Dynamics of reversible protein phosphorylation in thylakoids of flowering plants: The roles of STN7, STN8 and TAP38

Abstract

Phosphorylation is the most common post-translational modification found in thylakoid membrane proteins of flowering plants, targeting more than two dozen subunits of all multiprotein complexes, including some light-harvesting proteins. Recent progress in mass spectrometry-based technologies has led to the detection of novel low-abundance thylakoid phosphoproteins and localised their phosphorylation sites. Three of the enzymes involved in phosphorylation/dephosphorylation cycles in thylakoids, the protein kinases STN7 and STN8 and the phosphatase TAP38/PPH1, have been characterised in the model species Arabidopsis thaliana. Differential protein phosphorylation is associated with changes in illumination and various other environmental parameters, and has been implicated in several acclimation responses, the molecular mechanisms of which are only partly understood. The phenomenon of State Transitions, which enables rapid adaptation to short-term changes in illumination, has recently been shown to depend on reversible phosphorylation of LHCII by STN7-TAP38/PPH1. STN7 is also necessary for long-term acclimation responses that counteract imbalances in energy distribution between PSII and PSI by changing the rates of accumulation of their reaction-centre and light-harvesting proteins. Another aspect of photosynthetic acclimation, the modulation of thylakoid ultrastructure, depends on phosphorylation of PSII core proteins, mainly executed by STN8. Here we review recent advances in the characterisation of STN7, STN8 and TAP38/PPH1, and discuss their physiological significance within the overall network of thylakoid protein phosphorylation. This article is part of a Special Issue entitled: Regulation of Electron Transport in Chloroplasts.

Changes in the Phosphoproteome and Metabolome Link Early Signaling Events to Rearrangement of Photosynthesis and Central Metabolism in Salinity and Oxidative Stress Response in Arabidopsis

“…Phosphorylation of LHCII proteins was reported for the adaptation to environmental changes (Fristedt et al, 2009). Moreover, LHCII proteins have been shown to be substrates of STN7 protein kinase (Pesaresi et al, 2011). Phosphorylation of LHCII was shown to be involved in the energy distribution between the two photosystems, and signaling between light reception and phosphorylation of LHCII was found to be related to the redox state of the plastoquinone pool, whereby reduced plastoquinol leads to kinase activation (Vener et al, 1998).…”

Structural changes of the thylakoid membrane network induced by high light stress in plant chloroplasts

“…Whether a link exists between protein phosphorylation and the swelling of the lumen is unknown. If a link exists, then it must be an indirect one because PSII core phosphorylation by STN8 takes places exclusively on the stromal side [37]. However, concerning partial destacking, two models were postulated that explain how protein phosphorylation triggers unstacking.…”

“…The multi-step PSII repair cycle is outlined in figure 1. The mainstream model is that after high-light-induced damage, the PSII subunits D1, D2, CP43 and psbH are phosphorylated (figure 1(2)), catalysed mainly by the STN8 kinase [34,35] and possibly by the STN7 kinase [36][37][38]. As evidence exists that in STN7/STN8 double mutants, the disassembly of the PSII holocomplex is inhibited [33,[39][40][41], it was hypothesized that phosphorylation of core subunits triggers disassembly ( figure 1(3)).…”

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

“…[3][4][5] At the level of ETC, the adjustments of electron transport in response to rapid environmental changes are achieved by cooperation of several short-term photoprotective mechanisms, which include: (i) "State Transitions," i.e. optimization of light absorption between PSI and PSII achieved upon phosphorylation and association of the so-called 'mobile pool' of LHCII with either PSI or PSII [6][7][8] ; (ii) "Alternative Electron Transport Routes," i.e., redistribution of electron fluxes through different alternative pathways, including Cyclic Electron Transport (CET) mediated by either the NADH dehydrogenase-like (NDH) complex or the PRG5-PGRL1 protein complex [9][10][11] ; (iii) "Non Photochemical Quenching (NPQ)," i.e. pH-dependent dissipation of excess energy in the LHCII to protect the photosynthetic apparatus against photooxidation [12][13][14] ; (iv) "Photosynthesis Control," i.e., regulation of electron transport by the Cyt b 6 f complex, governed by the pH of thylakoid lumen and stroma.…”