and the virulence factor βC1 of Cotton leaf curl Multan virus (CLCuMuV) through ATG8 binding. Barley stripe mosaic virus (BSMV) subverts antiviral autophagy with the help of the γb protein, which disrupts ATG7–ATG8 interaction and thus impairs autophagosome formation. Different viruses hijack autophagy mechanisms to enhance viral pathogenicity. The TuMV VPg protein mediates the autophagic degradation of the host RNA silencing component SGS3 and its partner protein RDR6. SGS3 is also targeted during geminivirus infection involving the host protein NbCaM. The poleroviral protein P0 triggers ubiquitination and autophagic breakdown of AGO1, another component of the RNA silencing pathway. The movement protein NSvc4 of Rice stripe virus (RSV) induces the autophagic turnover of the group 1 remorin (REM1) protein through interference with its S‐acetylation, thereby preventing the REM1‐mediated negative regulation of viral cell‐to‐cell movement. Viruses like CaMV and TuMV also benefit from autophagy‐mediated suppression of disease‐associated host cell death, but it is unclear if and how viral proteins are involved in autophagy activation and which host components are targeted to mediate the cytoprotective effects. See also text for further details. Graphical elements are partly adapted from Marshall and Vierstra (2018).
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