The photosynthetic chloroplast thylakoid membrane of higher plants is a complex three-dimensional structure that is morphologically dynamic on a timescale of just a few minutes. The membrane dynamics are driven by the phosphorylation of light-harvesting complex II (LHCII) by the STN7 kinase, which controls the size of the stacked grana region relative to the unstacked stromal lamellae region. Here, I hypothesise that the functional significance of these membrane dynamics is in controlling the partition of electrons between photosynthetic linear and cyclic electron transfer (LET and CET), which determines the ratio of NADPH/ATP produced. The STN7 kinase responds to the metabolic state of the chloroplast by sensing the stromal redox state. A high NADPH/ATP ratio leads to reduction of thioredoxin f (TRXf), which reduces a CxxxC motif in the stromal domain of STN7 leading to its inactivation, whereas a low NADPH/ATP ratio leads to oxidation of TRXf and STN7 activation. Phosphorylation of LHCII leads to smaller grana, which favour LET by speeding up diffusion of electron carriers plastoquinone (PQ) and plastocyanin (PC) between the domains. In contrast, dephosphorylation of LHCII leads to larger grana that slow the diffusion of PQ and PC, leaving the PQ pool in the stroma more oxidised, thus enhancing the efficiency of CET. The feedback regulation of electron transfer by the downstream metabolism is crucial to plant fitness, since perturbations in the NADPH/ATP ratio can rapidly lead to the inhibition of photosynthesis and photo-oxidative stress.

Introduction

The plant chloroplast thylakoid membrane houses the photosynthetic electron transfer (PET) reactions that provide the NADPH and ATP required for CO2 fixation by the Calvin–Benson–Bassham (CBB) cycle. Generally, PET and the CBB cycle are conceptualised and studied separately, even though the two processes are intimately coupled. Interactions take place not only at the level of shared turnover of the NADP+/NADPH and ADP/ATP pools in the chloroplast, but also in the feedforward and feedback regulation the two processes impart on one another [13]. Feedforward regulation of the CBB by PET involves the alteration of the stromal environment in terms of redox potential, pH and ionic status, which modulates the activity of numerous enzymes involved in CO2 assimilation [3]. In turn, feedback regulation of PET by the CBB cycle influences the redox state of the electron carriers and the size of the proton motive force (Δp) of the thylakoid membrane [1,2]. These factors control the balance between light energy utilisation in the photochemical reactions and the dissipation of this energy as heat by non-photochemical quenching (NPQ) through regulation of the LHCII antenna system and ATP synthase [48]. In principle, the CBB cycle in C3 plants consumes ATP to NADPH in the strict ratio of 1.5 : 1, yet the linear electron transfer (LET) pathway from H2O to NADP+ during photosynthesis only produces 1.28 ATP per NADPH if the H+/ATP ratio is 4.67, as suggested by early biochemical studies and later the structure of the c-ring of the spinach ATP synthase [9,10]. In addition to production of glyceraldehyde 3-phosphate by the CBB cycle, a range of other metabolic processes also make varying demands on the chloroplast NADPH and ATP pools, including photorespiration, nitrogen and sulfur reduction, and protein, lipid and carbohydrate biosynthesis [1,11,12] (Figure 1A). The activity of these pathways varies depending on environmental conditions and developmental state of the leaf, thus affecting the ratio of ATP to NADPH required by the cell [1,11,12]. Since the turnover of ATP and NADPH pools is so rapid, any mismatch in the ATP/NADPH ratio can rapidly inhibit photosynthesis [1214]. Therefore, several regulatory mechanisms exist in the plant cell for the dissipation of the metabolite in excess or the augmentation of the metabolite in deficit. These mechanisms include the water–water cycle (WWC or Mehler reaction) [15], the malate valve [16], chlororespiration via plastoquinol oxidase (PTOX) [17] and cyclic electron transfer (CET) [18,19]. In plants, CET appears to be the dominant pathway for ATP augmentation and has been shown to be crucial to plant fitness, particularly in fluctuating light conditions [2022]. Whereas LET involves photosystem II (PSII), plastoquinone (PQ), cytochrome b6f (cytb6f), plastocyanin (PC), photosystem I (PSI), ferredoxin (Fd) and ferredoxin-NADP+ reductase (FNR) complexes acting in series and generates NADPH and a proton gradient that is utilised by ATP synthase to make ATP, CET transfers electrons from Fd back to PQ, forming a cycle around PSI. This allows proton transfer and thus synthesis of ATP without net NADPH formation (Figure 1B) [18,19]. Therefore, by controlling the balance between LET and CET, plants can adjust the ATP/NADPH ratio and contribute to the fulfilment of metabolic demand [1,4,11]. A greatly lowered capacity for electron transfer and photoprotection is observed when CET is knocked out by genetic mutation, suggesting that the balance between LET and CET is central to the proper regulation of photosynthesis in vivo [2022].

Role of LET and CET in photosynthesis.

Figure 1.
Role of LET and CET in photosynthesis.

(A) Sunlight initiates electron transfer in the chloroplast thylakoid membrane that leads to the synthesis of NADPH and ATP by LET, with ATP production further augmented by CET. The thylakoid membrane must continually adjust the LET/CET balance to provide the correct ratio of NADPH/ATP to meet changeable metabolic demand that depends on the relative activity of the Calvin cycle, N and S fixation, photorespiration and biosynthesis in the chloroplast stroma, which vary according to the environmental and developmental state of the plant. (B) Lateral heterogeneity in organisation of photosynthetic complexes in the thylakoid membrane. PSII is located in the grana stacks; PSI, ATP synthase and PGRL1/PGR5 and NDH are located in the stromal lamellae; and cytb6f is present in both domains. LET involves electron transfer from water to NADP+ via both PSII and PSI, with water oxidation at PSII and PQH2 oxidation at cytb6f leading to proton accumulation in the lumen, which is utilised by ATP synthase to drive ATP synthesis. CET involves recycling electrons from Fd to the stromal PQ pool and therefore produces ATP without net NADPH synthesis. Three possible CET pathways based on the NDH, PGRL1/PGR5 and FNR/cytb6f are shown.

