Cell specialization and coordination in Arabidopsis leaves upon pathogenic attack revealed by scRNAseq

Plant defense responses involve several biological processes that allow plants to fight against pathogenic attacks. How these different processes are orchestrated within organs and depend on specific cell types is poorly known. Here, using scRNAseq technology, we identified 18 distinct cell populations in wild-type Arabidopsis leaves inoculated with the hemibiotrophic pathogen Pseudomonas syringae DC3000. Among those, we retrieved major cell types of the leaves (mesophyl, guard, epidermial, companion and vascular S cells) to which we could associate characteristic transcriptional reprogramming, thereby specifying different cell-type responses to the pathogen. Further analyses of transcriptional dynamics, based on inference of cell trajectories, indicated that the different cell types, in addition to their characteristic defense responses, can also share similar modules of gene reprogramming, allowing for instance vascular S cells, epidermal cells and mesophyl cells to converge towards an identical cell fate, mostly characterized by lignification and detoxification functions. Moreover, it appeared that defense responses of these three cell types can evolve along a second separate path. As this divergence does not correspond to the differentiation between immune and susceptible cells, we speculate that this might reflect the discrimination between cell-autonomous and non-cell-autonomous responses. Altogether our data provide an upgraded framework to describe, explore and explain the specialization and the coordination of plant cell responses upon pathogenic challenge.

植物防御响应包含一系列可帮助植物对抗病原侵染的生物学过程。目前学界对这些不同的生物学过程如何在器官内协同调控、且如何依赖特定细胞类型仍知之甚少。本研究借助单细胞RNA测序（single-cell RNA sequencing, scRNAseq）技术，对接种半活体营养病原丁香假单胞菌DC3000（Pseudomonas syringae DC3000）的野生型拟南芥叶片进行分析，共鉴定出18种不同的细胞群。其中涵盖了叶片的主要细胞类型（叶肉细胞（mesophyll）、保卫细胞（guard cell）、表皮细胞（epidermal cell）、伴胞（companion cell）及血管S细胞（vascular S cells）），我们为这些细胞类型匹配了特征性的转录重编程（transcriptional reprogramming）特征，由此明确了不同细胞类型对病原的响应模式。进一步基于细胞轨迹推断开展的转录动态分析显示，不同细胞类型除了各自特有的防御响应外，还可共享相似的基因重编程模块：例如血管S细胞、表皮细胞与叶肉细胞可收敛至同一细胞命运，该命运主要以木质化和解毒功能为特征。此外，这三种细胞类型的防御响应还可沿第二条独立路径发生动态变化。由于该分化并非对应免疫细胞与易感细胞间的分化，我们推测这或许反映了细胞自主性响应与非细胞自主性响应之间的区分。综上，本研究的数据提供了一个升级后的研究框架，用于描述、探究并阐释植物细胞在病原侵染下的响应特化与协同调控机制。