Unveiling the early defense response dynamics in grapevines against Plasmopara viticola by single-cell transcriptomics

BACKGROUND: The viticulture has long suffered from the downy mildew caused by Plasmopara viticola, a strictly obligate biotrophic oomycete. Numerous studies have been performed to reveal how grapevine defends against Plasmopara viticola, but they mainly investigate the plant defense responses on the whole tissue level, not on the cellular level. RESULTS: Here we employ single-cell RNA sequencing and spatial RNA sequencing to profile approximately 100,000 individual cells (~ 89,000 from scRNA-seq and ~ 11,000 from spRNA-seq), generating the first single-cell transcriptome atlas of grapevine leaves during Plasmopara viticola infection. This high-resolution atlas reveals the dynamic and distinct defense responses of plant cells at early stages of oomycete infection. Notably, we find that Plasmopara viticola reprograms the guard cell transcriptome to facilitate successful invasion, likely by altering the expression of ABA negative regulators and modulating a potassium channel regulatory pathway to influence stomatal movement. CONCLUSIONS: Overall, our work reveals differential and dynamic responses of grapevine to the Plasmopara viticola infection at a single-cell level, providing valuable clues for dissecting the interaction between plants and oomycetes.