Host microenvironment in potato-Phytophthora infestans interaction revealed by single-cell spatiotemporal transcriptome.

Late blight, caused by Phytophthora infestans (P. infestans), is one of the most destructive diseases in potato production. Yet, the interaction landscape between potato and the late blight pathogen at single-cell and spatial resolution remains elusive. Here we utilize Stereo-seq to present the spatiotemporal transcriptome atlas in potato leaves inoculated with P. infestans at single-cell resolution. We retrieve the major cell types of potato leaves, highlighting the coordination and specialization of immune responses among distinct cell types. We also conduct a comprehensive analysis to elucidate the multifaceted infection strategies employed by P. infestans to facilitate successful host colonization. Furthermore, we distinguish pathogen-targeted cells (PTCs) and surrounding PTC cells (SPCs) on the basis of pathogen distribution, thereby revealing the cellular and spatial heterogeneity of plant immune responses. Specifically, transcriptional profiling indicates that PTCs are mainly involved in cell wall reinforcement and regulation of redox homeostasis, whereas SPCs probably play a role in coordinating systemic immune signalling. Collectively, our findings elucidate a regulatory paradigm wherein PTCs and SPCs integrate with the cell-type-specific responses and dynamic expression patterns of P. infestans, orchestrating a complex and finely tuned host microenvironment during the interaction between potato and P. infestans. These findings provide a resource for advancing our understanding of the dynamic and heterogeneous nature of plant-pathogen interactions, offering novel insights to enhance crop disease resistance.