Defender or accomplice? Dual roles of plant vesicle trafficking in restricting and enabling geminiviral systemic infection

Abstract

The vesicle trafficking system enables multidirectional cargo fluxes between endomembrane compartments. However, vesicle trafficking plays dual roles during pathogen infections. In plants, it mediates autophagic immune responses but can also be hijacked by pathogens to facilitate successful infections. We demonstrate that vesicle trafficking machinery acts as a double-edged sword during infection by the geminivirus tomato yellow leaf curl Sardinia virus (TYLCSaV) in Nicotiana benthamiana. Virus-induced gene silencing of eight genes encoding key vesicle trafficking regulators revealed contrasting outcomes. Silencing of NbSAR1 and NbAP-1γ significantly increased systemic geminiviral DNA accumulation, whereas silencing of Nbδ-COP, NbARF1 and clathrin genes almost completely abolished infection. Notably, this inhibition is hypothesized to result from direct or indirect impairment in viral movement, as replication remained unaffected by gene silencing. The observed effects affect other geminiviruses, including tomato yellow leaf curl virus (TYLCV) and beet curly top virus (BCTV), but not unrelated pathogens, such as the RNA potato virus X (PVX) or the plant pathogenic bacterium Pseudomonas syringae. These findings suggest that while the vacuolar and autophagy branches of the vesicle trafficking system might mediate antiviral autophagic defence responses, the integrity of endocytosis and retrograde transport is essential for systemic geminiviral infection.