Figure 1.
Role of LET and CET in photosynthesis.

(A) Sunlight initiates electron transfer in the chloroplast thylakoid membrane that leads to the synthesis of NADPH and ATP by LET, with ATP production further augmented by CET. The thylakoid membrane must continually adjust the LET/CET balance to provide the correct ratio of NADPH/ATP to meet changeable metabolic demand that depends on the relative activity of the Calvin cycle, N and S fixation, photorespiration and biosynthesis in the chloroplast stroma, which vary according to the environmental and developmental state of the plant. (B) Lateral heterogeneity in organisation of photosynthetic complexes in the thylakoid membrane. PSII is located in the grana stacks; PSI, ATP synthase and PGRL1/PGR5 and NDH are located in the stromal lamellae; and cytb6f is present in both domains. LET involves electron transfer from water to NADP+ via both PSII and PSI, with water oxidation at PSII and PQH2 oxidation at cytb6f leading to proton accumulation in the lumen, which is utilised by ATP synthase to drive ATP synthesis. CET involves recycling electrons from Fd to the stromal PQ pool and therefore produces ATP without net NADPH synthesis. Three possible CET pathways based on the NDH, PGRL1/PGR5 and FNR/cytb6f are shown.

In plants, two major routes of CET have been discovered to date, the antimycin A (AA)-sensitive proton gradient regulation complex (PGRL1/PGR5)-dependent pathway and the AA-insensitive NADPH-like dehydrogenase (NDH)-dependent pathway [18,19] (Figure 1B). There is evidence that PGRL1/PGR5 acts as an Fd-PQ oxidoreductase that can transiently interact with both PSI and cytb6f [23,24]. Alternatively, it has been suggested that PGR5 may be a regulator of the cytb6f complex [21] and that CET may involve transfer of electrons from an Fd–FNR complex to the Qn site of cytb6f [25,26], a pathway which may involve the unusual haem c [27,28] (Figure 1B). NDH (NADPH-like dehydrogenase complex) is an Fd-PQ oxidoreductase that forms a supercomplex with PSI and shows similarity to complex I in mitochondria [2931]. The NDH complex has been shown to act as a proton pump, thus increasing the H+/e ratio of this CET pathway compared with the PGR5/PGRL1 and Fd/FNR/cytb6f routes, which only translocate protons at cytb6f [32].

Current models for regulation of the LET/CET balance

Since the CBB cycle uses 1.5 ATP/NADPH and LET only produces a ratio of 1.28, a constant portion of CET can be expected even in the steady state, estimated at ∼15% of the total LET flux [4]. Indeed, different isoforms of Fd and FNR genes, which encode proteins with activities devoted to LET or CET [33], could provide the basis for a constant portion of CET regulated by the protein copy number. However, just as the developmental state of the leaf and its environment can change with time, the relative demand for ATP/NADPH, and hence, the ratio of LET/CET can be expected to dynamically vary [1,4,18,19]. Several metabolic signals, indicative of an imbalance in the NADPH/ATP ratio, have been suggested to regulate the amount of CET including the PQ redox state [1,34], ADP/ATP ratio [35], stromal redox state [3638], reactive oxygen species [39,40], phosphorylation of NDH [41] and PGRL1 [42] and calcium signalling [43].

The suggested regulation of the LET/CET balance via the PQ redox state is based on the state transition [1,34]. State transitions in plants involve the dynamic reallocation of LHCII between PSI and PSII, provoked by preferential excitation of PSI (far-red light) or PSII (red/blue light). PQ reduction in red/blue light activates STN7 kinase [44,45]-mediated phosphorylation of LHCII, favouring its association with PSI (State II). PQ oxidation in far-red light inactivates STN7, allowing the constitutively active TAP38 [46,47] to dephosphorylate LHCII, favouring its association with PSII (State I). Reduction of PQ was suggested to parallel PSI acceptor side limitation due to a high NADPH/ATP ratio [1,34]. The transition to State II would then lead to an increased excitation of PSI relative to PSII, thus increasing CET and making good the ATP deficit. In contrast, a low NADPH/ATP ratio would lead to PQ oxidation via removal of the acceptor side limitation of PSI and a transition to State I and thus enhanced LET to augment NADPH production [1,34]. In line with this, anoxic conditions that lead to induction of State II in the green alga Chlamydomonas also cause increased CET flux and accumulation of a supercomplex containing PGRL1, PSI and cytb6f [37,48]. However, the CET supercomplex formation and enhanced CET flux still occurred in the absence of state transitions in Chlamydomonas [37]; similarly, in Arabidopsis, CET activity was unaffected by the absence of the STN7 kinase [49].

