Cell-type-specific response in host plants to the co-infection by sweet potato viruses

Host-virus interactions determine infection outcomes, with cellular heterogeneity playing a critical role in the dynamic interplay between host immune responses and viral evasion strategies. While animal and plant viruses use different mechanisms for cell entry, viral tropism is essential for pathogenesis across both kingdoms. To examine this overarching hypothesis, we studied sweet potato virus disease, the most devastating disease affecting sweet potato (Ipomoea batatas), which involves synergistic co-infection by the aphid-transmitted sweet potato feathery mottle virus and the whitefly-transmitted sweet potato leaf curl virus. By integrating single-cell RNA-Seq profiling with phenotypic assessments, we mapped virus specificity to a particular cell type within the host plant. As a result, we: 1) generated a comprehensive cellular atlas of sweet potato leaves, documenting the transcriptional response of 38,526 cells during co-infection; 2) traced virus-infected cells by examining viral genomic reads in each cell; 3) identified a tissue tropism in mesophyll, suggesting that selectively targeting cells with highly active cellular machinery is a common theme during infection by both plant and animal viruses; and finally 4) identified and characterized VIPE1, an AP2/ERF family transcription factor that contributes to viral resistance in sweet potato. These findings highlight the differential susceptibility and immune responses at both host and virus levels, underscoring the importance of understanding specific cellular and molecular features in developing targeted strategies for managing plant viruses.