Cryptophyte algae contain two kinds of light-harvesting protein, phycobiliproteins and chlorophyll a,c-binding proteins. The β subunit of the phycobiliprotein phycoerythrin (PE) is encoded in the chloroplast. Genes for the other PE polypeptides are located in the nucleus but little is known of their organization. We cloned and sequenced six cpeA genes encoding the phycoerythrin α subunit from a genomic library of the cryptophyte Rhodomonas CS24. Derived peptide sequences of the cpeA genes show that α subunits occur in at least two forms, a longer α1 form and a shorter α2 form. Remarkably, all six cpeA genes occur in divergent pairs encoding one α1 and one α2 subunit. Four cac genes encoding chlorophyll a,c-binding proteins were cloned and sequenced and also found to occur in divergent pairs comprising one cac1 and one cac2 gene. Inspection of the predicted targeting sequences of the α1 and α2 phycoerythrin polypeptides shows that only the α1 polypeptides have a thylakoid lumen targeting sequence, corresponding to the TAT pathway. Given the previously reported lack of a lumen-targeting sequence on the β subunit, we propose a novel import mechanism in which the entire α1α2ββ phycoerythrin complex is assembled in the stroma and transported into the thylakoid under the direction of the single targeting sequence on the α1 protein. The FAP motif implicated in plastid targeting in diatoms appears to be conserved in this cryptophyte.