In Vivo Changes of the Oxidation-Reduction State of NADP and of the ATP/ADP Cellular Ratio Linked to the Photosynthetic Activity in <i>Chlamydomonas reinhardtii</i>

Forti, Giorgio; Furia, Alberto; Bombelli, Paolo; Finazzi, Guido

doi:10.1104/pp.102.018861

Cited by 56 publications

(51 citation statements)

References 53 publications

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“…Conversely, our observation that the ATP levels in dum22 stt7-9 cells cannot be decreased further below the levels seen in dum22 cells ( Table 1) strongly suggests that below a threshold level, ATP becomes limiting for photosynthetic growth. This possibility is in agreement with previous data (35). Thus, the limited energy supply in the double mutant at low light probably is consumed in intracellular metabolism at the expense of biomass production and cell division.…”

Section: Discussionsupporting

confidence: 93%

Impaired respiration discloses the physiological significance of state transitions in Chlamydomonas

Cardol

Alric

Girard‐Bascou

et al. 2009

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

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119

104

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State transitions correspond to a major regulation process for photosynthesis, whereby chlorophyll protein complexes responsible for light harvesting migrate between photosystem II and photosystem I in response to changes in the redox poise of the intersystem electron carriers. Here we disclose their physiological significance in Chlamydomonas reinhardtii using a genetic approach. Using single and double mutants defective for state transitions and/or mitochondrial respiration, we show that photosynthetic growth, and therefore biomass production, critically depends on state transitions in respiratory-defective conditions. When extra ATP cannot be provided by respiration, enhanced photosystem I turnover elicited by transition to state 2 is required for photosynthetic activity. Concomitant impairment of state transitions and respiration decreases the overall yield of photosynthesis, ultimately leading to reduced fitness. We thus provide experimental evidence that the combined energetic contributions of state transitions and respiration are required for efficient carbon assimilation in this alga.cyclic electron flow ͉ photosynthesis ͉ energetic metabolism S tate transitions (ST) are a short-term photosynthetic acclimation process that controls the reversible association of the photosystem II (PSII) antenna protein complex (LHCII) with either PSII (in state 1) or photosystem I (PSI) (in state 2) (1-3). This process relies on the reversible LHCII phosphorylation involving the membrane-bound protein kinase Stt7-STN7, which recently has been identified in Chlamydomonas reinhardtii and Arabidopsis thaliana (4, 5). Phosphorylation changes lead to the migration of a fraction of the antenna between the PSII-enriched membrane domains and the PSI-enriched membrane domains within the thylakoids in plant and algal chloroplasts (3, 6).STs first were observed in unicellular green algae and originally were described as a mechanism linking the redox poise of the intersystem electron carriers to changes in the absorption capacity of the photosystems (3). Reduction of the plastoquinone (PQ) pool upon increased PSII sensitization activates the kinase via the cytochrome b 6 f complex (7). Conversely, upon increased PSI sensitization, PQH 2 oxidation inactivates the kinase. P i -LHCII then is dephosphorylated by a phosphatase (3) whose biochemical nature and regulation remain elusive.In plants, STs are of limited amplitude, involving Ϸ20% of LHCII (8). Their occurrence probably is not essential for plant survival, as suggested by the very limited effects on growth (4, 9-11) and on fitness (12) of mutations preventing STs in Arabidopsis. One of these mutants shows a marked phenotype only under a very particular regimen of fluctuating light (4). In Chlamydomonas, STs involve a larger fraction of PSII antenna than in plants, with Ϸ80% of PSII antennae being involved in this phenomenon (13), including monomeric LHCII (14). The very large redistribution of light-harvesting complexes with STs in this alga is difficult to reconcile with a role...

