Singlet oxygen-mediated signaling in plants: moving from flu to wild type reveals an increasing complexity

Abstract

Singlet oxygen (1O2)-mediated signaling has been established in the conditional fluorescent (flu) mutant of Arabidopsis. In the dark, the flu mutant accumulates free protochlorophyllide (Pchlide), a photosensitizer that in the light generates 1O2. The release of 1O2 leads to growth inhibition of mature plants and bleaching of seedlings. These 1O2-mediated responses depend on two plastid proteins, EXECUTER (EX) 1 and 2. An ex1/ex2/flu mutant accumulates in the dark Pchlide and upon illumination generates similar amounts of 1O2 as flu, but 1O2-mediated responses are abrogated in the triple mutant. The 1O2- and EX-dependent signaling pathway operates also in wild type placed under light stress. However, it does not act alone as in flu, but interacts with other signaling pathways that modulate 1O2-mediated responses. Depending on how severe the light stress is, 1O2- and EX-dependent signaling may be superimposed by 1O2-mediated signaling that does not depend on EX and is associated with photo-oxidative damage. Because of its high reactivity and short half-life, 1O2 is unlikely to be a signal that is translocated across the chloroplast envelope, but is likely to interact with other plastid components close to its site of production and to generate more stable signaling molecules during this interaction. Depending on the site of 1O2 production and the severity of stress, different signaling molecules may be expected that give rise to different 1O2-mediated responses.

Cell growth defect factor 1 is crucial for the plastid import of NADPH:protochlorophyllide oxidoreductase A in Arabidopsis thaliana

“…Presumably by virtue of its holdase activity (23), CDF1 bound the transporting pPORA and transA-DHFR and thereby blocked their retrograde movement to the cytosol. At the same time, CDF1 permitted Pchlide binding to proceed to the transporting polypeptide chains, and thereby CDF1 lowered the risk of photooxidative damage by free Pchlide molecules operating as a photosensitizer and triggering the production of singlet oxygen (27).…”

“…The large amount of free, non-POR-bound Pchlide in Atcdf1 seedlings suggested that the porphyrin pigment could act as a photosensitizer and trigger the production of singlet oxygen once the seedlings were illuminated. Kim and Apel (27) have shown that singlet oxygen operates both as a powerful signaling compound and cytotoxin and that both effects contribute to cell death execution.…”

The Roles of Reactive Oxygen Metabolism in Drought: Not So Cut and Dried

“…The Arabidopsis flu (fluorescent) mutant has been extensively used to study singlet oxygen signaling (Kim and Apel, 2013). The excess singlet oxygen production in this line does not occur within the PSII reaction center, which is probably the most relevant site for electron transport-linked singlet oxygen signaling.…”

“…However, because of the spatial separation of scavengers from the site of generation, singlet oxygen produced in the reaction center can largely evade removal by cellular antioxidants. Hence, drought-induced increases in singlet oxygen generation in the chloroplasts will facilitate the operation of oxylipin and jasmonatedependent pathways that underpin further local and systemic responses in gene expression (Kim and Apel, 2013). Recent evidence suggests that oxidation products produced by interactions with carotenoids are also important in singlet oxygen signaling (Ramel et al, 2012).…”

The ROS Wheel: Refining ROS Transcriptional Footprints

“…Unlike the vast amounts of ATH1 microarray data that have documented oxidative stress responses at the transcript level, RNA-Seq studies are still outnumbered. Examples of oxidative stress RNA-Seq studies are a time-course experiment during reillumination of the flu mutant (Kim and Apel, 2013) and O 3 treatments in different accessions (Xu et al, 2015a(Xu et al, , 2015b. In order to assess transcriptional changes upon photorespiratory stress, we conducted an additional RNA-Seq study in cat2 mutants after 3 h of stress (Supplemental Materials and Methods S1).…”