A Conserved Salicylic Acid Signaling Pathway Controls Plant Immunity against Pseudomonas thought the unique TGA transcription factor in Marchantia polymorpha

Land plants have co-evolved with microorganisms since its transition to a terrestrial habitat around 500 million years ago. In angiosperms, salicylic acid (SA) activates plant immunity against hemibiotrophic pathogens thought TGA transcription factors, which bind to the promoter of SA-responsive loci, such as pathogenesis-related (PR) genes, to enforce plants immunity. While those mechanisms are well-known in flowering plants, our understanding in bryophytes remains limited, as genetic evidences for the role of SA in plant immunity are still largely 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 M. polymorpha with the generation of SA-deficient plants in this liverwort by overexpressing the bacterial NahG gene, a SA-degrading enzyme. Our results indicate that P. syringae induced transcriptional footprint is enriched in SA-responsive genes and that Marchantia NahG plants are compromised in immune responses against P. syringae. We found that MpTGA is modulated by SA and essential for controlling resistance against Pseudomonas. Further transcriptional analysis to identify the coregulatory network controlled by SA and MpTGA, indicate that a SA/MpTGA module might execute the boost of plants' defence responses thought a variety of MpPRs, highlighting a notable control of class III secretory peroxidases belonging to the MpPR9 subfamily. Altogether, our data demonstrate the functional conservation of SA as an immune hormone and underpin the existence of a SA-controlled MpTGA transcriptional cluster driving resistance against Pseudomonas in M. polymorpha Overall design: RNA-seq of Marchantia WT Tak-1, Mptga mutant and SA-deficient Marchantia NahG plants infected with Pseudomonas syringae pv. tabaci (Pta) 11528 (performed on 3 weeks old whole plants)