Comparative analysis of strategies to prepare electron sinks in aquatic photoautotrophs

Shimakawa, Ginga; Murakami, Akio; Niwa, Kyosuke; Matsuda, Yusuke; Wada, Ayumi; Miyake, Chikahiro

doi:10.1007/s11120-018-0522-z

Cited by 27 publications

(39 citation statements)

References 64 publications

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“…When photosynthesis is severely limited, where both photosynthesis and photorespiration functions are suppressed, P700 cannot be oxidized because the oxidation of P700* becomes the ratedetermining step in the P700 photo-oxidation reduction cycle. Furthermore, we found that inductions of the pmf and RISE oxidize P700 in PSI of the C3-plant wheat leaves [42,87]. A decrease in the intercellular partial pressure of CO 2 lowers the photosynthetic rate and increases the photorespiration rate.…”

Section: How Do the Accumulated Protons In The Lumenal Space And Elecmentioning

confidence: 84%

“…Furthermore, we found that inductions of the pmf and RISE oxidize P700 in PSI of the C3-plant wheat leaves [42,87]. A decrease in the intercellular partial pressure of CO2 lowers the photosynthetic rate and increases the photorespiration rate.…”

Section: How Do the Accumulated Protons In The Lumenal Space And Elecmentioning

confidence: 84%

“…The decrease in Jf (=Jg) shows the negative linear relationship with P700 + (Figure 5) [42,87]. The decrease in photosynthesis efficiency induces the oxidation of P700 in PSI.…”

Section: How Do the Accumulated Protons In The Lumenal Space And Elecmentioning

confidence: 97%

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Molecular Mechanism of Oxidation of P700 and Suppression of ROS Production in Photosystem I in Response to Electron-Sink Limitations in C3 Plants

Miyake

2020

Antioxidants

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Photosynthesis fixes CO2 and converts it to sugar, using chemical-energy compounds of both NADPH and ATP, which are produced in the photosynthetic electron transport system. The photosynthetic electron transport system absorbs photon energy to drive electron flow from Photosystem II (PSII) to Photosystem I (PSI). That is, both PSII and PSI are full of electrons. O2 is easily reduced to a superoxide radical (O2−) at the reducing side, i.e., the acceptor side, of PSI, which is the main production site of reactive oxygen species (ROS) in photosynthetic organisms. ROS-dependent inactivation of PSI in vivo has been reported, where the electrons are accumulated at the acceptor side of PSI by artificial treatments: exposure to low temperature and repetitive short-pulse (rSP) illumination treatment, and the accumulated electrons flow to O2, producing ROS. Recently, my group found that the redox state of the reaction center of chlorophyll P700 in PSI regulates the production of ROS: P700 oxidation suppresses the production of O2− and prevents PSI inactivation. This is why P700 in PSI is oxidized upon the exposure of photosynthesis organisms to higher light intensity and/or low CO2 conditions, where photosynthesis efficiency decreases. In this study, I introduce a new molecular mechanism for the oxidation of P700 in PSI and suppression of ROS production from the robust relationship between the light and dark reactions of photosynthesis. The accumulated protons in the lumenal space of the thylakoid membrane and the accumulated electrons in the plastoquinone (PQ) pool drive the rate-determining step of the P700 photo-oxidation reduction cycle in PSI from the photo-excited P700 oxidation to the reduction of the oxidized P700, thereby enhancing P700 oxidation.

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Section: How Do the Accumulated Protons In The Lumenal Space And Elecmentioning

confidence: 84%

Section: How Do the Accumulated Protons In The Lumenal Space And Elecmentioning

confidence: 84%

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Molecular Mechanism of Oxidation of P700 and Suppression of ROS Production in Photosystem I in Response to Electron-Sink Limitations in C3 Plants

Miyake

2020

Antioxidants

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“…We clarified that O 2 -evolving photosynthesis organisms suppress ROS generation in PSI through P700 oxidation [1,3,4,[7][8][9][10][11][12]. Shimakawa et al [4], in particular, revealed that a cyanobacterial strain that does not maintain a high level of P700 + suffers from rapid PSI oxidative damage under AL illumination.…”

Section: Introductionmentioning

confidence: 90%

Photorespiration Enhances Acidification of the Thylakoid Lumen, Reduces the Plastoquinone Pool, and Contributes to the Oxidation of P700 at a Lower Partial Pressure of CO2 in Wheat Leaves

