Protein kinases and phosphatases involved in the acclimation of the photosynthetic apparatus to a changing light environment

Abstract

Photosynthetic organisms are subjected to frequent changes in light quality and quantity and need to respond accordingly. These acclimatory processes are mediated to a large extent through thylakoid protein phosphorylation. Recently, two major thylakoid protein kinases have been identified and characterized. The Stt7/STN7 kinase is mainly involved in the phosphorylation of the LHCII antenna proteins and is required for state transitions. It is firmly associated with the cytochrome b(6)f complex, and its activity is regulated by the redox state of the plastoquinone pool. The other kinase, Stl1/STN8, is responsible for the phosphorylation of the PSII core proteins. Using a reverse genetics approach, we have recently identified the chloroplast PPH1/TAP38 and PBPC protein phosphatases, which counteract the activity of STN7 and STN8 kinases, respectively. They belong to the PP2C-type phosphatase family and are conserved in land plants and algae. The picture that emerges from these studies is that of a complex regulatory network of chloroplast protein kinases and phosphatases that is involved in light acclimation, in maintenance of the plastoquinone redox poise under fluctuating light and in the adjustment to metabolic needs.

Figure 1.

Scheme of state transitions. State transitions involve a redistribution of the mobile light-harvesting antenna of PSII (LHCII) between PSII and PSI. Upon preferential excitation of PSII, the plastoquinone pool (PQ) is reduced and plastoquinol docks to the Qo site of cyt b₆f. This leads to the activation of a protein kinase that phosphorylates LHCII. The latter dissociates from PSII and migrates to PSI. If PSI is preferentially excited, the plastoquionone pool is oxidized, the kinase is inactivated and a phosphatase dephosphorylates the mobile LHCII, which moves back to PSII. (a) State 1 and (b) state 2 refer to the states in which the mobile LHCII is associated with PSII and PSI, respectively. Fd, ferredoxin; PC, plastocyanin. Reproduced with permission from Rochaix  [9].

Figure 2.

Model of Stt7/STN7 kinase in the thylakoid membrane. The Stt7/STN7 kinase contains a trans-membrane region with its N-terminal end in the lumen and the catalytic domain on the stromal side of the thylakoid membrane. This kinase is firmly associated with the cyt b₆f complex and interacts with LHCII and PSI, based on co-immunoprecipitations. The kinase probably exists as a dimer. Two conserved Cys between Stt7 and STN7 are located on the lumen side and could form an intersubunit disulphide bridge. One possibility is that inactivation of the kinase under conditions that lead to reduction of ferredoxin and thioredoxin occurs through a trans-thylakoid thiol pathway, including CcdA and Hcf164, which would reduce the disulphide bond (indicated with a broken line). TR, thioredoxin; FTR, ferredoxin-thioredoxin reductase, Fd, ferredoxin

Figure 3.

Phosphorylation sites in Stl1, Stt7 and STN7. The sequences of the Stl1, Stt7, STN7 and STN8 protein kinases have been aligned, and the phosphorylation sites in Stl1, Stt7 and STN7 are indicated by circles. Note that these sites are poorly conserved in these kinases especially in the C-terminal regions. The two conserved Cys are indicated by wedges.

Figure 4.

Regulatory network of thylakoid kinases and phosphatases. The redox state of the plastoquinone pool (PQ/PQH2) is dependent on irradiance, CO₂ level and cellular ATP/ADP ratio. Reduced plastoquinol activates the Stt7/STN7 kinase through the cyt b₆f complex. The major substrates of the Stt7/STN7 and Stl1/STN8 kinases are LHCII and the PSII core proteins [,–31]. STN7 is also involved in retrograde signalling (LTR) [30]. The LHCII kinase has been proposed to be inactivated through reduced thioredoxin (TRX) [7]. The PPH1 and the PBCP phosphatases act as the counterparts of the Stt7/STN7 and Stl1/STN8 kinases, respectively [–55]. The kinases CK2α and CSK act on the chloroplast gene expression system and may be redox-controlled [56,57]. TAK1 has been proposed to be involved in LHCII phosphorylation but its precise role remains to be determined [58,59].