The thylakoid proton motive force in vivo. Quantitative, non-invasive probes, energetics, and regulatory consequences of light-induced pmf

Takizawa, Kayoko; Cruz, Jeffrey A.; Kanazawa, Atsuko; Kramer, David

doi:10.1016/j.bbabio.2007.07.006

Cited by 233 publications

(245 citation statements)

References 67 publications

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“…Increased CEF in GO5 was further indicated by a complementary approach comparing estimated light-driven proton flux (v H +) as a function of LEF (47,48). As shown in Fig.…”

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.

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119

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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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“…Increased CEF in GO5 was further indicated by a complementary approach comparing estimated light-driven proton flux (v H +) as a function of LEF (47,48). As shown in Fig.…”

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.

Self Cite

119

116

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“…4A) and at pH 5.5 ( Fig. 4B), which approximately corresponds to the luminal pH in photosynthetic organisms under illumination (26,27 Table S1). Comparison of Fig.…”

Section: Significancementioning

confidence: 99%

Mobile hydrogen carbonate acts as proton acceptor in photosynthetic water oxidation

Koroidov

Shevela

Shutova

et al. 2014

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

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Cyanobacteria, algae, and plants oxidize water to the O 2 we breathe, and consume CO 2 during the synthesis of biomass. Although these vital processes are functionally and structurally well separated in photosynthetic organisms, there is a long-debated role for CO 2 /HCO − 3 in water oxidation. Using membrane-inlet mass spectrometry we demonstrate that HCO − 3 acts as a mobile proton acceptor that helps to transport the protons produced inside of photosystem II by water oxidation out into the chloroplast's lumen, resulting in a light-driven production of O 2 and CO 2 . Depletion of HCO − 3 from the media leads, in the absence of added buffers, to a reversible down-regulation of O 2 production by about 20%. These findings add a previously unidentified component to the regulatory network of oxygenic photosynthesis and conclude the more than 50-y-long quest for the function of CO 2 / HCO − 3 in photosynthetic water oxidation.O xygenic photosynthesis in cyanobacteria, algae, and higher plants leads to the reduction of atmospheric CO 2 to energy-rich carbohydrates. The electrons needed for this process are extracted in a cyclic, light-driven process from water that is split into dioxygen (O 2 ) and protons. This reaction is catalyzed by a penta-μ-oxo bridged tetra-manganese calcium cluster (Mn 4 CaO 5 ) within the oxygen-evolving complex (OEC) of photosystem II (PSII) (1-4). The possible roles of inorganic carbon, C i ðC i = CO 2 ; H 2 CO 3 ; HCO − 3 ; CO 2− 3 Þ, in this process have been a controversial issue ever since Otto Warburg and Günter Krippahl (5) reported in 1958 that oxygen evolution by PSII strictly depends on CO 2 and therefore has to be based on the photolysis of H 2 CO 3 ("Kohlensäure") and not of water. These first experiments were indirect and, as became apparent later, were wrongly interpreted (6-8). Several research groups followed up on these initial results and identified two possible sites of C i interaction within PSII (reviewed in refs. 9-12). Functional and spectroscopic studies showed that HCO − 3 facilitates the reduction of the secondary plastoquinone electron acceptor (Q B ) of PSII by participating in the protonation of Q 2− B . Binding of HCO − 3 (or CO 2− 3 ) to the nonheme Fe between the quinones Q A and Q B was recently confirmed by X-ray crystallography (3,13,14). Despite this functional role at the acceptor side, the very tight binding of HCO − 3 to this site makes it impossible for the activity of PSII to be affected by changing the C i level of the medium; instead inhibitors such as formate need to be added to induce the acceptor-side effect (15). Consequently, the watersplitting electron-donor side of PSII has also been studied intensively (for recent reviews, see refs. 11 and 12). Although a tight binding of C i near the Mn 4 CaO 5 cluster is excluded on the basis of X-ray crystallography (3, 14), FTIR spectroscopy (16), and mass spectrometry (17, 18), the possibility that a weakly bound HCO − 3 affects the activity of PSII at the donor side remains a viable option (reviewed i...

