Greening in the dark: light-independent chlorophyll biosynthesis from anoxygenic photosynthetic bacteria to gymnosperms

The enzymatic reduction of protochlorophyllide (Pchlide) represents a key regulatory step in Mg-tetrapyrrole pigment biosynthesis among organisms from eubacteria to higher plants. Pchlide is a late precursor of both chlorophylls (Chls) and bacteriochlorophylls (Bchls), the crucial pigments required for charge separation during oxygenic and anoxygenic photosynthesis, respectively. Two biochemically and genetically distinct strategies to reduce Pchlide have arisen during evolution and coexist in many photosynthetic organisms. One strategy relies on NADPH:Pchlide oxidoreductase (POR), a nuclear-encoded, plastid-localized enzyme. POR requires light and NADPH as cofactors for the enzymatic reduction of Pchlide to chlorophyllide during light-dependent Chl biosynthesis. This reaction is lacking in anoxygenic photosynthetic bacteria, but occurs in cyanobacteria, algae and plants, including their most highly evolved representatives, the angiosperms. The main focus of this review will be the genetics and regulation of a light-independent strategy for Pchlide reduction catalyzed by the darkactive Pchlide oxidoreductase (DPOR). The presence of DPOR allows light-independent Bchl biosynthesis in anoxygenic photosynthetic bacteria, and light-independent Chl biosynthesis in cyanobacteria, algae and many plants, angiosperms excepted. DPOR, which is structurally distinct from POR, is specified by three plastid-encoded genes in eukaryotes that green in the dark. The corresponding gene products, ChlB, ChlL and ChlN, are evolutionarily related to the subunits of the eubacterial nitrogenase enzyme complex.