Both small heat shock protein and J-Domain protein direct defense against Areca palm velarivirus 1 (APV1) by degrading coat protein via autophagy pathway

Both autophagy and heat shock proteins (HSPs) play dual roles in promoting or inhibiting viral infections. However, the coordination between autophagy and HSPs in the defense against viral infections remains underexplored, and the underlying mechanisms are still poorly understood. This study first revealed an interaction between a cytosolic small heat shock protein (AcsHSP) and a type II J-domain protein (AcDNAJB13) of areca palm with the coat protein (CP) of Areca Palm Velarivirus 1 (APV1) and the interaction is independent of the HSP70 chaperones. The closest homologs in Nicotiana benthamiana (NbsHSP and NbDNAJB13) also interacted with CP. Both AcsHSP and AcDNAJB13 were localized in the cytoplasm and nucleus, and co-expression with CP altered AcsHSP intracellular localization. APV1 infection or transient CP expression induced the expression of AcsHSP and AcDNAJB13 , which, in turn, inhibited CP accumulation. Virus-induced gene silencing (VIGS) of NbsHSP and NbDNAJB13 significantly increased the accumulation of transiently expressed CP-GFP. CP degradation occurred via an autophagic pathway. Both AcsHSP and AcDNAJB13 interacting with AcATG8f1, and these interactions were required for CP degradation. Furthermore, silencing endogenous NbsHSP and NbDNAJB13 enhanced APV1 replication, while overexpression of AcsHSP reduced APV1 accumulation. Our findings demonstrate that AcsHSP and AcDNAJB13 function as selective cargo receptors for CP degradation via autophagy pathway, thereby limiting APV1 infection and offering new insights into the roles of heat shock protein families.