Identification of maize genes conditioning the early systemic infection of sugarcane mosaic virus by single-cell transcriptomics

During the early systemic infection of plant pathogens, individual cells can harbor pathogens at various stages of infection, ranging from absent to abundant. Consequently, the alterations in gene expression levels within these cells in response to the pathogens exhibit significant variability. These variations are pivotal in determining pathogenicity or susceptibility, yet they remain largely unexplored and poorly understood. Sugarcane mosaic virus (SCMV) is a representative member of the monocot-infecting potyviruses with a polyadenylated RNA genome, which could be captured by single-cell RNA sequencing (scRNA-seq). Here, we performed scRNA-seq with SCMV-infected maize leaves during the early systemic infection (prior to symptom manifestation) to investigate the co-variation patterns between viral accumulation levels and alterations in intracellular gene expression levels. We identified five cell types and found that mesophyll-4 (MS4) cells had the highest viral accumulation levels in most cells. The early systemic infection of SCMV resulted in up-regulation of most differentially expressed genes (DEGs), which were mainly enriched in biological processes related to translation, peptide biosynthesis and metabolism. Co-variation analysis of the altered maize gene expression levels and viral accumulation levels in MS1, 2 and 4 revealed several patterns, and the co-expression relationships between them were mainly positive. Furthermore, functional studies identified several potential anti- or pro-viral factors that may play crucial roles during the early stage of SCMV systemic infection. These results not only provide new insights into plant gene regulation during viral infection, but also offer feasible references for future investigations of host-virus interaction across molecular, cellular, and physiological scales.