An alternative means through which metabolic signals may regulate the LET/CET balance is via control of the partition of electrons between the pathways. CET is sensitive to the ‘redox poise’ of the electron transfer chain, and thus, it is inhibited by over-reduction or over-oxidation [50]. Therefore, when high NADPH levels inhibit LET, PQ will tend to be over-reduced, thus potentially curtailing the ability of CET to operate. For this reason, LET and CET may require some degree of structural compartmentalisation. One possibility is through the formation of supercomplexes dedicated to CET [2931,37,48] with a sequestered PQ pool. Yet, to date, no counterpart to the PGRL1/PSI/cytb6f supercomplex in Chlamydomonas [37,48] has been found in plants, although associations between PGRL1 and PSI, PGRL1 and cytb6f, NDH and PSI [2931], cytb6f and FNR [51], NDH and FNR [52], PSI and FNR [53], and more recently between PSI and cytb6f [31] have been described, none of these has yet been shown to be more abundant in conditions favouring CET. Another possibility is the maintenance of separate PQ pools within membrane domains [54,55]. The thylakoid membrane in plants is divided into two domains: the stacked grana and the interconnecting stromal lamellae with the various electron transfer components heterogeneously distributed among them [56]. PSII is found mainly within the grana stacks, while PSI and ATP synthase are found mainly within the stromal lamellae, and cytb6f is found within both domains [56,57]. There is evidence for compartmentation of PQ in dark-adapted thylakoids, with ∼70% of the PQ pool available for rapid reduction by PSII (t½ = 25 ms) and the remaining 30% only slowly reduced (t½ = 6 s) [54]. These fast and slow PQ pools were suggested to arise from the grana and stromal lamellae, respectively, with diffusion of PQ confined by the extreme protein crowding within the grana [54,58]. Joliot et al. [54] suggested that the presence of a distinct PQ pool associated with cytb6f in the stromal lamellae, isolated by diffusion limitation from PSII in the grana, could create the conditions necessary for CET to coexist with LET. In this view, CET and LET would share a common pool of PC and PSI, with injection of electrons into the CET pathways determined by competition at the level of Fd [18]. Importantly, the restricted diffusion of PQ is largely abolished upon either unstacking of thylakoids [58] or light adaptation [54], suggesting that changes in membrane organisation can significantly influence the rate of diffusion and potentially therefore the balance between CET and LET.

A new model for the regulation of the LET/CET balance based on dynamic thylakoid stacking

Here, I propose that dynamic changes in thylakoid stacking regulate the LET/CET balance by altering the degree of partition of the PQ pool. Rapid changes in thylakoid stacking have been observed in spinach upon transition from darkness to low light and from low light to high light [5961]. Darkness and high light led to larger grana stacks, whereas low light led to smaller grana stacks. These changes parallel the trends in LHCII phosphorylation, which peak at low light and are decreased in high light and darkness [62,63]. Phosphorylation regulates the surface charge on LHCII and hence the cation dependency of stacking [64,65]. Smaller grana have been shown to facilitate faster diffusion of PQH2 and PC from the grana to stromal lamellae thylakoids and more rapid reduction of PSI, i.e. reduced partition of electron carriers between domains [61] (Figure 2A). Since the rate-limiting step of LET is the diffusion of PQH2 from PSII to cytb6f and its oxidation therein, any change in the diffusion time has the potential to affect the overall rate considerably [66]. Indeed, more efficient LET has also been observed in ΔTAP38 Arabidopsis plants [46], which possess smaller grana, whereas LET is compromised in the ΔCURT mutant with larger grana [67]. In contrast with enhanced LET, smaller grana and reduced stacking have a negative impact on the ability to induce CET [61]. The rate of PSI reduction following far-red illumination was slower when the grana size was smaller, indicating reduced CET, and transient NPQ generation upon moderate light challenge, which is a proxy for ΔpH generation by CET [22], was also compromised [61]. Thus, larger grana may benefit CET through increased partition of electron carriers between the domains, leaving the stromal PQ pool in a relatively more oxidised state, which is more competitive for electrons from Fd (Figure 2B). Larger grana are also favoured in high light and darkness conditions [59], where there is evidence that CET is up-regulated [20,35,68].

Variable grana stacking alters the partition of the thylakoid PQ pool and hence LET/CET balance.

Figure 2.
Variable grana stacking alters the partition of the thylakoid PQ pool and hence LET/CET balance.

(A) Smaller grana create a larger area of contact between the grana and stromal lamellae membranes. Under these conditions, the diffusion of PC and PQ between grana and stromal lamellae is relatively fast, engaging cytb6f in both domains efficiently in LET, which predominates over CET. (B) Larger grana reduce the area of contact between the grana and stromal lamellae membranes. Under these conditions, the diffusion of PC and PQ between grana and stromal lamellae is relatively slow, leaving the stromal lamellae PQ pool in a more oxidised state that promotes more efficient CET.

Figure 2.
Variable grana stacking alters the partition of the thylakoid PQ pool and hence LET/CET balance.

(A) Smaller grana create a larger area of contact between the grana and stromal lamellae membranes. Under these conditions, the diffusion of PC and PQ between grana and stromal lamellae is relatively fast, engaging cytb6f in both domains efficiently in LET, which predominates over CET. (B) Larger grana reduce the area of contact between the grana and stromal lamellae membranes. Under these conditions, the diffusion of PC and PQ between grana and stromal lamellae is relatively slow, leaving the stromal lamellae PQ pool in a more oxidised state that promotes more efficient CET.

How might the STN7 kinase be regulated to allow these dynamics? STN7 is activated when PQH2 binds to the QO site of the cytb6f complex [69], wherein it is suggested to reduce a lumenal facing disulfide linkage between two cysteines in the kinase [70]. Therefore, increasing reduction of the PQ pool with light intensity should up-regulate STN7. However, a second negative feedback loop exists that sees STN7 inactivated by thioredoxin f (TRXf) upon a build-up of reducing power on the PSI acceptor side with increasing light intensity [71,72]. TRXf is suggested to reduce a buried disulfide linkage between cysteines near the ATP-binding motif on the stromal side of STN7 [70,72]. STN7 is therefore maximally active at ∼100–200 μmol photons m−2 s−1 in white light and inactivated in darkness (by PQ oxidation) and in high light (by TRXf) [44,62,71,72]. Interestingly, changes in white light intensity cause no alterations in relative PSI and PSII antenna sizes in contrast with the preferential excitation of the photosystems described above [8,63]. Thus, under natural white light conditions, the hyper-phosphorylation of LHCII, and thus the state transition, is prevented by the TRXf regulation of STN7. Thus, white light-driven LHCII phosphorylation is sufficient for changes in grana size, but insufficient to provoke the state transition in plants. This situation contrasts with that in Chlamydomonas, where the STT7 LHCII kinase (counterpart of STN7) is not inhibited by TRXf and therefore state transitions and stromal over-reduction (and therefore increased CET) coexist [37,48].

