Plants Actively Avoid State Transitions upon Changes in Light Intensity: Role of Light-Harvesting Complex II Protein Dephosphorylation in High Light

Mekala, Nageswara Rao; Suorsa, Marjaana; Rantala, Marjaana; Aro, Eva‐Mari; Tikkanen, Mikko

doi:10.1104/pp.15.00488

Cited by 82 publications

(77 citation statements)

References 66 publications

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“…These observations suggest that Lhcb phosphorylation may contribute to the movement of the PSII-LHCII supercomplexes from grana cores toward lessstacked domains of the thylakoid membrane, grana margins, and stromal lamellae. This hypothesis is consistent with the recent proposal that phosphorylation of both the LHCII antenna and the PSII core assists the migration of PSII-LHCII out of grana (Mekala et al, 2015). The phosphorylation patterns of Lhcb1 and Lhcb2 may be rationalized by considering that, in low levels of white light, energy capture should be maximized by ensuring that all LHCII trimers are associated with photosystems.…”

Section: Antenna Phosphorylation In the Psii-lhcii Supercomplexessupporting

confidence: 74%

Phosphorylation of the Lhcb2 isoform of Light Harvesting Complex II is central to state transitions

et al. 2015

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ORCID IDs: 0000-0003-0587-7621 (P.L.); 0000-0002-6155-9153 (D.D.).Light-harvesting complex II (LHCII) is a crucial component of the photosynthetic machinery, with central roles in light capture and acclimation to changing light. The association of an LHCII trimer with PSI in the PSI-LHCII supercomplex is strictly dependent on LHCII phosphorylation mediated by the kinase STATE TRANSITION7, and is directly related to the light acclimation process called state transitions. In Arabidopsis (Arabidopsis thaliana), the LHCII trimers contain isoforms that belong to three classes: Lhcb1, Lhcb2, and Lhcb3. Only Lhcb1 and Lhcb2 can be phosphorylated in the N-terminal region. Here, we present an improved Phos-tag-based method to determine the absolute extent of phosphorylation of Lhcb1 and Lhcb2. Both classes show very similar phosphorylation kinetics during state transition. Nevertheless, only Lhcb2 is extensively phosphorylated (.98%) in PSI-LHCII, whereas phosphorylated Lhcb1 is largely excluded from this supercomplex. Both isoforms are phosphorylated to different extents in other photosystem supercomplexes and in different domains of the thylakoid membranes. The data imply that, despite their high sequence similarity, differential phosphorylation of Lhcb1 and Lhcb2 plays contrasting roles in light acclimation of photosynthesis.

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Section: Antenna Phosphorylation In the Psii-lhcii Supercomplexessupporting

confidence: 74%

Phosphorylation of the Lhcb2 isoform of Light Harvesting Complex II is central to state transitions

et al. 2015

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“…Recently, an alternative interpretation for the role of PSII-LHCII protein phosphorylation has been suggested based, in part, on several reports that indicate that LHCII, rather than being associated primarily with PSII, serves as an antenna pigment bed for both PSII and PSI during the acclimation of Arabidopsis to irradiance (Kou ril et al, 2013;Wientjes et al, 2013;Grieco et al, 2015). Furthermore, it appears that changes in light intensity induce alterations in the level of thylakoid protein phosphorylation independently of state transitions Mekala et al, 2015). Thus, a new model has emerged whereby PSII and PSI are embedded in a common lake of LCHII and, consequently, are energetically coupled to one another.…”

Section: Discussionmentioning

confidence: 99%

The Antarctic Psychrophile Chlamydomonas sp. UWO 241 Preferentially Phosphorylates a Photosystem I-Cytochrome b₆/f Supercomplex

et al. 2015

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Chlamydomonas sp. UWO 241 (UWO 241) is a psychrophilic green alga isolated from Antarctica. A unique characteristic of this algal strain is its inability to undergo state transitions coupled with the absence of photosystem II (PSII) light-harvesting complex protein phosphorylation. We show that UWO 241 preferentially phosphorylates specific polypeptides associated with an approximately 1,000-kD pigment-protein supercomplex that contains components of both photosystem I (PSI) and the cytochrome b 6 /f (Cyt b 6 /f) complex. Liquid chromatography nano-tandem mass spectrometry was used to identify three major phosphorylated proteins associated with this PSI-Cyt b 6 /f supercomplex, two 17-kD PSII subunit P-like proteins and a 70-kD ATP-dependent zinc metalloprotease, FtsH. The PSII subunit P-like protein sequence exhibited 70.6% similarity to the authentic PSII subunit P protein associated with the oxygen-evolving complex of PSII in Chlamydomonas reinhardtii. Tyrosine-146 was identified as a unique phosphorylation site on the UWO 241 PSII subunit P-like polypeptide. Assessment of PSI cyclic electron transport by in vivo P700 photooxidation and the dark relaxation kinetics of P700 + indicated that UWO 241 exhibited PSI cyclic electron transport rates that were 3 times faster and more sensitive to antimycin A than the mesophile control, Chlamydomonas raudensis SAG 49.72. The stability of the PSI-Cyt b 6 /f supercomplex was dependent upon the phosphorylation status of the PsbP-like protein and the zinc metalloprotease FtsH as well as the presence of high salt. We suggest that adaptation of UWO 241 to its unique low-temperature and high-salt environment favors the phosphorylation of a PSI-Cyt b 6 /f supercomplex to regulate PSI cyclic electron transport rather than the regulation of state transitions through the phosphorylation of PSII light-harvesting complex proteins.