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Section: Discussionsupporting

confidence: 93%

Impaired respiration discloses the physiological significance of state transitions in Chlamydomonas

Cardol

Alric

Girard‐Bascou

et al. 2009

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

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119

104

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“…The calculated K m ATP (600 M) is higher than that observed for p72 (27) or the bacterial helicases CrhC (20) and DbpA (28) but similar to that reported for yeast eIF4A (29). These values would not be expected to inhibit CrhR activity, because ATP levels do not vary significantly during light-dark transitions (30). The observed specific activity of 500 min Ϫ1 is at the upper range reported for helicases, similar to DbpA (28) and Ded1p (21).…”

Section: Figsupporting

confidence: 76%

RNA Structural Rearrangement via Unwinding and Annealing by the Cyanobacterial RNA Helicase, CrhR

Chamot

Colvin

Kujat-Choy³

et al. 2005

Journal of Biological Chemistry

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Rearrangement of RNA secondary structure is crucial for numerous biological processes. RNA helicases participate in these rearrangements through the unwinding of duplex RNA. We report here that the redox-regulated cyanobacterial RNA helicase, CrhR, is a bona fide RNA helicase possessing both RNA-stimulated ATPase and bidirectional ATP-stimulated RNA helicase activity. The processivity of the unwinding reaction appears to be low, because RNA substrates containing duplex regions of 41 bp are not unwound. CrhR also catalyzes the annealing of complementary RNA into intermolecular duplexes. Uniquely and in contrast to other proteins that perform annealing, the CrhR-catalyzed reactions require ATP hydrolysis. Through a combination of the unwinding and annealing activities, CrhR also catalyzes RNA strand exchange resulting in the formation of RNA secondary structures that are too stable to be resolved by helicase activity. RNA strand exchange most probably occurs through the CrhR-dependent formation and resolution of an RNA branch migration structure. Demonstration that another cyanobacterial RNA helicase, CrhC, does not catalyze annealing indicates that this activity is not a general biochemical characteristic of RNA helicases. Biochemically, CrhR resembles RecA and related proteins that catalyze strand exchange and branch migration on DNA substrates, a characteristic that is reflected in the recently reported structural similarities between these proteins. The data indicate the potential for CrhR to catalyze dynamic RNA secondary structure rearrangements through a combination of RNA helicase and annealing activities.The ability of organisms to rearrange nucleic acid secondary structure is crucial for cellular function and is catalyzed by a diverse range of proteins or protein complexes that facilitate nucleic acid annealing and unwinding. Two protein families, nucleic acid-binding proteins and helicases, catalyze these reactions. RNA-binding proteins are structurally unrelated to helicases (1, 2) and rearrange RNA secondary structure through chaperone-mediated annealing or unwinding in ATPindependent reactions (3, 4). Helicases have been classified into five major groups based on characteristic amino acid motifs with the two largest families, superfamilies 1 and 2, composed of RNA and DNA helicases (5). The other helicase families include proteins possessing fewer conserved motifs and having different substrate specificities.Biochemically, helicases function as ATP-driven molecular motors, catalyzing NTP-dependent nucleic acid duplex destabilization or strand displacement (6, 7). Although a number of RNA helicases possess RNA unwinding activity in vitro, only three have been reported to exhibit intrinsic RNA annealing activity, the highly related yeast nuclear DEAD-box RNA helicases, p68 and p72 (8), and the nucleolar DExD-box protein, RNA helicase II/Gu (9, 10). Although these helicases unwind dsRNA, 1 the RNA substrates on which they catalyze RNA annealing differ with p68/72 capable of annealing complementary ssRNA...

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“…The initial rate of state transition was inhibited approximately to the same extent, while the final value of F v /F m reached was only 0.44, indicating a very partial transition to state 1 and therefore the persistence of a large excess of the PSI antenna size over that of PSII. The simultaneous existence in the same cell, and therefore in the same chloroplast, of chains in state 2 and in state 1 has been reported previously (Forti et al, 2003).…”

