A conserved F-box gene with unusual transcript localization

Drosophila partner of paired (ppa), which encodes an F-box protein that targets the Pax transcription factor Paired (Prd) for degradation, has the striking property that its mRNA is expressed in a striped pattern with a characteristic registration relative to the striped expression of prd in early embryos. Localized expression of F-box genes was not expected because F-box proteins generally have multiple substrates. We hypothesize that the patterned mRNA expression of Drosophila and zebrafish ppa homologs may reflect constraints resulting from the localized expression of their degradation substrates. To begin to test this idea, we wished to determine whether patterned mRNA expression is commonly observed among F-box genes, or whether it might be peculiar to ppa and its homologs, or even specific to Drosophila. We examined embryonic expression of all predicted F-box genes in Drosophila and found that mRNAs of 21 out of 23 predicted F-box genes are expressed uniformly in early Drosophila embryos, whereas ppa and CG4911 mRNAs are patterned, CG4911 being expressed at the positions of gastrulation folds. We also identified and tested expression of ppa in zebrafish, which has two highly conserved homologs, ppaA and ppaB, and found that both are expressed during embryogenesis and have enriched mRNA expression in regions including the neural tube, the head, and the fin buds. Despite being unusual in having localized transcripts, we found that the Drosophila and zebrafish homologs interact with the expected Drosophila components of the cellular degradation machinery - Skp1 (SkpA) and Rbx1 (Roc1a) - suggesting that the Ppa proteins are indeed functional F-box proteins. We conclude that patterning of ppa mRNA could reflect a constraint on ppa function that is not common among F-box genes. Electronic supplementary material to this paper can be obtained by using the Springer LINK server located at http://dx.doi.org/10.1007/ s00427-002-0222-7.