Fig. 8
Comprehensive model explaining the roles of Lhcb phosphorylation during ST. Panel A: Top view of the thylakoid membrane system depicting the multiple consequences of Lhcb phosphorylation events. A shift of the light environment from a far red- (FR) enriched to a red- enriched (R) condition activates a state 1—state 2 transition involving the phosphorylation of threonine residues of the Lhcb1 and Lhcb2 polypeptides by the STN7 kinase. Under state 1, Lhcb1/2 serine residues are phosphorylated by a kinase unrelated to STN7 (yellow circles) and independently of LHCII trimer identity. Upon transition to state 2 light conditions, the activation of the STN7 kinase results in the phosphorylation of residues Thr-38 (cyan stars) and Thr-40 (green stars) of Lhcb1 (excluded the Lhcb1.4 isoform) and Lhcb2 polypeptides, respectively. The phosphorylated Lhcb1 polypeptides are exclusively found in the strongly- (gold) and moderately- (blue) bound LHCII trimers, while phosphorylated Lhcb2 polypeptides are enriched in the mobile L trimer type (red). The latter predominantly contains the non-phosphorylatable Lhcb1.4 protein isoform [32]. The phosphorylation of Lhcb proteins induces a shrinkage of the grana diameter which brings the L trimers in contact with the STN7 kinase resulting in further phosphorylation of Lhcb2 proteins. The phosphorylated L trimer pool migrates towards the stroma lamellae where it associates with PSI to form a PSI-LHCI-LHCII supercomplex. Upon shifts to state 1 light conditions, the PPH1 (TAP38) de-phosphorylates Lhcb1/2 proteins causing the return of L trimers to the grana region and association with PSII. The graphical elements displayed were created using the structures retrieved from the Protein Data Bank [16] of the following PBD files: 5XNL, stacked C2S2M2-type PSII-LHCII supercomplex from Pisum sativum [87], 5ZJI, photosystem I supercomplex with light-harvesting complexes I and II [69]. The structures of the Serine/threonine-protein kinase STN7(Uniprot sequence code Q9S713) and TAP38 protein phosphatase (Uniprot sequence code P49599) were created with the AlphaFold Protein Structure software [94]. Panel B: the faster phosphorylation kinetics of Lhcb2 polypeptides compared with Lhcb1 by STN7 are explained by an optimal recognition of the substrate by the kinase owing to two consecutive arginine (R) residues directly upstream of the phosphorylatable Thr-40 residue [54]. The figures displayed in panel A and B were created with BioRender.com. Panel C: tridimensional structure of the PSI-LHCI-LHCII supercomplex of Zea mays, (PDB file 5ZJI) [69] depicting the PSI antenna system composed of the Lhca1 (cyan), Lhca4 (pink), Lhca2 (light green), Lhca3 (yellow) polypeptides in association with the phosphorylated LHCII L trimer (red). The PSI subunits which mediate the interaction are highlighted: PsbO (orange); PsbL (blue), PsbH (green), and PsbI (magenta). Panel D: detailed region occupied by the phosphate group of Lhcb2 P-Thr-40 and of its stabilizing interactions implicated in the formation of the PSI-LHCI-LHCII supercomplex mediated via hydrogen bonds (dotted yellow lines) with the amino group of arginine and the hydroxy group of threonine residues of the PSI PsbL subunit