An Evolutionarily Ancient Immune System Governs the Interactions between Pseudomonas syringae and an Early-Diverging Land Plant Lineage

Abstract

Evolutionary molecular plant-microbe interactions (EvoMPMI) is an emerging field bridging the gap between molecular phytopathology and evolutionary studies. EvoMPMI research is currently challenging due to the scarcity of pathogenic model systems in early-diverging land plants. Liverworts are among the earliest diverging land-plant lineages, and Marchantia polymorpha has emerged as a liverwort model for evolutionary studies. However, bacterial pathogens of Marchantia have not yet been discovered, and the molecular mechanisms controlling plant-pathogen interactions in this early-diverging land plant remain unknown. Here, we describe a robust experimental plant-bacterial pathosystem for EvoMPMI studies and discover that an ancient immune system governs plant-microbe interactions between M. polymorpha and the hemi-biotrophic pathogenic bacteria Pseudomonas syringae. We show that P. syringae pv tomato (Pto) DC3000, causal agent of tomato bacterial speck disease, colonizes M. polymorpha and activates typical hallmarks of plant innate immunity. Virulence of Pto DC3000 on M. polymorpha relies on effector activities inside liverwort cells, including conserved AvrPto and AvrPtoB functions. Host specificity analyses uncovered pathogenic differences among P. syringae strains, suggesting that M. polymorpha-P. syringae interactions are controlled by the genetic backgrounds of both host and pathogen. Finally, we show that ancient phytohormone defensive networks govern M. polymorpha-P. syringae interactions. Altogether, our results demonstrate that the basic structure of the plant immune system of extant angiosperms is evolutionarily ancient and conserved in early-diverging land plants. This basic immune system may have been instrumental for land colonization by the common ancestor of land plants.

Keywords: EvoMPMI; Marchantia-Pseudomonas syringae; PTI; effectors; hormones; model system.