Spatial H2O2 Signaling Specificity: H2O2 from Chloroplasts and Peroxisomes Modulates the Plant Transcriptome Differentially

Abstract

Hydrogen peroxide (H2O2) operates as a signaling molecule in eukaryotes, but the specificity of its signaling 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; Inzé et al., 2012) were grown under non-photorespiratory conditions and then transferred to photorespiratory conditions to foster the production of H2O2 in both organelles. We show that H2O2 originating in a specific organelle induces two types of responses: one that integrates signals independently from the subcellular site of H2O2 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 chloroplastic-produced H2O2, 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.

Suppressing Farnesyl Diphosphate Synthase Alters Chloroplast Development and Triggers Sterol-Dependent Induction of Jasmonate- and Fe-Related Responses

“…7A). Thus, our RNA-seq and RT-qPCR transcriptomic analyses further strengthen the connection between distinct biotic and abiotic stresses and changes in sterol composition, in particular those affecting the stigmasterol-to-b-sitosterol ratio (Grunwald, 1978;Whitaker, 1994;Griebel and Zeier, 2010;Wang et al, 2012b;Senthil-Kumar et al, 2013;Sewelam et al, 2014), which declines sharply upon the silencing of FPS (Fig. 3B).…”

Study of the Interactive Effects of Calcium and Abscisic Acid on Drought Stressed Triticum aestivum Seedlings

“…3). In accordance with these findings, it was reported that drought stress led to a decrease in the Fv/Fm ratio in bean plant, STUDY OF THE INTERACTIVE EFFECTS OF CALCIUM ... suggesting chronic photo-inhibition due to photooxidation of photosynthetic apparatus (Sewelam et al, 2014) and damage to the PSII oxygenevolving complex possibly attributable to D1 protein damage under drought stress (Zlatve & Yordanov, 2004). Likewise, it was suggested that the photosynthetic efficiency has been declined in Nothofagus species under drought stress (Piper et al, 2007 andLuo et al, 2015).…”

Redox- and Reactive Oxygen Species-Dependent Signaling into and out of the Photosynthesizing Chloroplast

“…The data indicate that ROS and redox signaling participate in early retrograde signaling (Gläßer et al, 2014). Conditional H 2 O 2 generation in chloroplasts or peroxisomes elicits distinct changes in gene expression (Sewelam et al, 2014). Chloroplast H 2 O 2 causes the up-regulation of transcripts involved in early signaling (including transcription factors), secondary signaling, mitochondrial retrograde signaling, and the biosynthesis of defense compounds in a time-dependent manner (Sewelam et al, 2014).…”