Sri Lankan cassava mosaic virus Silencing Suppressor AC4 Mediates Autophagic Degradation of SGS3/RDR6 Bodies in Plants

Abstract

RNA silencing and autophagy play crucial roles in maintaining cellular homeostasis and defending against viral infections in diverse eukaryotic hosts. In response to RNA silencing defenses, the majority of plant viruses have evolved viral suppressors of RNA silencing (VSRs). Cassava mosaic geminiviruses (CMGs) are a group of bipartite begomoviruses that cause significant losses to the staple food crop cassava (Manihot esculenta Crantz). The AC4 protein, encoded by CMGs, is a well-characterized VSR; however, the precise mechanism underlying its suppression of RNA silencing remains unclear. This study demonstrates that AC4 expression impedes tasiRNA biogenesis. Moreover, the AC4 protein has been observed to interact with both SGS3 and its partner RDR6, which are essential for the synthesis of trans-acting small interfering RNAs and the amplification of RNA silencing. Notably, these interactions do not disrupt the association between AtSGS3 and AtRDR6 but instead induce their degradation. Furthermore, the AC4-mediated degradation of AtSGS3 is suppressed by an autophagy inhibitor, and AC4 enhances autophagy activity. The results indicate that the autophagy pathway is involved in AC4-mediated degradation of SGS3. These findings reveal a previously unidentified mechanism by which AC4 exploits autophagy to attenuate host RNA silencing, thereby impacting plant development and fulfilling its VSR function. This study offers new insights into the intricate relationship between RNA silencing and autophagy.