No single way to understand singlet oxygen signalling in plants

Kim, Chanhong; Meskauskiene, Rasa; Apel, Klaus; Laloi, Christophe

doi:10.1038/embor.2008.57

Cited by 144 publications

(125 citation statements)

References 49 publications

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“…They can both function as a signal to activate stress-related responses and cause oxidative damage to cells [46]. High salinity in soil is a serious environmental stress to plants and induction of ROS accumulation in plants has also been observed [35,47].…”

Section: Discussionmentioning

confidence: 99%

The endoplasmic reticulum-associated degradation is necessary for plant salt tolerance

et al. 2010

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Eukaryotic organisms have quality-control mechanisms that allow misfolded or unassembled proteins to be retained in the endoplasmic reticulum (ER) and subsequently degraded by ER-associated degradation (ERAD). The ERAD pathway is well studied in yeast and mammals; however, the biological functions of plant ERAD have not been reported. Through molecular and cellular biological approaches, we found that ERAD is necessary for plants to overcome salt stress. Upon salt treatment ubiquitinated proteins increased in plant cells, especially unfolded proteins that quickly accumulated in the ER and subsequently induced ER stress responses. Defect in HRD3A of the HRD1/ HRD3 complex of the ERAD pathway resulted in alteration of the unfolded protein response (UPR), increased plant sensitivity to salt, and retention of ERAD substrates in plant cells. Furthermore, we demonstrated that Ca 2+ release from the ER is involved in the elevation of UPR and reactive oxygen species (ROS) participates the ERAD-related plant salt response pathway.

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Section: Discussionmentioning

confidence: 99%

The endoplasmic reticulum-associated degradation is necessary for plant salt tolerance

et al. 2010

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“…Low subtoxic levels of 1 O 2 that do not cause any significant LPO are apparently sufficient to trigger signaling events in bacteria (Agnez-Lima et al, 2001), cyanobacteria (Anthony et al, 2005), algae (Ledford et al, 2007), and mammalian cells (Klotz et al, 2003). In the Arabidopsis flu mutant, 1 O 2 is produced by protochlorophyllides that accumulate after a dark-to-light shift hereby leading to cytotoxic effects in etiolated seedlings and to 1 O 2 -mediated stress signaling and programmed cell death in green plantlets (op den Camp et al, 2003;Wagner et al, 2004;Kim et al, 2008;Przybyla et al, 2008). In agreement with the 1 O 2 signaling function, we observed an early accumulation of 1 O 2 -specific transcripts in light-stressed ch1 and Cat (2) plants.…”

Section: Discussionmentioning

confidence: 99%

“…In leaves of the flu mutant, a genetic cell death program can be triggered by protochlorophyllidedependent 1 O 2 , involving 13-LOX LPO, and apparently occurs without any increase of nonenzymatic LPO early in the signaling phase, whereas in etiolated seedlings transferred to the light, 1 O 2 production appeared to be cytotoxic and led to nonenzymatic LPO and cell death (Kim et al, 2008;Przybyla et al, 2008). We observed in our experiments that the first photooxidative leave damage symptoms, which appeared in the light 4 h after the dark/light shift, were accompanied by a nonenzymatic LPO caused almost exclusively by 1 O 2 (about 15% of the 13-LOX LPO; Supplemental Fig.…”

Section: O 2 Generation Induces Cell Death In Arabidopsis Leaf Tissuesmentioning

confidence: 99%

Singlet Oxygen Is the Major Reactive Oxygen Species Involved in Photooxidative Damage to Plants