I suggest that the prevailing NADPH/ATP ratio in the chloroplast controls the activity of STN7 and thus the size of the grana. In this view, PQ reduction in the light activates STN7 and its activity is then largely regulated by the stromal redox state and therefore the extent of TRXf reduction. Thus, when the NADPH/ATP ratio is low, TRXf is oxidised, allowing ATP binding and phosphorylation of LHCII (Figure 3A). In contrast, when ATP is in deficit (high NADPH/ATP ratio), STN7 is inactivated by reduced TRXf, leading to larger grana stacks and increased CET. The amount of thylakoid membrane stacking and thus LET/CET balance are therefore regulated by the metabolic state of the chloroplast. Evidence for metabolic regulation of STN7 already exists in the literature. For instance, treatment of thylakoids with reduced dithiothreitol (DTT) resulted in decreased LHCII phosphorylation and increased CET activation [38,71], while oxidised DTT stimulated LHCII phosphorylation [62,71]. In turn, the addition of ADP or an ATP sink such as ribulose-5-phosphate, which would elevate the NADPH/ATP ratio, also provokes dephosphorylation of LHCII [73,74], while the addition of ATP or increased adenylate pool energy charge stimulates LHCII phosphorylation through consumption of NADPH and therefore oxidation of TRXf [73]. It is also possible that the PGR5/PGRL1 complex may play a crucial role in sensing the stromal redox state [26] and directly or indirectly regulating STN7 [63]. Such a role for PGR5 would be consistent with two other observations: the lack of LHCII dephosphorylation upon shift from low to high light in the ΔPGR5 mutant of Arabidopsis and the stimulation of LHCII phosphorylation in the presence of AA [63,75]. If grana size remains small in the ΔPGR5 mutant in high light, this may partly explain the inefficient CET in this mutant.

Metabolic regulation of the STN7 kinase.

Figure 3.
Metabolic regulation of the STN7 kinase.

In light, PQ reduction leads to STN7 activation. Two conditions can then ensue: (A) When the NADPH/ATP ratio is low, the STN7 kinase is active and LHCII phosphorylation is increased, leading to smaller grana that favour LET, augmenting NADPH production (dashed arrow). (B) When the NADPH/ATP ratio is high, reduced TRXf inactivates the STN7 kinase and the constitutively active TAP38 phosphatase dephosphorylates LHCII, leading to larger grana that favour CET, augmenting ATP production (dashed arrow). The PGR5/PGRL1 complex appears to have some as yet undefined regulatory role in sensing the stromal redox poise, and its absence [63] or inhibition by AA [75] prevents the inactivation of STN7 by TRXf.

Figure 3.
Metabolic regulation of the STN7 kinase.

In light, PQ reduction leads to STN7 activation. Two conditions can then ensue: (A) When the NADPH/ATP ratio is low, the STN7 kinase is active and LHCII phosphorylation is increased, leading to smaller grana that favour LET, augmenting NADPH production (dashed arrow). (B) When the NADPH/ATP ratio is high, reduced TRXf inactivates the STN7 kinase and the constitutively active TAP38 phosphatase dephosphorylates LHCII, leading to larger grana that favour CET, augmenting ATP production (dashed arrow). The PGR5/PGRL1 complex appears to have some as yet undefined regulatory role in sensing the stromal redox poise, and its absence [63] or inhibition by AA [75] prevents the inactivation of STN7 by TRXf.

Concluding remarks

I have suggested a novel hypothesis that links grana dynamics with LHCII phosphorylation and the regulation of the LET/CET balance. The key player in this regulatory model is the effect of TRXf on STN7 activity, which provides information on the NADPH/ATP ratio in the stroma. There are several important implications of this hypothesis, both in terms of future experiments and biological function. The hypothesis predicts a central role for grana stacking in controlling the degree of partition of the PQ pool and thus control of the relative efficiencies of CET versus LET. Therefore, CET should be less competitive for electrons in the ΔTAP38 and oeCURT mutants of Arabidopsis, which have smaller grana. It is equally important to establish whether the absence of STN7 and/or TAP38 prevents dynamic changes in stacking and understand whether changing PSII (and possibly CURT) phosphorylation plays any role. In principle, by manipulating the metabolic state of the chloroplast, it should be possible to alter the extent of grana stacking, while keeping the light intensity constant. Moreover, with modern metabolomic approaches, it should now be possible to accurately quantify the dynamic transients in metabolite pools that elicit changes in LHCII phosphorylation upon fluctuations in light intensity.

