Rhizobiales commensal bacteria promote Arabidopsis thaliana root growth via host sulfated peptide pathway

Abstract Root-associated commensal bacteria that belong to the order Rhizobiales, which also contains symbiotic and pathogenic bacteria, promote primary root growth of Arabidopsis thaliana. Yet, its underlying molecular mechanism and physiological impact remained unclear. Here, we conducted a transcriptomic analysis of A. thaliana roots inoculated with root-associated commensal bacteria of Rhizobiales and sister lineages and revealed common and strain/lineage-specific transcriptional responsea, possibly mediated by WRKY and ANAC family of transcription factors. We revealed that the observed common response was also partially triggered by a wide range of non-pathogenic bacteria, fungi, and a multi-kingdom synthetic community (SynCom). This response was characterized by a down-regulation of genes related to intracellular redox regulation, suggesting distinctive redox status between pathogenic and non-pathogenic interactions. By integrating this analysis with developmental and cell biological analyses, we identified a crucial role for the sulfated peptide pathway mediated by TYROSYLPROTEIN SULFOTRANSFERASE (TPST) in Rhizobiales root growth promotion (RGP) activity. Conversely, none of the known sulfated peptide pathway appeared to be required for this activity, suggesting a novel sulfated protein pathway targeted by Rhizobiales RGP. Finally, we show that TPST is needed for RGP exerted by Rhizobiales but not Pseudomonadales isolates, delineating lineage-specific mechanisms to manipulate host root development.