Triantaphylidès¹,

Krischke²,

Hoeberichts³

et al. 2008

Plant Physiology

507

358

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Reactive oxygen species act as signaling molecules but can also directly provoke cellular damage by rapidly oxidizing cellular components, including lipids. We developed a high-performance liquid chromatography-electrospray ionization-tandem mass spectrometry-based quantitative method that allowed us to discriminate between free radical (type I)-and singlet oxygen ( 1 O 2 ; type II)-mediated lipid peroxidation (LPO) signatures by using hydroxy fatty acids as specific reporters. Using this method, we observed that in nonphotosynthesizing Arabidopsis (Arabidopsis thaliana) tissues, nonenzymatic LPO was almost exclusively catalyzed by free radicals both under normal and oxidative stress conditions. However, in leaf tissues under optimal growth conditions, 1 O 2 was responsible for more than 80% of the nonenzymatic LPO. In Arabidopsis mutants favoring 1 O 2 production, photooxidative stress led to a dramatic increase of 1 O 2 (type II) LPO that preceded cell death. Furthermore, under all conditions and in mutants that favor the production of superoxide and hydrogen peroxide (two sources for type I LPO reactions), plant cell death was nevertheless always preceded by an increase in 1 O 2 -dependent (type II) LPO. Thus, besides triggering a genetic cell death program, as demonstrated previously with the Arabidopsis fluorescent mutant, 1 O 2 plays a major destructive role during the execution of reactive oxygen species-induced cell death in leaf tissues.Plant leaves capture sun-derived light energy to drive CO 2 fixation during photosynthesis. During this process, leaves need to cope with photooxidative stress when the balance between energy absorption and consumption is disturbed. Excess excitation energy in the photosystems (PSI and PSII) leads to the inhibition of photosynthesis via the production of various reactive oxygen species (ROS) at different spatial levels of the cell (Apel and Hirt, 2004;Asada, 2006;Van Breusegem and Dat, 2006). Both exposure to high light intensities and decreased CO 2 availability direct linear electron transfer toward the reduction of molecular oxygen, generating superoxide radicals (O 2 2. ) at PSI (the Mehler reaction). Superoxide dismutation generates hydrogen peroxide (H 2 O 2 ), which is detoxified in the chloroplast by ascorbate peroxidases. As such, this so-called water-water cycle participates in the dissipation of excess energy (Asada, 2006). Decreased CO 2 availability affects the first step in CO 2 fixation by shifting the carboxylation of Rubisco by the Rubisco carboxylase-oxygenase enzyme toward oxygenation, a process called photorespiration. This leads, through the action of glycolate oxidase, to peroxisomal H 2 O 2 production that is counteracted by catalases. Finally, when the intersystem electron carriers are overreduced, triplet excited P680 in the PSII reaction center as well as triplet chlorophylls in the light-harvesting antennae are produced, with the production of singlet oxygen ( 1 O 2 ) as a consequence (Krieger-Liszkay, 2005). In photosynthetic membranes, 1 O 2 ...

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“…4, we showed that light-induced 1 O 2 production in z2 leaves is a crucial factor for transverse variegation. It was previously reported that 1 O 2 is not only a cytotoxic molecule, but is also involved in the control of nuclear gene expression in plants (Kim et al, 2008). In addition to stress-related genes, 1 O 2 triggers ectopic expression of programmed cell death-related genes, leading to the formation of necrotic lesions in plant tissues (Danon et al, 2004;op den Camp et al, 2003).…”

Section: Altered Expression Ofmentioning

confidence: 99%

Leaf Variegation in the Rice zebra2 Mutant Is Caused by Photoperiodic Accumulation of Tetra-Cis-Lycopene and Singlet Oxygen

Han

Sakuraba

Koh

et al. 2012

Molecules and Cells

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In field conditions, the zebra2 (z2) mutant in rice (Oryza sativa) produces leaves with transverse pale-green/yellow stripes. It was recently reported that ZEBRA2 encodes carotenoid isomerase (CRTISO) and that low levels of lutein, an essential carotenoid for non-photochemical quenching, cause leaf variegation in z2 mutants. However, we found that the z2 mutant phenotype was completely suppressed by growth under continuous light (CL; permissive) conditions, with concentrations of chlorophyll, carotenoids and chloroplast proteins at normal levels in z2 mutants under CL. ]) accumulated to high levels in z2 mutants grown under short-day conditions (SD; alternate 10-h light/14-h dark; restrictive), but do not accumulate under CL conditions. However, the levels of lutein and zeaxanthin in z2 leaves were much lower than normal in both permissive CL and restrictive SD growth conditions, indicating that deficiency of these two carotenoids is not responsible for the leaf variegation phenotype. We found that the CRTISO substrate tetra-cis-lycopene accumulated during the dark periods under SD, but not under CL conditions. Its accumulation was also positively correlated with 1 O 2 levels generated during the light period, which consequently altered the expression of 1 O 2 -responsive and cell death-related genes in the variegated z2 leaves. Taking these results together, we propose that the z2 leaf variegation can be largely attributed to photoperiodic accumulation of tetra-cis-lycopene and generation of excessive 1 O 2 under natural day-night conditions.

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No single way to understand singlet oxygen signalling in plants

Cited by 144 publications

References 49 publications

The endoplasmic reticulum-associated degradation is necessary for plant salt tolerance

The endoplasmic reticulum-associated degradation is necessary for plant salt tolerance

Singlet Oxygen Is the Major Reactive Oxygen Species Involved in Photooxidative Damage to Plants

Leaf Variegation in the Rice zebra2 Mutant Is Caused by Photoperiodic Accumulation of Tetra-Cis-Lycopene and Singlet Oxygen

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