Thylakoid Protein Phosphorylation in Higher Plant Chloroplasts Optimizes Electron Transfer under Fluctuating Light    

Abstract

Several proteins of photosystem II (PSII) and its light-harvesting antenna (LHCII) are reversibly phosphorylated according to light quantity and quality. Nevertheless, the interdependence of protein phosphorylation, nonphotochemical quenching, and efficiency of electron transfer in the thylakoid membrane has remained elusive. These questions were addressed by investigating in parallel the wild type and the stn7, stn8, and stn7 stn8 kinase mutants of Arabidopsis (Arabidopsis thaliana), using the stn7 npq4, npq4, npq1, and pgr5 mutants as controls. Phosphorylation of PSII-LHCII proteins is strongly and dynamically regulated according to white light intensity. Yet, the changes in phosphorylation do not notably modify the relative excitation energy distribution between PSII and PSI, as typically occurs when phosphorylation is induced by "state 2" light that selectively excites PSII and induces the phosphorylation of both the PSII core and LHCII proteins. On the contrary, under low-light conditions, when excitation energy transfer from LHCII to reaction centers is efficient, the STN7-dependent LHCII protein phosphorylation guarantees a balanced distribution of excitation energy to both photosystems. The importance of this regulation diminishes at high light upon induction of thermal dissipation of excitation energy. Lack of the STN7 kinase, and thus the capacity for equal distribution of excitation energy to PSII and PSI, causes relative overexcitation of PSII under low light but not under high light, leading to disturbed maintenance of fluent electron flow under fluctuating light intensities. The physiological relevance of the STN7-dependent regulation is evidenced by severely stunted phenotypes of the stn7 and stn7 stn8 mutants under strongly fluctuating light conditions.

Regulation of the photosynthetic apparatus under fluctuating growth light

“…Using normal white light, however, the excitation balance between PSII and PSI provided by steady-state LHCII phosphorylation is essential only for plants grown under light intensity fluctuations [41]. Furthermore, we have observed that the excitation balance provided by steady-state LHCII phosphorylation under fluctuating light is a key factor in maintaining the activity of PSI, but not PSII [42].…”

“…The traditional use of different qualities of low intensity light to study state transitions contradict the natural redox regulation of the thylakoid protein kinases and phosphatases in plant chloroplasts, leading to a full dephosphorylation (state I) or a full phosphorylation (state II) of both the PSII and LHCII phosphoproteins. LHCII phosphorylation and dephosphorylation by different intensities of white light, however, does not lead to such state transitions, apparently owing to opposite behaviours of the PSII core and LHCII protein phosphorylation under these light conditions [41,79]. We have provided evidence that LHCII phosphorylation establishes a common antenna bed for both PSII and PSI in the so-called thylakoid megacomplexes [80], which ensure proper distribution of excitation energy to PSII and PSI.…”

“…On the basis of the experiments performed under physiologically relevant light conditions, i.e. different intensities of white light, we postulate that 'state transitions' as such do not occur in higher plant chloroplasts under physiological white light conditions [41]. The traditional use of different qualities of low intensity light to study state transitions contradict the natural redox regulation of the thylakoid protein kinases and phosphatases in plant chloroplasts, leading to a full dephosphorylation (state I) or a full phosphorylation (state II) of both the PSII and LHCII phosphoproteins.…”

“…We have provided evidence that LHCII phosphorylation establishes a common antenna bed for both PSII and PSI in the so-called thylakoid megacomplexes [80], which ensure proper distribution of excitation energy to PSII and PSI. This balance is based on delicate regulation of the phosphorylation levels of different individual thylakoid proteins and on protein surface charges that affect the protein-protein interactions and the migration of PSII core and LHCII complexes in the thylakoid membrane [41,81]. Coordination of excitation energy distribution between PSII and PSI from the common P-LHCII antenna is crucial in preventing the accumulation of electrons in ETC under low illumination phases of fluctuating growth light, and is therefore important for photoprotection of PSI in plant chloroplasts during the subsequent high light peak.…”

Photosynthesis Control: An underrated short-term regulatory mechanism essential for plant viability

“…48,54 Furthermore, when pgr5 mutants were grown under naturally fluctuating light in the field, they showed higher mortality rates as compared to WT (Fig. 1), whereas no difference between pgr5 and WT was observed when seedlings were grown under constant light.…”