Generation of Hydrogen Peroxide in Chloroplasts of Arabidopsis Overexpressing Glycolate Oxidase as an Inducible System to Study Oxidative Stress

Fahnenstich, Holger; Scarpeci, Telma E.; Valle, Estela M.; Flügge, Ulf‐Ingo; Maurino, Verónica G.

doi:10.1104/pp.108.126789

Cited by 136 publications

(145 citation statements)

References 56 publications

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“…These "GO" plants produce H 2 O 2 in the chloroplast by the oxidation of glycolate upon activation of photorespiration, and are thus useful tools for studying changes in photosynthetic activities induced by the metabolic generation of H 2 O 2 in the chloroplast. We focus mainly on the GO5 line because of its relatively high and robust H 2 O 2 production rates (38,39) (Fig. S1), but we obtained similar results with other lines (discussed below).…”

Section: Effects Of H 2 O 2 Production By Plants Expressing Glycolatesupporting

confidence: 73%

“…Moreover, as shown in Figs. S3-S5, the qualitative increase in H 2 O 2 content of GO5, GO16, and GO20 and estimates of increased CEF indicate a positive relationship between the extent of H 2 O 2 production in multiple GO lines with differing levels of GO activity (38).…”

Section: Effects Of H 2 O 2 Production By Plants Expressing Glycolatementioning

confidence: 99%

“…We next tested whether CEF is activated when intracellular H 2 O 2 production is rapidly induced. To achieve this, we compared photosynthetic properties of Col-0 and transgenic Arabidopsis plants that express glycolate oxidase (GO) targeted to the chloroplast (38). These "GO" plants produce H 2 O 2 in the chloroplast by the oxidation of glycolate upon activation of photorespiration, and are thus useful tools for studying changes in photosynthetic activities induced by the metabolic generation of H 2 O 2 in the chloroplast.…”

Section: Effects Of H 2 O 2 Production By Plants Expressing Glycolatementioning

confidence: 99%

“…However, in the GO plants glyoxylate, produced by the glycolate oxidase in the chloroplasts, also accumulates and may induce CEF. To test this possibility we measured CEF in GO5 plants also coexpressing malate synthase targeted to the chloroplast (GOMS1 and GOMS14 lines), which can further convert glyoxylate to malate (38). We do not expect large effects of increased malate production because it is already produced in the chloroplast, readily exported through the malate shunt, and subsequently oxidized by the mitochondria.…”

Section: Effects Of H 2 O 2 Production By Plants Expressing Glycolatementioning

confidence: 99%

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Activation of cyclic electron flow by hydrogen peroxide in vivo

Strand

Livingston

Satoh-Cruz

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

119

116

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Cyclic electron flow (CEF) around photosystem I is thought to balance the ATP/NADPH energy budget of photosynthesis, requiring that its rate be finely regulated. The mechanisms of this regulation are not well understood. We observed that mutants that exhibited constitutively high rates of CEF also showed elevated production of H 2 O 2 . We thus tested the hypothesis that CEF can be activated by H 2 O 2 in vivo. CEF was strongly increased by H 2 O 2 both by infiltration or in situ production by chloroplastlocalized glycolate oxidase, implying that H 2 O 2 can activate CEF either directly by redox modulation of key enzymes, or indirectly by affecting other photosynthetic processes. CEF appeared with a half time of about 20 min after exposure to H 2 O 2 , suggesting activation of previously expressed CEF-related machinery. H 2 O 2 -dependent CEF was not sensitive to antimycin A or loss of PGR5, indicating that increased CEF probably does not involve the PGR5-PGRL1 associated pathway. In contrast, the rise in CEF was not observed in a mutant deficient in the chloroplast NADPH:PQ reductase (NDH), supporting the involvement of this complex in CEF activated by H 2 O 2 . We propose that H 2 O 2 is a missing link between environmental stress, metabolism, and redox regulation of CEF in higher plants. I n oxygenic photosynthesis, linear electron flow (LEF) is the process by which light energy is captured to drive the extraction of electrons and protons from water and transfer them through a system of electron carriers to reduce NADPH. LEF is coupled to proton translocation into the thylakoid lumen, generating an electrochemical gradient of protons ðΔμ H +Þ or proton motive force (pmf). The pmf drives the synthesis of ATP to power the reactions of the Calvin-Benson-Bassham (CBB) cycle and other essential metabolic processes in the chloroplast. The pmf is also a key regulator of photosynthesis in that it activates the photoprotective q E response to dissipate excess light energy and downregulates electron transfer by controlling the rate of oxidation of plastoquinol at the cytochrome b 6 f complex (b 6 f), thus preventing the buildup of reduced intermediates (1, 2).LEF results in the transfer or deposition into the lumen of three protons for each electron transferred through PSII, plastoquinone (PQ), b 6 f, plastocyanin, and photosystem I (PSI) to ferredoxin (Fd). The synthesis of one ATP is thought to require the passage of 4.67 protons through the ATP synthase, so that LEF should produce a ratio of ATP/NADPH of about 1.33; this ratio is too low to sustain the CBB cycle or supply ATP required for translation, protein transport, or other ATP-dependent processes (3). In addition, the relative demands for ATP and NADPH can change dramatically depending on environmental, developmental, and other factors, leading to rapid energy imbalances that require dynamical regulation of ATP/NADPH balance.Several alternative electron flow pathways in the chloroplast have been proposed to augment ATP production, thus balancing the ATP/NADPH ...

