The structurally related light-dependent protochlorophyllide (Pchlide) oxidoreductases PORA and PORE mediate the only light-requiring step in chlorophyll (Chi) biosynthesis in higher plants. Correlative evidence suggests that some in vivo functions of PORA and PORE may be unique, including a postulated photoprotective role for PORA. For example, wild-type Arabidopsis thaliana seedlings grown in non-photooxidative far-red light (cFR) resemble those grown in white light (WL), but they are yellow and do not green normally thereafter in WL. This defect is accompanied by the absence of detectable PORA and reduced levels of PORE expression. Here, direct evidence is provided that the presence of FOR, either as PORA or PORE, can confer photoprotection in plants. In contrast to the wild-type, the plastids of transgenic PORA- or PORB-overexpressing Arabidopsis seedlings grown in cFR possess extensive prolamellar bodies. Upon a subsequent shift to WL, POR-overexpressing seedlings develop thylakoid membranes, accumulate large amounts of Chi and are viable at fluence rates lethal to the wild-type. Intriguingly, the plastid membrane architectures of greening transgenic seedlings seem to depend on whether PORA or PORE has been overproduced. POR-overexpressing seedlings shifted from cFR to WL of fluence rates from 20 to 500 mu E m(-2) sec(-1) accumulate substantially higher amounts of Chi than does the wild-type. Furthermore, the WL fluence rate that permits maximal Chi accumulation increases from 8 mu E m(-2) sec(-1) in the wild-type to 125 mu E m(-2) sec(-1) in transgenic seedlings. FOR overexpression during growth in cFR also correlates with a fourfold decrease in the steady-state content of Pchlide, a potentially lethal photosensitizer.