Chlorophyll f synthesis by a super-rogue photosystem II complex

Certain cyanobacteria synthesize chlorophyll molecules (Chl d and Chl f ) that absorb in the far-red region of the solar spectrum, thereby extending the spectral range of photosynthetically active radiation 1 , 2 . The synthesis and introduction of these far-red chlorophylls into the photosynthetic apparatus of plants might improve the efficiency of oxygenic photosynthesis, especially in far-red enriched environments, such as in the lower regions of the canopy 3 . Production of Chl f requires the ChlF subunit, also known as PsbA4 (ref. 4 ) or super-rogue D1 (ref. 5 ), a paralogue of the D1 subunit of photosystem II (PSII) which, together with D2, bind cofactors involved in the light-driven oxidation of water. Current ideas suggest that ChlF oxidizes Chl a to Chl f in a homodimeric ChlF reaction centre (RC) complex and represents a missing link in the evolution of the heterodimeric D1/D2 RC of PSII (refs. 4 , 6 ). However, unambiguous biochemical support for this proposal is lacking. Here, we show that ChlF can substitute for D1 to form modified PSII complexes capable of producing Chl f . Remarkably, mutation of just two residues in D1 converts oxygen-evolving PSII into a Chl f synthase. Overall, we have identified a new class of PSII complex, which we term ‘super-rogue’ PSII, with an unexpected role in pigment biosynthesis rather than water oxidation.