A plant RNA virus activates selective autophagy in a UPR-dependent manner to promote virus infection
Citation
Li, F., Zhang, C., Tang, Z., Zhang, L., Dai, Z., Lyu, S., Li, Y., Hou, X., Bernards, M., Wang, A. (2020). A plant RNA virus activates selective autophagy in a UPR-dependent manner to promote virus infection. New Phytologist, [online] 228(2), 622-639. http://dx.doi.org/10.1111/nph.16716
Plain language summary
In this study, turnip mosaic virus (TuMV) was used as a model virus to better understand the complex roles of autophagy during virus infection in plants. We show that TuMV infection or transient expression of a small protein of TuMV named 6K2 upregulates the expression of the selective autophagy cargo adaptor gene NBR1 via activation of a major unfolded protein response (UPR) pathway. NBR1 interacts selectively with the TuMV trplcase protein NIb to promote virus infection. Moreover, NBR1 physically interacts with ATG8f of both Nicotiana benthamiana and Arabidopsis, and this interaction likewise promotes TuMV replication. We also discover that, in TuMV-infected cells, a large number of viral particles accumulates in the vacuole, and NbATG8f3 interacts with N. benthamiana tonoplast intrinsic protein 1 (NbTIP1), and the interaction complex together with NBR1 colocalise to the tonoplast-associated viral replication complex. Taken together our data suggest that TuMV takes advantage of NBR1-mediated selective autophagy through a cascade of protein–protein interactions to target the NIb-containing viral replication complex to the tonoplast for viral replication and virion assembly.
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.