A plant RNA virus activates selective autophagy in a UPR‐dependent manner to promote virus infection

Abstract

Autophagy is an evolutionarily conserved pathway in eukaryotes that delivers unwanted cytoplasmic materials to the lysosome/vacuole for degradation/recycling. Stimulated autophagy emerges as an integral part of plant immunity against intracellular pathogens. In this study, we used turnip mosaic virus (TuMV) as a model to investigate the involvement of autophagy in plant RNA virus infection. The small integral membrane protein 6K2 of TuMV, known as a marker of the virus replication site and an elicitor of the unfolded protein response (UPR), upregulates the selective autophagy receptor gene NBR1 in a UPR-dependent manner. NBR1 interacts with TuMV NIb, the RNA-dependent RNA polymerase of the virus replication complex (VRC), and the autophagy cargo receptor/adaptor protein ATG8f. The NIb/NBR1/ATG8f interaction complexes colocalise with the 6K2-stained VRC. Overexpression of NBR1 or ATG8f enhances TuMV replication, and deficiency of NBR1 or ATG8f inhibits virus infection. In addition, ATG8f interacts with the tonoplast-specific protein TIP1 and the NBR1/ATG8f-containing VRC is enclosed by the TIP1-labelled tonoplast. In TuMV-infected cells, numerous membrane-bound viral particles are evident in the vacuole. Altogether these results suggest that TuMV activates and manipulates UPR-dependent NBR1-ATG8f autophagy to target the VRC to the tonoplast to promote viral replication and virion accumulation.

Rheostatic Balance of Circadian Rhythm and Autophagy in Metabolism and Disease

“…Therefore, the reasons for the diseases induced by rhythmic autophagy dysfunction are discussed here. Rhythmic autophagy is capable of removing damaged materials from cells regularly, and a deficiency in this process can lead to the accumulation of abnormal cellular components, which finally induce cells and whole organisms to undergo pathological conditions (Li et al, 2020;Wu and Nagy, 2020). Autophagy might be activated to eliminate damaged organelles, proteins and lipids after oxidative phases of metabolism (Pacheco et al, 2020).…”

“…Cytoplasmic materials are first surrounded by vesicles, which eventually form double membrane structures called autophagosomes (Klionsky et al, 2014;Gou et al, 2020). The autophagosomes then fuse with lysosomes and create autolysosomes where the cargo is degraded and released as critical nutrients, such as fatty acids, back into the cytosol (Gatica et al, 2018;Li et al, 2020;Patra et al, 2020). Autophagy is capable of regulating many0020biochemical processes, including embryogenesis, development, antigen presentation, metabolism and infection removal (Bonam et al, 2020;Farhan et al, 2020;Wu and Nagy, 2020).…”

Emerging Roles of the Selective Autophagy in Plant Immunity and Stress Tolerance

“…Targeting TuMV VRCs to tonoplast and promote viral replication and assembly. [110] Hordeivirus BSMV γb NbATG7…”

“…It has been reported that Beclin1/ATG6 in N. benthamiana serves as a cargo receptor that selectively mediates the degradation of TuMV NIb protein (RDRP) and restricts TuMV replication [ 98 ]. Interestingly, the same group showed that NBR1 can serve as a selective receptor for TuMV NIb via interacting with ATG8f [ 110 ]. However, instead of being targeted to vacuoles for degradation, the NIb-NBR1-ATG8f-containing autophagosomes, to which the viral replication complexes (VRCs) are associated, are targeted to the tonoplast via an interaction between ATG8f and the tonoplast-intrinsic protein 1 (TIP1), leading to robust viral genome translation/replication and virion assembly in the tonoplast-associated VRCs [ 110 ].…”

“…Interestingly, the same group showed that NBR1 can serve as a selective receptor for TuMV NIb via interacting with ATG8f [ 110 ]. However, instead of being targeted to vacuoles for degradation, the NIb-NBR1-ATG8f-containing autophagosomes, to which the viral replication complexes (VRCs) are associated, are targeted to the tonoplast via an interaction between ATG8f and the tonoplast-intrinsic protein 1 (TIP1), leading to robust viral genome translation/replication and virion assembly in the tonoplast-associated VRCs [ 110 ]. It seems that the NBR1- and Beclin1-mediated selective autophagy of NIb antagonize with each other to promote and inhibit the TuMV infection, respectively [ 98 , 110 ].…”