Protein phosphorylation and oxidative protein modification mediate plant photosystem II disassembly and repair

The light-driven water-splitting reaction of photosystem II exposes its key reaction center core protein subunits to irreversible oxidative photodamage. A rapid repair cycle replaces photodamaged core subunits in plants, but how the large antenna-core supercomplex structures of plant photosystem II disassemble for repair is not currently understood. Phosphorylation of reaction center core protein subunits has been suggested as a mechanism of disassembly. Consistent with this, we find specific involvement of phosphorylation in removing peripheral antenna from the core and monomerization of the dimeric cores in Arabidopsis. However, photosystem disassembly occurred to some degree even in the absence of phosphorylation as suggestive of other unknown mechanisms of disassembly. Here we show that the oxidative modifications of amino acid residues in core protein subunits of photosystem II are active mediators of disassembly. Exogenously-applied hydrogen peroxide induces photosystem disassembly, especially the conversion of the monomeric cores into two reaction center subcomplexes. We further show that the extent of monomer disassembly is proportional to the oxidative protein damage, with the fully disassembled reaction center subcomplexes containing more modifications. In the monomeric core, some amino acid oxidative modifications map at the D1-CP43 interface as consistent with a dissociation of the core along these subunits. Oxidative modifications thus likely disassemble only the damaged monomeric cores, ensuring an economical photosystem disassembly process. Our results suggest oxidative protein modification represents an ancient mechanism of photosystem disassembly, and that phosphorylation originated later in evolution to impart explicit control over the repair process.