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“…These slow processes are unable to respond to the more rapid fluctuations, but will approach steady-states reflecting the conditions averaged over the many minutes-to-hours time-scale. Antenna statetransitions respond over the medium times-scales, but appear to be more important in green algae than higher plants (65). Intriguingly, the remaining, rapidly responding photoprotective processes are all controlled (directly or indirectly) by lumen pH, most importantly the adjustment of q E and the photosynthetic control of electron flow at the cytochrome b 6 f complex, and are thus likely to be limited by the slow rates of ΔpH formation and decay.…”

Section: Control Of the Extent And Kinetics Of Pmf Partitioningmentioning

confidence: 99%

Hacking the thylakoid proton motive force for improved photosynthesis: modulating ion flux rates that control proton motive force partitioning into Δ ψ and ΔpH

Davis

Rutherford

Kramer

2017

Phil. Trans. R. Soc. B

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SummaryThere is considerable interest in improving plant productivity by altering the dynamic responses of photosynthesis in tune with natural conditions. This is exemplified by the "energy-dependent" form of nonphotochemical quenching (q E ), the formation and decay of which can be considerably slower than natural light fluctuations, limiting photochemical yield. In addition, we recently reported that rapidly fluctuating light can produce Field Recombination Induced Photodamage (FRIP), where large spikes in electric field across the thylakoid membrane (Δψ) induce photosystem II recombination reactions that produce damaging singlet oxygen ( 1 O 2 ). Both q E and FRIP are directly linked to the thylakoid proton motive force (pmf), and in particular the slow kinetics of partitioning pmf into its ΔpH and Δψ components. Using a series of computational simulations, we explored the possibility of "hacking" pmf partitioning as a target for improving photosynthesis. Under a range of illumination conditions, increasing the rate of counter-ion fluxes across the thylakoid membrane should lead to more rapid dissipation of Δψ and formation of ΔpH. This would result in increased rates for the formation and decay of q E while ameliorating the amplitudes of Δψ-spikes and decreasing 1 O 2 production. These results suggest that ion fluxes may be a viable target for plant breeding or engineering. However, these changes also induce transient, but substantial mismatches in the ATP:NADPH output ratio as well as in the osmotic balance between the lumen and stroma, either of which may explain why evolution has not already accelerated thylakoid ion fluxes. Overall, though the model is simplified, it recapitulates many of the responses seen in vivo, while spotlighting critical aspects of the complex interactions between pmf components and photosynthetic processes. By making the program available, we hope to enable the community of photosynthesis researchers to further explore and test specific hypotheses.*Author for correspondence (kramerd8@cns.msu.edu). 2This opinion/hypothesis paper was inspired by the recent Royal Society symposium on "Enhancing Photosynthesis in Crop Plants: Targets for Improvement," (http://www.rsc.org/events/download/Document/cee7d4f2-9ff1-477b-b155-3e2492577d77) that brought together experts in a range of photosynthetic processes. A prominent theme of several of the presentations was the sensitivity of photosynthesis to rapid, rather than gradual, changes in environmental conditions. Of particular interest was the kinetic mismatch between fluctuations in photosynthetically active radiation (PAR), which can change by orders of magnitude within a second, and the relatively slow onset of photoprotective mechanisms (1, 2). Indeed, there is growing evidence that this mismatch can sensitize both PSI and PSII to oxidative photodamage (3, 4), of which the focus of this paper is the irreversible damage to PSII (to D1 and other subunits) due to 1 O 2 generated by PSII charge recombination. It has also been proposed that the...

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Plants Actively Avoid State Transitions upon Changes in Light Intensity: Role of Light-Harvesting Complex II Protein Dephosphorylation in High Light

Cited by 82 publications

References 66 publications

Phosphorylation of the Lhcb2 isoform of Light Harvesting Complex II is central to state transitions

Phosphorylation of the Lhcb2 isoform of Light Harvesting Complex II is central to state transitions

The Antarctic Psychrophile Chlamydomonas sp. UWO 241 Preferentially Phosphorylates a Photosystem I-Cytochrome b₆/f Supercomplex

Hacking the thylakoid proton motive force for improved photosynthesis: modulating ion flux rates that control proton motive force partitioning into Δ ψ and ΔpH

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Plants Actively Avoid State Transitions upon Changes in Light Intensity: Role of Light-Harvesting Complex II Protein Dephosphorylation in High Light

Cited by 82 publications

References 66 publications

Phosphorylation of the Lhcb2 isoform of Light Harvesting Complex II is central to state transitions

Phosphorylation of the Lhcb2 isoform of Light Harvesting Complex II is central to state transitions

The Antarctic Psychrophile Chlamydomonas sp. UWO 241 Preferentially Phosphorylates a Photosystem I-Cytochrome b6/f Supercomplex

Hacking the thylakoid proton motive force for improved photosynthesis: modulating ion flux rates that control proton motive force partitioning into Δ ψ and ΔpH

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The Antarctic Psychrophile Chlamydomonas sp. UWO 241 Preferentially Phosphorylates a Photosystem I-Cytochrome b₆/f Supercomplex