Activation of cyclic electron flow by hydrogen peroxide in vivo

Abstract

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 ...

Redox- and Reactive Oxygen Species-Dependent Signaling into and out of the Photosynthesizing Chloroplast

“…Cyclic electron flow (CEF) via ferredoxin-dependent quinone reductase is sensitive to antimycin A and is stimulated by thiol-reducing conditions, with a redox midpoint potential of 2306 mV (Strand et al, 2016). In a converse manner, the NADPH dehydrogenase-dependent CEF pathway is activated by oxidizing conditions in vivo after H 2 O 2 infiltration or in mutants with enhanced production of chloroplast H 2 O 2 (Strand et al, 2015). In contrast to these observations, TRX m4 appears to inhibit CEF, based on the analysis of mutants affected in TRX m4 (Courteille et al, 2013).…”

“…O 2 $ 2 /H 2 O 2 is then generated by the Mehler reaction, and the H 2 O 2 is decomposed by APX, PRX, and GPX. However, above a certain threshold of accumulation, H 2 O 2 may oxidize the thiols, rendering enzymes of the Calvin cycle inactive and simultaneously activating the NDH-dependent CEF (Strand et al, 2015).…”

Systemic induction of photosynthesis via illumination of the shoot apex is mediated by phytochrome B

“…Phytohormones such as brassinosteroids enhance CO 2 assimilation rates in an RBOH-dependent manner in plants (Jiang et al, 2012). Moreover, H 2 O 2 activates CEF around PSI in order to increase CO 2 assimilation (Strand et al, 2015). Auxin and brassinosteroids have overlapping functions in relation to the control of gene expression.…”

“…CEF is particularly sensitive to the reductionoxidation (redox) status of the chloroplast, which in turn is responsive to cellular redox homeostasis. Oxidants such as hydrogen peroxide (H 2 O 2 ), which are produced by pseudocyclic electron flow in the chloroplasts, play a crucial role in the activation of CEF through modulation of the activity of the NADPHplastoquinone reductase complex (Strand et al, 2015). Hormone-mediated generation of H 2 O 2 also can stimulate CO 2 assimilation (Jiang et al, 2012).…”

Dinitrogenase-Driven Photobiological Hydrogen Production Combats Oxidative Stress in Cyanothece sp. Strain ATCC 51142

“…These pathways are important to the cell's ability to protect itself from damage associated with redox imbalance (6)(7)(8)(9). The signaling mechanisms that instigate alternative electron flow (AEF) processes to protect the cell from redox imbalance are ill defined (10). We hypothesize that redox-driven processes may provide the signal for multiple AEFs, allowing for flexibility of electron flow in the cell's pursuit to regulate redox homeostasis.…”