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

Abstract

Summary 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.

Transcriptomic and functional analyses reveal an antiviral role of autophagy during pepper mild mottle virus infection

“…Autophagy is known to play an antiviral role in plant [ 29 ]. To further investigate the effect of autophagy on PMMoV infection, we silenced NbATG3 , NbATG5 , NbBeclin1 , NbATG7 and NbATG8a expressions in N. benthamiana plants individually using specific TRV-based VIGS vectors.…”

“…Several recent studies on plant autophagy and pathogen infections have revealed the importance of autophagy during pathogen infections [ 29 , 46 ]. Other studies have shown the specific roles of autophagy in eliminating viruses in mammalian cells [ 47 , 48 ].…”

The RNA-Dependent RNA Polymerase NIb of Potyviruses Plays Multifunctional, Contrasting Roles during Viral Infection

“…In this case, it has been shown that both host proteins rgs-CaM, a calmodulin-like protein, and NBR1, an autophagy cargo receptor, can mediate the degradation of HC-Pro via autophagy to restrict virus infection [96,98]. Moreover, like many animal viruses, potyviruses have evolved some strategies to subvert autophagy to promote their infection [99]. For instance, suppressor of gene silencing 3 (SGS3) and its intimate partner RNA-dependent RNA polymerase 6 (RDR6) are two crucial components of RNA silencing.…”

The Case of Virus-Induced Plant Autophagy: Cui Bono?

“…Autophagy is a targeted degradation and recycling pathway in plants activated under nutritional deprivation, but its network of autophagosomes can also perform the targeted removal of unwanted cellular components. In several cases, viruses interfere with and suppress host autophagy because it is targeting viral factors for degradation and thus hindering infection (Kushwaha et al, 2019). In other cases, pathogens have evolved to hijack autophagy to degrade host defense components, such as the RNA silencing pathway, for their own benefit (Kushwaha et al, 2019).…”

“…In several cases, viruses interfere with and suppress host autophagy because it is targeting viral factors for degradation and thus hindering infection (Kushwaha et al, 2019). In other cases, pathogens have evolved to hijack autophagy to degrade host defense components, such as the RNA silencing pathway, for their own benefit (Kushwaha et al, 2019). However, the Cotton leaf curl Multan virus (CLCuMuV) investigated by researchers in the lab of Yule Liu, induces autophagy in the host Nicotiana benthamiana that in turn targets a key viral protein, βC1, for degradation (Haxim et al, 2017).…”