Abbreviations

     
  • AA

    antimycin A

  •  
  • CBB

    Calvin–Benson–Bassham

  •  
  • cytb6f

    cytochrome b6f

  •  
  • DTT

    dithiothreitol

  •  
  • Fd

    ferredoxin

  •  
  • LET and CET

    linear and cyclic electron transfer

  •  
  • LHCII

    light-harvesting complex II

  •  
  • NDH

    NADPH-like dehydrogenase

  •  
  • PC

    plastocyanin

  •  
  • PGRL1/PGR5

    proton gradient regulation complex

  •  
  • PQ

    plastoquinone

  •  
  • PSI

    photosystem I

  •  
  • PSII

    photosystem II

  •  
  • TRXf

    thioredoxin f

Acknowledgments

I thank the late Professor Jan Anderson FRS for inspiration in writing this hypothesis and dedicate it to her memory. I also thank Professor Peter Horton FRS (University of Sheffield), Professor Neil Hunter FRS (University of Sheffield) and Professor Alexander Ruban (Queen Mary University of London) for useful discussions and critiquing the work. I acknowledge funding from the Biotechnology and Biological Sciences Research Council (U.K.), Leverhulme Trust, Human Frontiers Science Programme and the University of Sheffield Krebs Institute and Grantham Centre for Sustainable Futures.

Competing Interests

The Author declares that there are no competing interests associated with this manuscript.

