Salicylic acid and the unique TGA transcription factor controls plant immunity against Pseudomonas syringae in Marchantia polymorpha.

Land plants have co-evolved with microorganisms since their transition to a terrestrial habitat, around 500 million years ago. In angiosperms, salicylic acid (SA) activates plant immunity against hemibiotrophic pathogens through TGACG-motif-binding (TGA) transcription factors, which bind to the promoter of SA-responsive loci, such as pathogenesis-related (PR) genes, to enforce plant immunity. While those mechanisms are well-known in flowering plants, our understanding in bryophytes remains limited, as genetic evidences for the role of SA during plant immunity are still missing. Here, we explore the interaction between Marchantia polymorpha and the bacterium Pseudomonas syringae to gain insights into the evolutionary immune function of SA during bryophyte-pathogen interactions. We combined transcriptomic profiling of P. syringae-infected Marchantia with the generation of SA-deficient plants in this liverwort by overexpressing the bacterial NahG gene, a SA-degrading enzyme. Our results indicate that the P. syringae-induced transcriptional footprint is enriched in SA-responsive genes and that SA-deficient Marchantia NahG plants are compromised in immune responses against P. syringae. We show that the unique MpTGA is essential for controlling resistance against Pseudomonas. Further transcriptional analyses into the coregulatory network controlled by SA and MpTGA indicate that an SA/MpTGA module activates plant defence responses through a variety of MpPRs, enriched in the regulation of class III of secretory peroxidases belonging to the MpPR9 subfamily during the early defensive response against P. syringae. Altogether, our data demonstrate the functional conservation of SA as an immune hormone and underpin the existence of a SA/MpTGA-regulated transcriptional cluster driving resistance against Pseudomonas in Marchantia.