Autophagy functions as an antiviral mechanism against geminiviruses in plants

Abstract

Autophagy is an evolutionarily conserved process that recycles damaged or unwanted cellular components, and has been linked to plant immunity. However, how autophagy contributes to plant immunity is unknown. Here we reported that the plant autophagic machinery targets the virulence factor βC1 of Cotton leaf curl Multan virus (CLCuMuV) for degradation through its interaction with the key autophagy protein ATG8. A V32A mutation in βC1 abolished its interaction with NbATG8f, and virus carrying βC1V32A showed increased symptoms and viral DNA accumulation in plants. Furthermore, silencing of autophagy-related genes ATG5 and ATG7 reduced plant resistance to the DNA viruses CLCuMuV, Tomato yellow leaf curl virus, and Tomato yellow leaf curl China virus, whereas activating autophagy by silencing GAPC genes enhanced plant resistance to viral infection. Thus, autophagy represents a novel anti-pathogenic mechanism that plays an important role in antiviral immunity in plants.DOI: http://dx.doi.org/10.7554/eLife.23897.001

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

“…Deficiency of ATG8h, ATG5, or ATG7 enhanced the pathogenicity of TLCYnV in N. benthamiana and S. lycopersicum plants (Fig. Therefore, the autophagic degradation of the bC1 protein might not be the reason leading to the general suppression of geminivirus infection (Haxim et al, 2017). This observation is consistent with the previous report that knocking down ATG5 or ATG7 in N. benthamiana plants rendered them more susceptible to the infection by several geminiviruses (Haxim et al, 2017).…”

“…These discoveries can pave the way to the design of novel antiviral strategies by exploiting autophagy to fight geminivirus infection (Fig. This observation is consistent with the previous report that knocking down ATG5 or ATG7 in N. benthamiana plants rendered them more susceptible to the infection by several geminiviruses (Haxim et al, 2017). Deficiency of ATG8h, ATG5, or ATG7 enhanced the pathogenicity of TLCYnV in N. benthamiana and S. lycopersicum plants (Fig.…”

“…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).…”

“…6). Although the viral DNA accumulation of different geminiviruses has been shown to be suppressed by the autophagic degradation of the bC1 protein encoded by the betasatellite (Haxim et al, 2017), only some monopartite begomoviruses are associated with the betasatellites (Zhou, 2013). 6), indicating that autophagy is an important defense mechanism against geminiviruses.…”

“…Silencing ATG8h, ATG5, or ATG7 alone did not induce observable phenotypes in N. benthamiana or S. lycopersicum plants, as described previously (Devarenne, 2011;Haxim et al, 2017;Li et al, 2017Li et al, , 2018: silencing of ATG8h, ATG5, or ATG7 was confirmed by RT-qPCR (Fig. Thus, five or six-leaf stage N. benthamiana plants were pre-inoculated with TRV-NbAG8h (to silence NbATG8h), TRV-NbATG5 (to silence NbATG5), TRV-NbATG7 (to silence NbATG7), or TRV-GUS (as a control) and agroinfiltrated with a TLCYnV infectious clone 7 d later.…”