Fortuitous events in the evolution of Light-dependent Protochlorophyllide Oxidoreductase

Abstract

Light-dependent protochlorophyllide oxidoreductase (LPOR) is a nuclear-encoded photoenzyme in many photosynthetic organisms. LPOR originated in primitive cyanobacterial ancestors during the great oxygenation event that was detrimental to the existence of the oxygen-sensitive LIPOR that prevailed in anoxygenic Earth. Both LIPOR and LPOR catalyse reduction of protochlorophyllide to chlorophyllide in the penultimate step of chlorophyll biosynthesis. Except for angiosperms and gnetophytes several oxygenic phototrophs harbour both LIPOR and LPOR. The coexistence of LIPOR and LPOR in certain phototrophs provides niche spaces for organisms in unconducive environment. The selection pressure of increased O2 concentration, changing light quality and quantity at different depths of the ocean, nutrient status of water, gene reorganization during several endosymbiotic events, horizontal gene transfer, LIPOR gene loss and multiple duplication events played a major role in the evolution and diversification of LPOR and its isoforms in photosynthetic and non-photosynthetic organisms. In the absence of LIPOR angiosperms become vulnerable to protochlorophyllide-sensitized and light-induced oxidative stress mediated by singlet oxygen. To overcome the photo-damage PORA was expressed abundantly in the plastids of etiolated plants. PORB evolved to take over the function of vanishing PORA isoform in light. Brassicales evolved PORC to protect plants from high light and other environmental stresses. HighlightsO_LIProtochlorophyllide oxidoreductase is an important photo-enzyme in angiosperms that needs light as a substrate for the synthesis of chlorophylls. Therefore, angiosperms cannot green in dark although several algae and lower green plants can synthesize chlorophyll in dark due to the presence of light-independent protochlorophyllide oxidoreductase (LIPOR). C_LIO_LIIn response to climate change, during the great oxygenation event light-dependent protochlorophyllide oxidoreductase (LPOR) evolved due to the O2-induced selection pressure that inactivated the oxygen-sensitive LIPOR. C_LIO_LIIncreased O2 concentration, changing light quality and quantity at different depths of ocean, gene reorganization during several endosymbiotic events, selective LIPOR gene loss and multiple duplication events played a major role in the evolution and diversification of LPOR and its isoforms in phototrophs. C_LIO_LIPhylogenetic studies indicate that LPOR genes have been overwhelmingly horizontally transferred between phototrophs and also non phototrophic organisms. C_LIO_LIPresence of LPOR in non-photosynthetic organisms, Mycobacterium and certain fungi suggests that LPOR may have some other reductive functions in these organisms. C_LI