DREPP protein StPCaP1 facilitates the cell‐to‐cell movement of Potato virus Y and Potato virus S by inhibiting callose deposition at plasmodesmata

Plant viruses, constrained by their limited genomic coding capacity, rely significantly on host factors for successful infection. Disruption of these essential host factors can confer resistance to viruses, with such factors categorized as susceptibility genes or recessive resistance genes. Recent research has identified developmentally regulated plasma membrane polypeptide (DREPP) proteins as susceptibility factors integral to the cell-to-cell movement of potyviruses. In the present study, we demonstrated that the silencing of StPCaP1, a DREPP gene in potato, confers novel resistance to both Potato virus Y (PVY, Potyvirus) and Potato virus S (PVS, Carlavirus). Interaction and subcellular localization analyses revealed that the movement proteins (MPs) of PVY (P3NPIPO) and PVS (TGB1) interact with StPCaP1, recruiting it to plasmodesmata (PD). Furthermore, transcriptome analysis and experimental validation indicated that compared to wild-type (WT) controls, StPCaP1-silenced lines exhibit significantly increased glucose content and elevated expression levels of several UDP-glucosyltransferases (UGTs), which are potential components of the callose synthesis complex. These findings suggest that StPCaP1 participates in callose deposition, as evidenced by the increased callose deposition at PD and reduced PD permeability observed in StPCaP1-silenced lines. Additionally, we found that StPCaP1 expression in Nicotiana benthamiana led to reduced callose deposition at PD and promoted PVY-GFP cell-to-cell movement in NbPCaP1-silenced plants in a concentration-dependent manner, which suggests the changes in callose deposition at PD induced by StPCaP1 relates to viral cell-to-cell movement. This study provides a deeper understanding of DREPP-mediated viral movement and highlights potential targets for developing virus-resistant crops.