Production and diffusion of chloroplastic H2O2 and its implication to signalling

Mubarakshina, Maria; Иванов, Б. Н.; Naydov, Ilya A.; Hillier, Warwick; Badger, Murray R.; Krieger‐Liszkay, Anja

doi:10.1093/jxb/erq171

Cited by 187 publications

(119 citation statements)

References 68 publications

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“…Chloroplast (approximately 0.01 mg Chl ml −1 ) ROS scavenging by nanoparticles was quantified by the conversion of the membrane permeant 2 , 7 -dichlorodihydrofluorescein diacetate (H 2 DCFDA, 0.6 mg ml −1 ) to the fluorescent 2 , 7 -dichlorofluorescein (DCF; ref. 35). The effect of nanoparticles on superoxide concentration was determined by the reduction of 2,3-bis (2-methoxy-4-nitro-5-sulphophenyl)-2H-tetrazolium-5-carboxanilide sodium salt (XTT, 0.06 mg ml −1 ) dye (Sigma Aldrich) in the presence of superoxide as in previous studies on plant cells 43,44 .…”

Section: Methodsmentioning

confidence: 99%

“…4f). H 2 DCFDA oxidation to DCF by a range of free radicals such as hydrogen peroxide, superoxide, NO and peroxidases has been applied to monitor ROS generated by extracted chloroplasts 35 . Under continuous illumination for six hours, chloroplasts interfaced with 6 µM PAA-NC showed a substantial 28.7% reduction in ROS relative to chloroplasts without nanoparticles.…”

Section: Nanoparticle Enhancement Of Chloroplast Ros Scavengingmentioning

confidence: 99%

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Plant nanobionics approach to augment photosynthesis and biochemical sensing

et al. 2014

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The interface between plant organelles and non-biological nanostructures has the potential to impart organelles with new and enhanced functions. Here, we show that single-walled carbon nanotubes (SWNTs) passively transport and irreversibly localize within the lipid envelope of extracted plant chloroplasts, promote over three times higher photosynthetic activity than that of controls, and enhance maximum electron transport rates. The SWNT-chloroplast assemblies also enable higher rates of leaf electron transport in vivo through a mechanism consistent with augmented photoabsorption. Concentrations of reactive oxygen species inside extracted chloroplasts are significantly suppressed by delivering poly(acrylic acid)-nanoceria or SWNT-nanoceria complexes. Moreover, we show that SWNTs enable near-infrared fluorescence monitoring of nitric oxide both ex vivo and in vivo, thus demonstrating that a plant can be augmented to function as a photonic chemical sensor. Nanobionics engineering of plant function may contribute to the development of biomimetic materials for light-harvesting and biochemical detection with regenerative properties and enhanced e ciency.

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Section: Methodsmentioning

confidence: 99%

Section: Nanoparticle Enhancement Of Chloroplast Ros Scavengingmentioning

confidence: 99%

Plant nanobionics approach to augment photosynthesis and biochemical sensing

et al. 2014

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“…Hydrogen peroxide was detected by resorufin (modified from ref. 67). Leaf discs of the same size were rapidly frozen and ground in liquid nitrogen and extracted in 50 mM potassium phosphate buffer (pH 7.5).…”

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

confidence: 99%

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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“…While electron transfer produces superoxide (O 2 2 ) radical ions that subsequently can be converted to hydrogen peroxide (H 2 O 2 ) or hydroxyl radicals, energy transfer to molecular oxygen results in the generation of singlet oxygen ( 1 O 2 ; Apel and Hirt, 2004). Plant cells produce ROS as unavoidable byproducts of aerobic metabolism, with the photosynthetic electron transport chain being a major source (Mullineaux and Karpinski, 2002;Foyer and Noctor, 2003;Wagner et al, 2004;Mubarakshina et al, 2010). Efficient enzymatic and nonenzymatic detoxification mechanisms are in place to prevent accumulation of excessive amounts of ROS and the resultant oxidative damage to biomolecules, especially proteins and lipids (op den Camp et al, 2003;Apel and Hirt, 2004;Henmi et al, 2004;Scheller and Haldrup, 2005;Krieger-Liszkay and Trebst, 2006).…”

Section: Introductionmentioning

confidence: 99%

A Mediator of Singlet Oxygen Responses in Chlamydomonas reinhardtii and Arabidopsis Identified by a Luciferase-Based Genetic Screen in Algal Cells

2013

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ORCID ID: 0000-0001-7502-6940 (R.B.).All cells produce reactive oxygen species (ROS) as by-products of their metabolism. In addition to being cytotoxic, ROS act as regulators of a wide range of developmental and physiological processes. Little is known about the molecular mechanisms underlying the perception of ROS and initiation of cellular responses in eukaryotes. Using the unicellular green alga Chlamydomonas reinhardtii, we developed a genetic screen for early components of singlet oxygen signaling. Here, we report the identification of a small zinc finger protein, METHYLENE BLUE SENSITIVITY (MBS), that is required for induction of singlet oxygendependent gene expression and, upon oxidative stress, accumulates in distinct granules in the cytosol. Loss-of-function mbs mutants produce singlet oxygen but are unable to fully respond to it at the level of gene expression. Knockout or knockdown of the homologous genes in the higher plant model Arabidopsis thaliana results in mutants that are hypersensitive to photooxidative stress, whereas overexpression produces plants with elevated stress tolerance. Together, our data indicate an important and evolutionarily conserved role of the MBS protein in ROS signaling and provide a strategy for engineering stress-tolerant plants.

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Production and diffusion of chloroplastic H2O2 and its implication to signalling

Cited by 187 publications

References 68 publications

Plant nanobionics approach to augment photosynthesis and biochemical sensing

Plant nanobionics approach to augment photosynthesis and biochemical sensing

Activation of cyclic electron flow by hydrogen peroxide in vivo

A Mediator of Singlet Oxygen Responses in Chlamydomonas reinhardtii and Arabidopsis Identified by a Luciferase-Based Genetic Screen in Algal Cells

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