References

References
1
Horton
,
P.
(
1985
) Interactions between electron transfer and carbon assimilation. In
Photosynthetic Mechanisms and the Environment
(
Barber
,
J.
and
Baker
,
N.R.
, eds), pp.
135
187
.
Elsevier
,
Amsterdam, NY
2
Foyer
,
C.
,
Furbank
,
R.
,
Harbinson
,
J.
and
Horton
,
P.
(
1990
)
The mechanisms contributing to photosynthetic control of electron transport by carbon assimilation in leaves
.
Photosyn. Res.
25
,
83
100
3
Walker
,
D.A.
and
Robinson
,
S.P.
(
1978
) Regulation of photosynthetic carbon assimilation. In
Photosynthetic Carbon Assimilation
(
Siegelman
,
H.W.
and
Hind
,
G.
, eds), pp.
43
59
.
Plenum Press
,
New York
4
Kramer
,
D.M.
,
Avenson
,
T.J.
and
Edwards
,
G.E.
(
2004
)
Dynamic flexibility in the light reactions of photosynthesis governed by both electron and proton transfer reactions
.
Trends Plant Sci.
9
,
349
357
5
Li
,
Z.
,
Wakao
,
S.
,
Fischer
,
B.B.
and
Niyogi
,
K.K.
(
2009
)
Sensing and responding to excess light
.
Annu. Rev. Plant Biol.
60
,
239
260
6
Horton
,
P.
(
2012
)
Optimization of light harvesting and photoprotection: molecular mechanisms and physiological consequences
.
Philos. Trans. R. Soc. B
367
,
3455
3465
7
Ruban
,
A.V.
,
Johnson
,
M.P.
and
Duffy
,
C.D.P.
(
2012
)
The photoprotective molecular switch in the photosystem II antenna
.
Biochim. Biophys. Acta
1817
,
167
181
8
Tikkanen
,
M.
and
Aro,
E.-M.
(
2014
)
Integrative regulatory network of plant thylakoid energy transduction
.
Trends Plant Sci.
19
,
10
17
9
Ort
,
D.R.
and
Izawa
,
S.
(
1974
)
Studies on the energy-coupling sites of photosynthesis: V. phosphorylation efficiencies (P/e2) associated with aerobic photooxidation of artificial electron donors
.
Plant Physiol.
53
,
370
376
10
Seelert
,
H.
,
Poetsch
,
A.
,
Dencher
,
N.A.
,
Engel
,
A.
,
Stahlberg
,
H.
and
Müller
,
D.J.
(
2000
)
Structural biology: proton-powered turbine of a plant motor
.
Nature
405
,
418
419
11
Kramer
,
D.M.
and
Evans
,
J.R.
(
2011
)
The importance of energy balance in improving photosynthetic productivity
.
Plant Physiol.
155
,
70
78
12
Noctor
,
G.
, and
Foyer
,
C.H.
(
2000
)
Homeostasis of adenylate status during photosynthesis in a fluctuating environment
.
J. Exp. Bot.
51
(
Suppl 1
),
347
356
13
Foyer
,
C.H.
,
Furbank
,
R.T.
and
Walker
,
D.A.
(
1989
)
Co-regulation of electron transport and Benson-Calvin cycle activity in isolated spinach chloroplasts: studies on glycerate 3-phosphate reduction
.
Arch. Biochem. Biophys.
268
,
687
697
14
Slabas
,
A.R.
and
Walker,
D.A.
(
1976
)
Transient inhibition by ribose 5-phosphate of photosynthetic O2 evolution in a reconstituted chloroplast system
.
Biochim. Biophys. Acta
430
,
154
164
15
Miyake
,
C.
(
2010
)
Alternative electron flows (water–water cycle and cyclic electron flow around PSI) in photosynthesis: molecular mechanisms and physiological functions
.
Plant Cell Physiol.
51
,
1951
1963
16
Scheibe
,
R.
(
2004
)
Malate valves to balance cellular energy supply
.
Physiol. Plantar.
120
,
21
26
17
Nawrocki
,
W.J.
,
Tourasse
,
N.J.
,
Taly
,
A.
,
Rappaport
,
F.
and
Wollman
,
F.-A.
(
2015
)
The plastid terminal oxidase: its elusive function points
to multiple contributions to plastid physiology
.
Annu. Rev. Plant Biol.
66
,
49
74
18
Johnson
,
G.N.
(
2011
)
Physiology of PSI cyclic electron transport in higher plants
.
Biochim. Biophys. Acta
1807
,
384
389
19
Yamori
,
W.
and
Shikanai
,
T.
(
2016
)
Physiological functions of cyclic electron transport around photosystem I in sustaining photosynthesis and plant growth
.
Annu. Rev. Plant Biol.
67
,
81
106
20
Munekage
,
Y.
,
Hashimoto
,
M.
,
Miyake
,
C.
,
Tomizawa
,
K.
,
Endo
,
T.
,
Tasaka
,
M.
et al. 
(
2004
)
Cyclic electron flow around photosystem I is essential for photosynthesis
.
Nature
429
,
579
582
21
Soursa
,
M.
,
Jarvi
,
S.
,
Grieco
,
M.
,
Nurmi
,
M.
,
Pietrzykowska
,
M.
,
Rantala
,
M.
et al. 
(
2012
)
Proton gradient regulation 5 is essential for proper acclimation of Arabidopsis photosystem I to naturally and artificially fluctuating light conditions
.
Plant Cell
24
,
2394
2948
22
Munekage
,
Y.
,
Hojo
,
M.
,
Meurer
,
J.
,
Endo
,
T.
,
Tasaka
,
M.
and
Shikanai
,
T.
(
2002
)
PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis
.
Cell
110
,
361
371
23
DalCorso
,
G.
,
Pesaresi
,
P.
,
Masiero
,
S.
,
Aseeva
,
E.
,
Schünemann
,
D.
,
Finazzi
,
G.
et al. 
(
2008
)
A complex containing PGRL1 and PGR5 is involved in the switch between linear and cyclic electron flow in Arabidopsis
.
Cell
132
,
273
285
24
Hertle
,
A.P.
,
Blunder
,
T.
,
Wunder
,
T.
,
Pesaresi
,
P.
,
Pribil
,
M.
,
Armbruster
,
U.
et al. 
(
2013
)
PGRL1 is the elusive ferredoxin-plastoquinone reductase in photosynthetic cyclic electron flow
.
Mol. Cell
49
,
511
523
25
Joliot
,
P.
, and
Johnson
,
G.N.
(
2011
)
Regulation of cyclic and linear electron flow in higher plants
.
Proc. Natl Acad. Sci. U.S.A.
108
,
13317
13322
26
Nandha
,
B.
,
Finazzi
,
G.
,
Joliot
,
P.
,
Hald
,
S.
and
Johnson
,
G.N.
(
2007
)
The role of PGR5 in the redox poising of photosynthetic electron transport
.
Biochim. Biophys. Acta
1767
,
1252
1259
27
Stroebel
,
D.
,
Choquet
,
Y.
,
Popot
,
J.-L.
and
Picot
,
D.
(
2003
)
An atypical haem in the cytochrome b6f complex
