SARD1 and CBP60g redundantly regulate N-hydroxypipecolic acid- and salicylic acid-dependent systemic immunity but are dispensable for the activation of indolic defense metabolism.

We investigated the roles of the cognate, redundantly acting transcription factors SARD1 and CPB60g in the metabolic reprogramming of leaves of Arabidopsis thaliana suffering from bacterial infection or UV light exposure. Comprehensive metabolite analyses reveal that SARD1/CBP60g exert distinct influences on major stress-inducible metabolic pathways. The SARD1/CBP60g transcriptional node decisively boosts the biosynthesis of the systemic acquired resistance (SAR)-inducing metabolites N-hydroxypipecolic acid (NHP) and salicylic acid (SA), as well as their metabolism to major glucose conjugates. Additionally, it significantly promotes the biotic stress-induced accumulation of aromatic and branched-chain amino acids, and the generation of the antioxidant γ-tocopherol. By contrast, SARD1/CBP60g does not impact or yet exerts negative influence on the stress-induced biosynthesis of indolic defense compounds, including the phytoalexin camalexin, accumulation of Lys, Ser and Gly, and sterol desaturation. Significantly, we show that SARD1/CBP60g also acts downstream of NHP and SA in immune signaling, indicating a critical function of this transcriptional node in an NHP- and SA-driven immune amplification relay operating in SAR. RNA-sequencing analysis highlight that the transcriptional response to NHP is separable into two gene groups with different regulatory characteristics. One group consists of strongly SARD1/CBP60g-promoted genes that invariably contain NHP and SA-pathway genes and is enriched in SA-inducible genes. Genes of the other group, which overrepresents H2O2-inducible genes and concentrates genes of indolic metabolism, are not promoted by SARD1/CBP60g. Interestingly, SARD1/CBP60g oppositely affect the NHP-mediated priming of pathogen-induced SA and camalexin biosynthesis as well, illustrating that plants realize priming of distinct defenses by different mechanisms.