Darkness rapidly induces a decline in the stability and translation of the pea Ferredoxin-1 (Fed-1) mRNA in transgenic tobacco. Direct half-life measurement showed that mutation of the (CAUU)(4) stabilizes Fed-1 mRNA in the dark. ( CAUU) 1, a feature more common in plant 50 UTRs than ( CAUU) 4, confers slight light-responsive mRNA accumulation. At least three but less than 11 CAUU repeats near the 50 end of the 5' UTR are required for full light-responsive accumulation. Furthermore, 26 nt of the 5' UTR, including the (CAUU)(4) repeat, is sufficient to confer a significant similar to 2.5-fold increase in light-regulated mRNA accumulation when fused to the 50 end of a heterologous plant mRNA. A mutation of the ( CAUU) 4 repeat that compromises light-regulated mRNA stability changes in vitro the accessibility of the region to ribonuclease V-1 and ribonuclease A suggesting the geometry formed by the repeat may be important for instability. Finally, dark-induced Fed-1 mRNA instability occurs even when most of the mRNA is retained on polyribosomes, and thus is likely an independent event regulated by darkness.