Oskar RNA, Not Protein, Required for Oogenesis

Science's STKE  25 Jul 2006:
Vol. 2006, Issue 345, pp. tw244
DOI: 10.1126/stke.3452006tw244

In Drosophila, maternal nurse cells deposit the mRNA for oskar into the oocyte, where the oskar transcript accumulates in the posterior pole of the oocyte during mid-oogenesis. Translation of oskar mRNA produces two alternatively spliced variants that are important for posterior patterning and formation of the abdomen and germ cells in the resulting embryos. Jenny et al. describe two new mutants of oskar (oskA87and osk187) that do not produce oskar mRNA and that result in oogenesis arrest in the mutant female flies, a phenotype that is different from that observed for oskar mutants that only disrupt protein production without loss of mRNA. The flies carrying the protein-disrupting oskar mutations are fertile but produce mutant offspring. The oogenesis arrest phenotype of oskA87and osk187 was rescued by introduction of protein-disrupting oskar alleles (either the previously defined oskar protein-disrupting alleles or alleles engineered to prevent translation initiation). The resulting flies produced embryos lacking abdomens, which is the phenotype observed in the absence of Oskar protein. Constructs lacking the oskar promoter or introns or coding sequence rescued the oogenesis defect, but constructs lacking the 3′-untranslated region (3′-UTR) did not. Further, constructs of only the 3′-UTR of oskar rescued the eggless phenotype of the oskar mRNA-deficient mutants. Thus, oskar mRNA has a role early in oogenesis that is independent of the Oskar protein's function in posterior patterning and abdomen formation in embryos. Oogenesis begins in the oskar mRNA-deficient mutants, but the RNA-binding protein Staufen does not accumulate in the developing oocyte and, ultimately, the mutant egg chamber degenerates. Introduction of the 3′-UTR of oskar recruited Staufen to the oocyte but failed to promote accumulation of both Staufen and the 3′-UTR of oskar to the posterior of the developing oocyte. Thus, the 3′-UTR of oskar is sufficient to restore oogenesis, whereas the protein is required to restore proper embryonic patterning.

A. Jenny, O. Hachet, P. Závorszky, A. Cyrklaff, M. D. J. Weston, D. St. Johnston, M. Erdélyi, A. Ephrussi, A translation-independent role of oskar RNA in early Drosophila oogenesis. Development 133, 2827-2833 (2006). [Abstract] [Full Text]