.
Nature
426
,
413
418
28
Kurisu
,
G.
,
Zhang
,
H.
,
Smith
,
J.L.
and
Cramer
,
W.A.
(
2003
)
Structure of the cytochrome b6f complex of oxygenic photosynthesis: tuning the cavity
.
Science
302
,
1009
1014
29
Kouřil
,
R.
,
Strouhal
,
O.
,
Nosek
,
L.
,
Lenobel
,
R.
,
Chamrád
,
I.
,
Boekema
,
E.J.
et al. 
(
2014
)
Structural characterization of a plant photosystem I and NAD(P)H dehydrogenase supercomplex
.
Plant J.
77
,
568
576
30
Peng
,
L.W.
,
Fukao
,
Y.
,
Fujiwara
,
M.
,
Takami
,
T.
and
Shikanai
,
T.
(
2009
)
Efficient operation of NAD (P)H dehydrogenase requires supercomplex formation with photosystem I via minor LHCI in Arabidopsis
.
Plant Cell
21
,
3623
3640
31
Sathish Yadav
,
K.N.
,
Semchonok
,
D.A.
,
Nosek
,
L.
,
Kouřil
,
R.
,
Fucile
,
G.
,
Boekema
,
E.
et al. 
(
2016
)
Supercomplexes of plant photosystem I with cytochrome b6f, light-harvesting complex II and NDH
.
Biochim. Biophys. Acta
1858
,
12
20
32
Strand
,
D.
,
Fisher
,
N.
and
Kramer
,
D.A.
(
2017
)
The higher plant plastid NAD(P)H dehydrogenase-like complex (NDH) is a high efficiency proton pump that increases ATP production by cyclic electron flow
.
J. Biol. Chem.
292
,
11850
11860
33
Goss
,
T.
and
Hanke
,
G.
(
2014
)
The End of the line: can ferredoxin and ferredoxin NADP(H) oxidoreductase determine the fate of photosynthetic electrons?
Curr. Protein Pept. Sci.
15
,
384
393
PMID:
[PubMed]
34
Allen
,
J.F.
(
1984
)
Protein phosphorylation and optimal production of ATP in photosynthesis
.
Biochem. Soc. Trans.
12
,
774
775
35
Joliot
,
P.
, and
Joliot
,
A.
(
2002
)
Cyclic electron transfer in plant leaf
.
Proc. Natl Acad. Sci. U.S.A.
99
,
10209
10214
36
Breyton
,
C.
,
Nandha
,
B.
,
Johnson
,
G.N.
,
Joliot
,
P.
and
Finazzi
,
G.
(
2006
)
Redox modulation of cyclic electron flow around PSI in C3 plants
.
Biochemistry
45
,
13465
13475
37
Takahashi
,
H.
,
Clowez
,
S.
,
Wollman
,
F.A.
,
Vallon
,
O.
and
Rappaport
,
F.
(
2013
)
Cyclic electron flow is redox-controlled but independent of state transition
.
Nat. Commun.
4
,
1954
38
Strand
,
D.D.
,
Fisher
,
N.
,
Davis
,
G.A.
and
Kramer
,
D.M.
(
2016
)
Redox regulation of the antimycin A sensitive pathway of cyclic electron flow around photosystem I in higher plant thylakoids
.
Biochim. Biophys. Acta
1857
,
1
6
39
Strand
,
D.D.
,
Livingston
,
A.K.
,
Satoh-Cruz
,
M.
,
Froehlich
,
J.E.
,
Maurino
,
V.G.
and
Kramer
,
D.M.
(
2015
)
Activation of cyclic electron flow by hydrogen peroxide in vivo
.
Proc. Natl Acad. Sci. U.S.A.
112
,
5539
5544
40
Casano
,
L.M.
,
Martín
,
M.
and
Sabater
,
B.
(
2001
)
Hydrogen peroxide mediates the induction of chloroplastic Ndh complex under photooxidative stress in barley
.
Plant Physiol.
125
,
1450
1458
41
Lascano
,
H.R.
,
Casano
,
L.M.
,
Martín
,
M.
and
Sabater
,
B.
(
2003
)
The activity of the chloroplastic Ndh complex is regulated by phosphorylation of the NDH-F subunit
.
Plant Physiol.
132
,
256
262
42
Reiland
,
S.
,
Finazzi
,
G.
,
Endler
,
A.
,
Willig
,
A.
,
Baerenfaller
,
K.
,
Grossman
,
J.
et al. 
(
2011
)
Comparative phosphoproteome profiling reveals a function of the STN8 kinase in fine-tuning of cyclic electron flow (CEF)
.
Proc. Natl Acad. Sci. U.S.A.
108
,
12955
12960
43
Terashima
,
M.
,
Petroutsos
,
D.
,
Hudig
,
M.
,
Tolsygina
,
I.
,
Trompelt
,
K.
,
Gabelein
,
P.
et al. 
(
2012
)
Calcium-dependent regulation of cyclic photosynthetic electron transfer by a CAS, ANR1, and PGRL1 complex
.
Proc. Natl Acad. Sci. U.S.A.
109
,
17717
17722
44
Horton
,
P.
and
Black
,
M.T.
(
1980
)
Activation of adenosine 5′ triphosphate-induced quenching of chlorophyll fluorescence by reduced plastoquinone. The basis of State I–State II transitions in chloroplasts
.
FEBS Lett.
119
,
141
144
45
Bellafiore
,
S.
,
Barneche
,
F.
,
Peltier
,
G.
and
Rochaix
,
J.-D.
(
2005
)
State transitions and light adaptation require chloroplast thylakoid protein kinase STN7
.
Nature
433
,
892
895
46
Pribil
,
M.
,
Pesaresi
,
P.
,
Hertle
,
A.
,
Barbato
,
R.
and
Leister
,
D.
(
2010
)
Role of plastid protein phosphatase TAP38 in LHCII dephosphorylation and thylakoid electron flow
.
PLoS Biol.
8
,
e1000288
47
Shapiguzov
,
A.
,
Ingelsson
,
B.
,
Samol
,
I.
,
Andres
,
C.
,
Kessler
,
F.
,
Rochaix
,
J.-D.
et al. 
(
2010
) The
PPH1 phosphatase is specifically involved in LHCII dephosphorylation and state transitions in Arabidopsis
.
Proc. Natl Acad. Sci. U.S.A.
107
,
4782
4787
48
Iwai
,
M.
,
Takizawa
,
K.
,
Tokutsu
,
R.
,
Okamuro
,
A.
,
Takahashi
,
Y.
and
Minagawa
,
J.
(
2010
)
Isolation of the elusive supercomplex that drives cyclic electron flow in photosynthesis
.
Nature
464
,
1210
1213
49
Pesaresi
,
P.
,
Hertle
,
A.
,
Pribil
,
M.
,
Kleine
,
T.
,
Wagner
,
R.
,
Strissel
,
H.
et al. 
(
2009
)
Arabidopsis STN7 kinase provides a link between short- and long-term photosynthetic acclimation
.
Plant Cell
21
,
2402
2423
50
Grant
,
B.R.
and
Whatley
,
F.R.
(
1967
) Some factors affecting the onset of cyclic photophosphorylation. In
Biochemistry of Chloroplasts
(
Goodwin
,
T.W.
, ed), pp.
505
521
,
Academic Press
51
Zhang
,
H.M.
,
Whitelegge
,
J.P.
and
Cramer
,
W.A
.
Ferredoxin:NADP(+) oxidoreductase is a subunit of the chloroplast cytochrome b6f complex
.
J. Biol. Chem.
276
,
38159
38165
52
