Plastid and cytoplasmic origins of 1O2-mediated transcriptomic responses

Abstract

The reactive oxygen species singlet oxygen, 1O2, has an extremely short half-life, yet is intimately involved with stress signalling in the cell. We previously showed that the effects of 1O2 on the transcriptome are highly correlated with 80S ribosomal arrest due to oxidation of guanosine residues in mRNA. Here, we show that dysregulation of chlorophyll biosynthesis in the flu mutant or through feeding by δ-aminolevulinic acid can lead to accumulation of photoactive chlorophyll intermediates in the cytoplasm, which generates 1O2 upon exposure to light and causes the oxidation of RNA, eliciting 1O2-responsive genes. In contrast, transcriptomes derived from DCMU treatment, or the Ch1 mutant under moderate light conditions display commonalties with each other but do not induce 1O2 gene signatures. Comparing 1O2 related transcriptomes to an index transcriptome induced by cycloheximide inhibition enables distinction between 1O2 of cytosolic or of plastid origin. These comparisons provide biological insight to cases of mutants or environmental conditions that produce 1O2.

Multiple paths of plant host toxicity are associated with the fungal toxin cercosporin

“…GO analysis of the 202 transcripts that were in common with CHX, RB and cercosporin treatments showed a preponderance of stress response genes (Supporting Information: Figure ). The results are similar to previous meta‐analyses of transcriptomes using endogenous photodynamic molecules such as protochlorophyllide that accumulates in the 1 O 2 ‐producing flu mutant (Koh et al, 2021, 2022). Thus, at least one component of the cercosporin transcriptome can be explained through its photooxidative behaviour.…”

“…Figure S7). The results are similar to previous meta-analyses of transcriptomes using endogenous photodynamic molecules such as protochlorophyllide that accumulates in the 1 O 2 -producing flu mutant (Koh et al, 2021(Koh et al, , 2022. Thus, at least one component of the cercosporin transcriptome can be explained through its photooxidative behaviour.…”

“…We first examined the toxicity of cercosporin in the non‐host species Arabidopsis. In Arabidopsis, molecular insights about the cellular effect of 1 O 2 have recently been established (Chen & Fluhr, 2018; Koh et al, 2021, 2022; op den Camp et al, 2003). Leaf discs of Arabidopsis treated with cercosporin induced significant ion leakage within 2 h in the light (30 µE m −2 s −1 ; Supporting Information: Figure ).…”

A novel glutathione peroxidase-based biosensor disentangles differential subcellular accumulation of H2O2 and lipid hydroperoxides

“…produced by long dark periods and carbon starvation) the transport of fatty acids from chloroplasts markedly increases (Fan et al 2017). In support of this suggestion, transcriptome studies in Arabidopsis that unite the various means of eliciting 1 O 2 -induced oxidative stress show many differentially expressed genes encoding ABC transporters (Willems et al 2016; Bode et al 2016; Koh et al 2022). An additional possibility is that lipid peroxides could be conjugated to or reduced by glutathione (as GSH) by a multiplicity of Glutathione-S-Transferase (GST) isoforms (Dixon and Edwards 2010; de Dios Alché 2019).…”

“…An additional possibility is that lipid peroxides could be conjugated to or reduced by glutathione (as GSH) by a multiplicity of Glutathione-S-Transferase (GST) isoforms (Dixon and Edwards 2010; de Dios Alché 2019). Many GST genes are highly expressed under the same oxidative stress conditions (Willems et al 2016; Koh et al 2022). However, notwithstanding how the accumulation of LOOH occurs in the cytosol, their presence likely indicates an advanced state of oxidative stress that would initiate programmed cell death (Mullineaux and Baker 2010; Willems et al 2016; Wasternak and Feussner 2018; Koh et al 2022).…”