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“…For intact plants illuminated at saturating light intensities, the pH in the lumen compartment and thus at the donor side of PSII has been estimated to be 5.7 Ϯ 0.5 (45). Accordingly, two steps in the transition S 3 3 S 0 ϩ O 2 work close to their respective thermodynamic limitations, whereas a clear free energy surplus (⌬G H , Equation 2) characterizes all other S-state transitions.…”

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confidence: 99%

“…However, the comparatively large volume and buffer capacity of the stroma space likely prevent a pronounced increase in the stroma pH.) To compensate, plants apparently control their trans-thylakoid ion fluxes such that a major fraction of the proton-motive force stems from the membrane voltage formed upon illumination (45,46). Moreover, any mechanism of physiological relevance for the pH-dependent down-regulation of PSII (47,48) needs to have a threshold pH Ͼ5 (49) to be effective.…”

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confidence: 99%

Thermodynamic Limitations of Photosynthetic Water Oxidation at High Proton Concentrations

Zaharieva¹,

Wichmann

Dau

2011

Journal of Biological Chemistry

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In oxygenic photosynthesis, solar energy drives the oxidation of water catalyzed by a Mn 4 Ca complex bound to the proteins of Photosystem II. Four protons are released during one turnover of the water oxidation cycle (S-state cycle), implying thermodynamic limitations at low pH. For proton concentrations ranging from 1 nM (pH 9) to 1 mM (pH 3), we have characterized the low-pH limitations using a new experimental approach: a specific pH-jump protocol combined with time-resolved measurement of the delayed chlorophyll fluorescence after nanosecond flash excitation. Effective pK values were determined for low-pH inhibition of the light-induced S-state transitions: pK 1 ‫؍‬ 3.3 ؎ 0.3, pK 2 ‫؍‬ 3.5 ؎ 0.2, and pK 3 ≈ pK 4 ‫؍‬ 4.6 ؎ 0.2. Alkaline inhibition was not observed. An extension of the classical Kok model facilitated assignment of these four pK values to specific deprotonation steps in the reaction cycle. Our results provide important support to the extended S-state cycle model and criteria needed for assessment of quantum chemical calculations of the mechanism of water oxidation. They also imply that, in intact organisms, the pH in the lumen compartment can hardly drop below 5, thereby limiting the ⌬pH contribution to the driving force of ATP synthesis.Light-driven water oxidation by plants, algae, and cyanobacteria is a pivotal process in biological solar energy conversion (1). Its evolutionary development, ϳ3.5 billion years ago, has boosted life on Earth by facilitating the efficient use of water as a source of electrons and protons for the synthesis of energystoring carbohydrates and biomass in general. The long-standing scientific interest in photosynthetic water oxidation has recently been invigorated by the vision of future technological systems that, akin to plants and cyanobacteria, use water as a substrate for light-driven formation of energy-rich and storable compounds (H 2 or other fuel materials) (2-5). We believe that insights into energetics and reaction mechanisms of the natural paragon could provide inspiration and guidelines for the development of new technologies (6 -8). However, the biological process is understood only insufficiently (9).In oxygenic photosynthesis, solar energy drives the oxidation of water and the accumulation of "energized" electrons by reduction of quinones (Fig.

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The thylakoid proton motive force in vivo. Quantitative, non-invasive probes, energetics, and regulatory consequences of light-induced pmf

Cited by 233 publications

References 67 publications

Activation of cyclic electron flow by hydrogen peroxide in vivo

Activation of cyclic electron flow by hydrogen peroxide in vivo

Mobile hydrogen carbonate acts as proton acceptor in photosynthetic water oxidation

Thermodynamic Limitations of Photosynthetic Water Oxidation at High Proton Concentrations

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