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Section: Effects Of H 2 O 2 Production By Plants Expressing Glycolatesupporting

confidence: 73%

Section: Effects Of H 2 O 2 Production By Plants Expressing Glycolatementioning

confidence: 99%

Section: Effects Of H 2 O 2 Production By Plants Expressing Glycolatementioning

confidence: 99%

Section: Effects Of H 2 O 2 Production By Plants Expressing Glycolatementioning

confidence: 99%

See 2 more Smart Citations

Activation of cyclic electron flow by hydrogen peroxide in vivo

Strand

Livingston

Satoh-Cruz

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

119

116

View full text Add to dashboard Cite

show abstract

“…Moreover, changes in the accumulation of small organic acids could also be due to a perturbation of cell metabolism. Thus, changes in the activity of enzymes such as glycolate oxidase could directly affect constitutive H 2 O 2 levels (Noctor et al, 2002;Fahnenstich et al, 2008).…”

Section: Knockdown Of Prx33/prx34 Leads To a Differential Accumulatiomentioning

confidence: 99%

A Peroxidase-Dependent Apoplastic Oxidative Burst in Cultured Arabidopsis Cells Functions in MAMP-Elicited Defense

O’Brien

Daudi²,

Finch³

et al. 2012

Plant Physiology

189

152

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Perception by plants of so-called microbe-associated molecular patterns (MAMPs) such as bacterial flagellin, referred to as pattern-triggered immunity, triggers a rapid transient accumulation of reactive oxygen species (ROS). We previously identified two cell wall peroxidases, PRX33 and PRX34, involved in apoplastic hydrogen peroxide (H 2 O 2 ) production in Arabidopsis (Arabidopsis thaliana). Here, we describe the generation of Arabidopsis tissue culture lines in which the expression of PRX33 and PRX34 is knocked down by antisense expression of a heterologous French bean (Phaseolus vulgaris) peroxidase cDNA construct. Using these tissue culture lines and two inhibitors of ROS generation, azide and diphenylene iodonium, we found that perxoxidases generate about half of the H 2 O 2 that accumulated in response to MAMP treatment and that NADPH oxidases and other sources such as mitochondria account for the remainder of the ROS. Knockdown of PRX33/PRX34 resulted in decreased expression of several MAMP-elicited genes, including MYB51, CYP79B2, and CYP81F2. Similarly, proteomic analysis showed that knockdown of PRX33/PRX34 led to the depletion of various MAMP-elicited defense-related proteins, including the two cysteine-rich peptides PDF2.2 and PDF2.3. Knockdown of PRX33/PRX34 also led to changes in the cell wall proteome, including increases in enzymes involved in cell wall remodeling, which may reflect enhanced cell wall expansion as a consequence of reduced H 2 O 2 -mediated cell wall cross-linking. Comparative metabolite profiling of a CaCl 2 extract of the PRX33/PRX34 knockdown lines showed significant changes in amino acids, aldehydes, and keto acids but not fatty acids and sugars. Overall, these data suggest that PRX33/PRX34-generated ROS production is involved in the orchestration of patterntriggered immunity in tissue culture cells.

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Transcriptome and phenotyping analyses support a role for chloroplast sigma factor 2 in red‐light‐dependent regulation of growth, stress, and photosynthesis

Strand

Kramer

et al. 2018

Plant Direct

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Sigma factor (SIG) proteins contribute to promoter specificity of the plastid‐encoded RNA polymerase during chloroplast genome transcription. All six members of the SIG family, that is, SIG1–SIG6, are nuclear‐encoded proteins targeted to chloroplasts. Sigma factor 2 (SIG2) is a phytochrome‐regulated protein important for stoichiometric control of the expression of plastid‐ and nuclear‐encoded genes that impact plastid development and plant growth and development. Among SIG factors, SIG2 is required not only for transcription of chloroplast genes (i.e., anterograde signaling), but also impacts nuclear‐encoded, photosynthesis‐related, and light signaling‐related genes (i.e., retrograde signaling) in response to plastid functional status. Although SIG2 is involved in photomorphogenesis in Arabidopsis, the molecular bases for its role in light signaling that impacts photomorphogenesis and aspects of photosynthesis have only recently begun to be investigated. Previously, we reported that SIG2 is necessary for phytochrome‐mediated photomorphogenesis specifically under red (R) and far‐red light, thereby suggesting a link between phytochromes and nuclear‐encoded SIG2 in light signaling. To explore transcriptional roles of SIG2 in R‐dependent growth and development, we performed RNA sequencing analysis to compare gene expression in sig2‐2 mutant and Col‐0 wild‐type seedlings at two developmental stages (1‐ and 7‐day). We identified a subset of misregulated genes involved in growth, hormonal cross talk, stress responses, and photosynthesis. To investigate the functional relevance of these gene expression analyses, we performed several comparative phenotyping tests. In these analyses, strong sig2 mutants showed insensitivity to bioactive GA3, high intracellular levels of hydrogen peroxide (H2O2) indicative of a stress response, and specific defects in photosynthesis, including elevated levels of cyclic electron flow (CEF) and nonphotochemical quenching (NPQ). We demonstrated that SIG2 regulates a broader range of physiological responses at the molecular level than previously reported, with specific roles in red‐light‐mediated photomorphogenesis.

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Generation of Hydrogen Peroxide in Chloroplasts of Arabidopsis Overexpressing Glycolate Oxidase as an Inducible System to Study Oxidative Stress

Cited by 136 publications

References 56 publications

Activation of cyclic electron flow by hydrogen peroxide in vivo

Activation of cyclic electron flow by hydrogen peroxide in vivo

A Peroxidase-Dependent Apoplastic Oxidative Burst in Cultured Arabidopsis Cells Functions in MAMP-Elicited Defense

Transcriptome and phenotyping analyses support a role for chloroplast sigma factor 2 in red‐light‐dependent regulation of growth, stress, and photosynthesis

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