José Quiles
,
M.
and
Cuello
,
J.
(
1998
)
Association of ferredoxin-NADP oxidoreductase with the chloroplastic pyridine nucleotide dehydrogenase complex in barley leaves
.
Plant Physiol.
117
,
235
244
53
Andersen
,
B.
,
Scheller
,
H.V.
and
Møller
,
B.L.
(
1992
)
The PSI-E subunit of photosystem I binds ferredoxin:NADP+ oxidoreductase
.
FEBS Lett.
311
,
169
173
54
Joliot
,
P.
,
Lavergne
,
J.
and
Béal
,
D.
(
1992
)
Plastoquinone compartmentation in chloroplasts. I. Evidence for domains with different rates of photo-reduction
.
Biochim. Biophys. Acta
1101
,
1
12
55
Dumas
,
L.
,
Chazaux
,
M.
,
Peltier
,
G.
,
Johnson
,
X.
and
Alric
,
J.
(
2016
)
Cytochrome b6f function and localization, phosphorylation state of thylakoid membrane proteins and consequences on cyclic electron flow
.
Photosyn. Res.
129
,
307
320
56
Andersson
,
B.
and
Anderson
,
J.M.
(
1980
)
Lateral heterogeneity in the distribution of chlorophyll-protein complexes of the thylakoid membranes of spinach chloroplasts
.
Biochim. Biophys. Acta
593
,
427
440
57
Cox
,
R.P.
and
Andersson
,
B.
(
1981
).
Lateral and transverse organisation of cytochromes in the chloroplast thylakoid membrane
.
Biochem. Biophys. Res. Commun.
103
,
1336
1342
58
Kirchhoff
,
H.
,
Horstmann
,
S.
and
Weis
,
E.
(
2000
).
Control of photosynthetic electron transport by PQ diffusion microdomains in thylakoids of higher plants
.
Biochim. Biophys. Acta
1459
,
148
168
59
Rozak
,
P.R.
,
Seiser
,
R.M.
,
Wacholtz
,
W.F.
and
Wise
,
R.R.
(
2002
)
Rapid, reversible alterations in spinach thylakoid appression upon changes in light intensity
.
Plant Cell Environ.
25
,
421
429
60
Anderson
,
J.M.
,
Horton
,
P.
,
Kim
,
E.-H.
and
Chow
,
W.S.
(
2012
)
Towards elucidation of dynamic structural changes of plant thylakoid architecture
.
Phil. Trans. R. Soc. London
367
,
3515
3524
61
Wood
,
W.H.J.
,
MacGregor-Chatwin
,
C.
,
Barnett
,
S.
,
Mayneord
,
G.
,
Huang
,
X.
,
Hobbs
,
J.
et al. 
(
2018
)
Dynamic thylakoid stacking regulates the balance between linear and cyclic photosynthetic electron transfer
.
Nat. Plants
4
,
116
127
62
Rintamäki
,
E.
,
Salonen
,
M.
,
Suoranta
,
U.-M.
,
Carlberg
,
I.
,
Andersson
,
B.
and
Aro
,
E.-M.
(
1997
)
Phosphorylation of light-harvesting complex II and photosystem II core proteins shows different irradiance-dependent regulation in vivo
.
J. Biol. Chem.
272
,
30476
30482
63
Mekala
,
N.R.
,
Soursa
,
M.
,
Rantala
,
M.
,
Aro
,
E.-M.
and
Tikkanen
,
M.
(
2015
)
Plants actively avoid state transitions upon changes in light intensity: role of light-harvesting complex II protein dephosphorylation in high light
.
Plant Phys.
168
,
721
734
64
Barber
,
J.
(
1982
)
Influence of surface charges on thylakoid structure and function
.
Annu. Rev. Plant Physiol.
33
,
261
295
65
Puthiyaveeti
,
S.
,
van Oort
,
B.
and
Kirchhoff
,
H.
(
2017
)
Surface charge dynamics in photosynthetic membranes and the structural consequences
.
Nat. Plants
3
,
17020
66
Haehnel
,
W.
(
1984
)
Photosynthetic electron transport in higher plants
.
Ann. Rev. Plant Physiol.
35
,
659
693
67
Armbruster
,
U.
,
Labs
,
M.
,
Pribil
,
M.
,
Viola
,
S.
,
Xu
,
W.
,
Scharfenberg
,
M.
et al. 
(
2013
)
Arabidopsis CURVATURE THYLAKOID1 proteins modify thylakoid architecture by inducing membrane curvature
.
Plant Cell
25
,
2661
2678
68
Miyake
,
C.
,
Miyata
,
M.
,
Shinzaki
,
Y.
and
Tomizawa
,
K.
(
2005
)
CO2 response of cyclic electron flow around PSI (CEF-PSI) in tobacco leaves—relative electron fluxes through PSI and PSII determine the magnitude of non-photochemical quenching (NPQ) of Chl fluorescence
.
Plant Cell Physiol.
46
,
629
637
69
Vener
,
A.V.
,
van Kan
,
P.J.M.
,
Rich
,
P.R.
,
Ohad
,
I.
and
Andersson
,
B.
(
1997
)
Plastoquinol at the quinol oxidation site of reduced cytochrome bf mediates signal transduction between light and protein phosphorylation: thylakoid protein kinase deactivation by a single-turnover flash
.
Proc. Natl Acad. Sci. U.S.A.
94
,
1585
1590
70
Puthiaveetil
,
S.
(
2011
)
A mechanism for regulation of chloroplast LHC II kinase by plastoquinol and thioredoxin
.
FEBS Lett.
585
,
1717
1721
71
Rintamaki
,
E.
,
Martinsuo
,
P.
,
Pursihemo
,
S.
and
Aro
,
E.-M.
(
2000
)
Cooperative regulation of light-harvesting complex II phosphorylation via the plastoquinol and ferredoxin-thioredoxin system
in chloroplasts
.
Proc. Natl Acad. Sci. U.S.A.
97
,
11644
11649
72
Wunder
,
T.
,
Xu
,
W.
,
Liu
,
Q.
,
Wanner
,
G.
,
Leiaster
,
D.
and
Pribil
,
M.
(
2013
)
The major thylakoid protein kinases STN7 and STN8 revisited: effects of altered STN8 levels and regulatory specificities of the STN kinases
.
Front. Plant Sci.
4
,
417
73
Markwell,
J.P.
,
Baker
,
N.R.
and
Thornber
,
J.P.
(
1982
)
Metabolic regulation of the thylakoid protein kinase
.
FEBS Lett.
142
,
171
174
74
Horton
,
P.
and
Foyer
,
C.
(
1983
)
Relationships between protein phosphorylation and electron transport in the reconstituted chloroplast system
.
Biochem. J.
210
,
517
521
75
Oxborough
,
K.
,
Lee
,
P.
and
Horton
,
P.
(
1987
)
Regulation of thylakoid protein phosphorylation by high-energy-state quenching
.
FEBS Lett.
221
,
211
214

Author notes

*

Matthew Johnson was the recipient of the Biochemical Society's Colworth Medal in 2018.