Wada

Suzuki

Miyake

2020

Plants

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The oxidation of P700 in photosystem I (PSI) is a robust mechanism that suppresses the production of reactive oxygen species. We researched the contribution of photorespiration to the oxidation of P700 in wheat leaves. We analyzed the effects of changes in partial pressures of CO2 and O2 on photosynthetic parameters. The electron flux in photosynthetic linear electron flow (LEF) exhibited a positive linear relationship with an origin of zero against the dissipation rate (vH+) of electrochromic shift (ECS; ΔpH across thylakoid membrane), indicating that cyclic electron flow around PSI did not contribute to H+ usage in photosynthesis/photorespiration. The vH+ showed a positive linear relationship with an origin of zero against the H+ consumption rates in photosynthesis/photorespiration (JgH+). These two linear relationships show that the electron flow in LEF is very efficiently coupled with H+ usage in photosynthesis/photorespiration. Lowering the intercellular partial pressure of CO2 enhanced the oxidation of P700 with the suppression of LEF. Under photorespiratory conditions, the oxidation of P700 and the reduction of the plastoquinone pool were stimulated with a decrease in JgH+, compared to non-photorespiratory conditions. These results indicate that the reduction-induced suppression of electron flow (RISE) suppresses the reduction of oxidized P700 in PSI under photorespiratory conditions. Furthermore, under photorespiratory conditions, ECS was larger and H+ conductance was lower against JgH+ than those under non-photorespiratory conditions. These results indicate that photorespiration enhances RISE and ΔpH formation by lowering H+ conductance, both of which contribute to keeping P700 in a highly oxidized state.

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“…We utilized a nearly identical protocol as Shimakawa et al (2019) to measure redox kinetics of P700, the 166 reaction center chlorophyll of PSI, in dark acclimated E. timida and Acetabularia during dark-to-light 167 transition ( Figure 4B-D). In aerobic conditions, Acetabularia P700 redox kinetics during a high-light pulse 168 followed the scheme where P700 is first strongly oxidized due to PSI electron donation to downstream 169 electron acceptors such as ferredoxin, and re-reduced by electrons from the upstream electron transfer 170 chain ( Figure 4B).…”

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confidence: 99%

Photosynthetic sea slugs inflict protective changes to the light reactions of the chloroplasts they steal from algae

Havurinne

Tyystjärvi

2020

Preprint

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7Sacoglossan sea slugs are able to maintain functional chloroplasts inside their own cells, and 8 mechanisms that allow preservation of the chloroplasts are unknown. We found that the slug Elysia 9 timida inflicts changes to the photosynthetic light reactions of the chloroplasts it steals from the alga 10 Acetabularia acetabulum. Working with a large continuous laboratory culture of both the slugs (>500 11 individuals) and their prey algae, we show that the plastoquinone pool of slug chloroplasts remains 12 oxidized, which can suppress reactive oxygen species formation. Slug chloroplasts also rapidly build up a 13 strong proton motive force upon a dark-to-light transition, which helps them to rapidly switch on 14 photoprotective non-photochemical quenching of excitation energy. Finally, our results suggest that 15 chloroplasts inside E. timida rely on flavodiiron proteins as electron sinks during rapid changes in light 16 intensity. These photoprotective mechanisms are expected to contribute to the long-term functionality 17 of the chloroplasts inside the slugs. 18 2014) and E. chlorotica (Rumpho et al., 2011), but still today most research is conducted on animals 55 caught from the wild. We have grown the sea slug E. timida and its prey Acetabularia in our lab for 56 several years ( Figure 1). As suggested by Schmitt et al. (2014), E. timida is an attractive model organism 57 for photosynthetic sea slugs because it is easy to culture with relatively low costs ( Figure 1E). A constant 58 supply of slugs has opened a plethora of experimental setups yet to be tested, one of the more exciting 59 ones being the case of red morphotypes of both E. timida and Acetabularia ( Figure 1C,D). Red 60 morphotypes of E. timida and Acetabularia were first described by González-Wangüemert et al. (2006) 61 and later shown to be due to accumulation of an unidentified carotenoid during cold/high-light 62 acclimation of the algae that were then eaten by E. timida (Costa et al., 2012). The red morphotypes 63 provide a visual proof that the characteristics of the kleptoplasts inside E. timida can be modified by 64 acclimating their feedstock to different environmental conditions. 65 4 We optimized a completely new set of biophysical methods to study photosynthesis in the sea slugs and 66 found differences in photosynthetic electron transfer reactions between E. timida and Acetabularia 67 grown in varying culture conditions. The most dramatic differences between the slugs and their prey 68 were noticed in PSII electron transfer of the red morphotype E. timida ( Figure 1C) and Acetabularia 69 ( Figure 1D). In addition to measuring chlorophyll a fluorescence decay kinetics, we also measured 70 fluorescence induction kinetics, PSI electron transfer and formation of proton motive force during dark 71 to light transition. Our results suggest that dark reduction of the plastoquinone (PQ) pool, a reserve of 72 central electron carriers of the photosynthetic electron transfer chain, is weak in the slugs compared to 73 the algae, and that a ...

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Comparative analysis of strategies to prepare electron sinks in aquatic photoautotrophs

Cited by 27 publications

References 64 publications

Molecular Mechanism of Oxidation of P700 and Suppression of ROS Production in Photosystem I in Response to Electron-Sink Limitations in C3 Plants

Molecular Mechanism of Oxidation of P700 and Suppression of ROS Production in Photosystem I in Response to Electron-Sink Limitations in C3 Plants

Photorespiration Enhances Acidification of the Thylakoid Lumen, Reduces the Plastoquinone Pool, and Contributes to the Oxidation of P700 at a Lower Partial Pressure of CO2 in Wheat Leaves

Photosynthetic sea slugs inflict protective changes to the light reactions of the chloroplasts they steal from algae

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