Spatial H202 Signaling Specificity： H202 from Chloroplasts and Peroxisomes Modulates the Plant Transcriptome Differentially

Hydrogen peroxide （H2O2） operates as a signaling molecule in eukaryotes, but the specificity of its signal- ing capacities remains largely unrevealed. Here, we analyzed whether a moderate production of H2O2 from two different plant cellular compartments has divergent effects on the plant transcriptome. Arabidopsis thaliana overexpressing glycolate oxidase in the chloroplast （Fahnenstich et al., 2008; Balazadeh et al., 2012） and plants deficient in peroxisomal catalase （Queval et al., 2007; Inze et al., 2012） were grown under non-photorespiratory conditions and then transferred to photorespiratory conditions to foster the production of H202 in both organelles. We show that H202 originating in a specific organelle induces two types of responses： one that integrates signals independently from the subcellular site of H202 production and another that is dependent on the H2O2 production site. H2O2 produced in peroxisomes induces transcripts involved in protein repair responses, while H2O2 produced in chloroplasts induces early signaling responses, including transcription factors and biosynthetic genes involved in production of secondary signaling messengers. There is a significant bias towards the induction of genes involved in responses to wounding and pathogen attack by chloroplas- tic-produced H202, including indolic glucosinolates-, camalexin-, and stigmasterol-biosynthetic genes. These transcriptional responses were accompanied by the accumulation of 4-methoxy-indol-3-ylmethyl glucosinolate and stigmasterol.

Regulatory and Functional Aspects of Indolic Metabolism in Plant Systemic Acquired Resistance

Tryptophan-derived, indolic metabolites possess diverse functions in Arabidopsis innate immunity to microbial pathogen infection. Hers, we investigate the functional role and regulatory characteristics of indolic metabolism in Arabidopsis systemic acquired resistance （SAR） triggered by the bacterial pathogen Pseudomonas syringae. Indolic metabolism is broadly activated in both P. syringae-inoculated and distant, non-inoculated leaves. At inoculation sites, camalexin, indol-3-ylmethylamine （13A）, and indole-3-carboxylic acid （ICA） are the major accumulating compounds. Camalexin accumulation is positively affected by MYB122, and the cytochrome P450 genes CYP81F1 and CYP81F2. Local 13A production, by contrast, occurs via indole glucosinolate breakdown by PEN2- dependent and independent pathways. Moreover, exogenous application of the defense hormone salicylic acid stimulates 13A generation at the expense of its precursor indol-3-ylmethylglucosinolate （13M）, and the SAR regulator pipecolic acid primes plants for enhanced P. syringae-induced activation of distinct branches of indolic metabolism. In uninfected systemic tissue, the metabolic response is more specific and associated with enhanced levels of the indolics 13A, ICA, and indole-3-carbaldehyde （ICC）. Systemic indole accumulation fully depends on functional CYP79B2/3, PEN2, and MYB34/51/122, and requires functional SAR signaling. Genetic analyses suggest that systemi- cally elevated indoles are dispensable for SAR and associated systemic increases of salicylic acid. However, soil-grown but not hydroponically -cultivated cyp79b2/3 and pen2 plants, both defective in indolic secondary metabolism, exhibit pre-induced immunity, which abrogates their intrinsic ability to induce SAR.