Barley stripe mosaic virus γb Protein Subverts Autophagy to Promote Viral Infection by Disrupting the ATG7-ATG8 Interaction

Abstract

Autophagy is a conserved defense strategy against viral infection. However, little is known about the counterdefense strategies of plant viruses involving interference with autophagy. Here, we show that γb protein from (BSMV), a positive single-stranded RNA virus, directly interacts with AUTOPHAGY PROTEIN7 (ATG7). BSMV infection suppresses autophagy, and overexpression of γb protein is sufficient to inhibit autophagy. Furthermore, silencing of autophagy-related gene and in plants enhanced BSMV accumulation and viral symptoms, indicating that autophagy plays an antiviral role in BSMV infection. Molecular analyses indicated that γb interferes with the interaction of ATG7 with ATG8 in a competitive manner, whereas a single point mutation in γb, Tyr29Ala (Y29A), made this protein deficient in the interaction with ATG7, which was correlated with the abolishment of autophagy inhibition. Consistently, the mutant BSMV virus showed reduced symptom severity and viral accumulation. Taken together, our findings reveal that BSMV γb protein subverts autophagy-mediated antiviral defense by disrupting the ATG7-ATG8 interaction to promote plant RNA virus infection, and they provide evidence that ATG7 is a target of pathogen effectors that functions in the ongoing arms race of plant defense and viral counterdefense.

Autophagic degradation of the Cucumber mosaic virus virulence factor 2b balances antiviral RNA silencing with proviral plant fitness and virus seed transmission

“…Whether viral proteins have evolved to function as autophagy cargo receptors to mediate degradation of RNA silencing components is indeed an exciting option. Our results, however, do not support that 2b uses this strategy to counteract RNA silencing-dependent resistance, and in general autophagy seems to support rather than antagonize resistance against plant viruses (7-9, 13, 14, 27).…”

“…While autophagy-mediated resistance has been established for several animal viruses (12), comparative findings were largely lacking for plant viruses. Only very recently we and others have found that autophagy targets multiple plant viruses, including the positive-stranded RNA viruses TuMV and Barley stripe mosaic virus (7, 14, 27), the negative-stranded RNA virus Rice stripe virus (13), the double-stranded DNA virus CaMV (8) and three single-stranded DNA geminiviruses (9). These findings established autophagy as a central component of plant immunity against viruses, which is fortified further by our current results on CMV.…”

Nuclear autophagy degrades a geminivirus nuclear protein to restrict viral infection in solanaceous plants

“…C1, C2, C3, V1 from DNA-A, and NSP from DNA-B), showing the functional importance of nuclear localization for the geminivirus infection cycle (Fondong 2013;Wang & Zhou 2016;Kushwaha et al, 2017). Recently, plant virus-infection-induced autophagy has been described in many plant-virus interactions (Nakahara et al, 2012;Hafr en et al, 2017Hafr en et al, , 2018Haxim et al, 2017;Li et al, 2017Li et al, , 2018Yang et al, 2018). Interestingly, we found that the C1 protein of TLCYnV is translocated from the nucleus to the cytoplasm after 24 hpi, with a concomitant decrease in protein accumulation (Figs 1, 2, S1).…”

“…Antiviral autophagy involves the recruitment of specific substrates (viral particles or viral proteins) by adaptor proteins, such as ATG8, NBR1 (neighbor of BRCA1 gene 1), and Beclin1, which guide the cargos to autophagosomes for degradation (Clavel et al, 2017;Ding et al, 2018). For example, the barley stripe mosaic virus cb protein subverts autophagy-mediated antiviral defense by disrupting the ATG7-ATG8 interaction to promote the virus infection (Yang et al, 2018); the geminivirus bC1 protein, on the other hand, exploits the autophagy pathway indirectly through upregulating rgs-CaM (regulator of gene silencing calmodulin-like protein) to promote the autophagic degradation of the SGS3 protein, involved in antiviral RNA silencing . For example, the barley stripe mosaic virus cb protein subverts autophagy-mediated antiviral defense by disrupting the ATG7-ATG8 interaction to promote the virus infection (Yang et al, 2018); the geminivirus bC1 protein, on the other hand, exploits the autophagy pathway indirectly through upregulating rgs-CaM (regulator of gene silencing calmodulin-like protein) to promote the autophagic degradation of the SGS3 protein, involved in antiviral RNA silencing .…”

Remorin interacting with PCaP1 impairs Turnip mosaic virus intercellular movement but is antagonised by VPg

“…Viruses and hosts antagonise each other. Mushrooming reports have shown that UPS and autophagy are extensively involved in the co-evolutionary arms race between plants and viruses (Liu et al, 2005;Nakahara et al, 2012;Jia et al, 2016;Cheng & Wang, 2017;Hafr en et al, 2017;Haxim et al, 2017;Fu et al, 2018;Hafr en et al, 2018;Li et al, 2018;Yang et al, 2018). For example, bC1 of Cotton leaf curl Multan virus interacts with NbSKP1s to subvert the UPS (Jia et al, 2016), but it interacts with ATG8 to be degraded through the autophagy pathway (Haxim et al, 2017).…”