Section: The Role Of Respirationmentioning

confidence: 70%

“…However, the transition to state 1 is slow and incomplete if O 2 is added in the dark, as indicated by the changes in fluorescence parameters. Oxaloacetate (OAA), which oxidizes NADPH (accumulated in the dark anaerobic conditions; see Forti et al, 2003) through the action of the stromal NADP-specific malate dehydrogenase, accelerates the transition in the light. However, it has no effect in the dark, indicating that the activity of PSI is necessary for the oxidation of the intersystem chain.…”

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confidence: 99%

State Transitions in Chlamydomonas reinhardtii. The Role of the Mehler Reaction in State 2-to-State 1 Transition

Forti

Caldiroli

2005

Plant Physiology

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The light intensity-dependent transition to state 1 of dark-adapted anaerobic state 2 Chlamydomonas reinhardtii cells is stimulated by oxygen and by other electron acceptors for photosystem I, such as oxaloacetate and methylviologen. This suggests that the transition to state 1 requires the oxidation of the intersystem chain by photosystem I photochemistry. On the other hand, the mere oxidation in the dark of the chain-by addition of O 2 -leads only to a slow and incomplete transition. The light-driven stimulation by O 2 of the state 1 transition is saturated at an O 2 concentration of 15 to 20 mM, definitely higher than that of respiration. We suggest that this may represent the affinity for oxygen of the Mehler reaction, a conclusion that is confirmed by the observations that mitochondrial respiration is apparently not involved in modulating state 2-to-state 1 transition. The catalysis of the state 2-to-state 1 transition upon illumination of anaerobically adapted algae might represent, therefore, a relevant physiological role of this process in C. reinhardtii.The phenomenon of state transitions in the photosynthetic apparatus, discovered by Bonaventura and Myers (1969;Murata, 1969), involves the reversible transfer of a fraction of the PSII outer antenna to PSI, and is understood as a mechanism for balancing the absorption cross-section size of both photosystems under natural illumination conditions and therefore their photochemical activities. The transition from state 1-to-state 2 decreases the PSII antenna to the advantage of that of PSI, and the opposite is true for the reverse process (see the reviews by Allen, 1992;Horton et al., 1996;Gal et al., 1997;Wollman, 2001). The mechanism of state transitions involves the phosphorylation of the light-harvesting chlorophyll a/b proteins of PSII (LHCII) by a membrane-bound protein kinase (state 1-to-state 2 transition) and its dephosphorylation by a phosphatase (state 2-to-state 1 transition). Following phosphorylation, a fraction of LHCII migrates to PSI by lateral diffusion in the thylakoids; the opposite process occurs after dephosphorylation. The kinase is activated by the over-reduction of the intersystem electron carriers (reviews by Allen, 1992;Horton et al., 1996;Gal et al., 1997;Wollman, 2001), and specifically by the binding of plastoquinol (PQH 2 ) to its Qo binding site on the cytochrome b6f complex (Vener et al., 1997;Zito et al., 1999).In higher plants, state transitions are light dependent, involve the transfer of 15% to 20% of the PSII antenna, and are effective in balancing the relative rates of the two photochemical reactions in series (see Allen, 1992). In the green alga Chlamydomonas reinhardtii, state 2 can be reached upon incubation for a few minutes in dark anaerobic conditions (Delepelaire and Wollman, 1985). During this process, a very large fraction of the PSII antenna is transferred to PSI (approximately 80%; Delosme et al., 1994Delosme et al., , 1996. State 2-to-state 1 transition requires the reoxidation of the intersystem electron tr...

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In Vivo Changes of the Oxidation-Reduction State of NADP and of the ATP/ADP Cellular Ratio Linked to the Photosynthetic Activity in Chlamydomonas reinhardtii

Cited by 56 publications

References 53 publications

Impaired respiration discloses the physiological significance of state transitions in Chlamydomonas

Impaired respiration discloses the physiological significance of state transitions in Chlamydomonas

RNA Structural Rearrangement via Unwinding and Annealing by the Cyanobacterial RNA Helicase, CrhR

State Transitions in Chlamydomonas reinhardtii. The Role of the Mehler Reaction in State 2-to-State 1 Transition

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