A phosphorylation map of the photosystem II supercomplex C2S2M2.

PS II PHOSPHORYLATION It was 36 years ago when John Bennett first discovered chloroplast protein phosphorylation (Bennett, 1977). The most conspicuous chloroplast phosphoprotein was the apoprotein of the Light Harvesting Complex II (LHC II) of photosystem II (PS II). Other phosphoproteins included the reaction center protein CP43 and the quinone-binding proteins D1 and D2 of PS II. These earlier studies also identified the PsbH protein, the minor subunit of PS II, as another chloroplast phosphoprotein (Allen, 1992). Nearly all of the first-known chloroplast phosphoproteins belong to PS II, the water-oxidizing photosystem of oxygenic photosynthesis. With more than 25 protein subunits and 350 kDa in size, the PS II core monomer is a massive structure (Umena et al., 2011). This enormous size is in addition to the peripheral light harvesting complexes. The major peripheral antenna of PS II is LHC II, which is a trimer. Some, so-called minor, LHC are monomeric and act as linkers in connecting the trimeric LHC II to the core. The core is composed of the reaction center proteins D1 and D2 and an internal antenna made up of CP43 and CP47. The PS II core with its peripheral antenna forms supercomplexes, which mainly differ in the number of LHC II bound to the core (Caffarri et al., 2009). The core itself is dimeric (C2) to which the LHC II could strongly (S), or moderately (M), or loosely (L) bind. The monomeric linker associated with the Sform is CP26, and for the M-form are CP29 and CP24. A dimeric core (C2) with 2 S and 2 M LHC II (C2S2M2) is the most abundant supercomplex in plant photosynthetic membranes (Kouril et al., 2012). PS II phosphorylation is light dependent. It turned out, however, light acts through the redox state of the plastoquinone (PQ) pool (Allen et al., 1981; Bennett, 1991). PS II phosphorylation can be divided into the core phosphorylation (D1, D2, CP43, and PsbH) and the peripheral antenna phosphorylation (LHC II). In plants, the protein kinases that phosphorylate the core and the LHC II have been identified as Stn8 and Stn7, respectively, (Bellafiore et al., 2005; Bonardi et al., 2005). PS II phosphorylation is only observed in green algae and plants, and not in cyanobacteria and red algae where the light harvesting antenna is phycobilisomebased (Pursiheimo et al., 1998). Core phosphorylation is responsive to light intensity with increasing levels of phosphorylation observed in high light (Elich et al., 1992; Tikkanen and Aro, 2012). On the contrary, LHC II phosphorylation was restricted to low light condition specific to PS II (Rintamaki et al., 2000). At higher light intensities, the activity of the Stn7 is inhibited by the reduced stromal electron carrier thioredoxin (Rintamaki et al., 2000; Puthiyaveetil, 2011). It was also noted that only the L-form of the LHC II trimer is phosphorylated, while the LHC II isoforms comprising the Sand M-trimers are not phosphorylated or do not contain phosphorylation sites (Galka et al., 2012). LHC II phosphorylation is the basis of state transitions, an acclimatory response to changes in light quality (Bonaventura and Myers, 1969; Murata, 1969). The precise function of PS II core phosphorylation, however, is still unclear. PS II undergoes damage in light, which results in photoinhibition—light-induced loss of photosynthetic activity (Aro et al., 1993; Long et al., 1994). In plants and green algae, PS II is mainly found in the stacked granal regions of the thylakoid membrane where it forms almost immobile supercomplexes (Kirchhoff et al., 2008; Mullineaux, 2008). The centrally located reaction center protein D1 is the main target of photodamage in PS II (Kyle et al., 1984). To maintain photosynthetic efficiency in high light, chloroplasts have evolved a robust repair process known as the PS II repair cycle, wherein the damaged D1 protein is degraded and replaced with a newly synthesized copy (Melis, 1999; Nixon et al., 2010). The PS II repair cycle operates through many constraints (Kirchhoff, 2013b), chief among them are how the repair machinery located in the unstacked regions of the thylakoid membrane accesses the damaged photosystems in the stacked, crowded granal membranes and how the damaged photosystems are mobilized in the rather “immobile” grana. The proposed functions of PS II phosphorylation include “marking” the damaged photosystems for degradation (Aro et al., 1993), increasing the mobility of photosystems (Goral et al., 2010; Herbstova et al., 2012), disassembly of PS II (Tikkanen et al., 2008; Fristedt and Vener, 2011), decreasing the granal diameter (Herbstova et al., 2012; Kirchhoff, 2013a), and for maintaining electron flow in high light (Harrison and Allen, 1991). Some of these proposals are not mutually exclusive. Functions such as increased mobility and disassembly are especially supported but how precisely phosphorylation produces these effects are unclear.