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JOURNAL ARTICLES
The mago nashi locus encodes an essential product required for germ plasm assembly in Drosophila
P.A. Newmark, R.E. Boswell
Development 1994 120: 1303-1313;

Summary

In Drosophila, the localization of maternal determinants to the posterior pole of the oocyte is required for abdominal segmentation and germ cell formation. These processes are disrupted by maternal effect mutations in ten genes that constitute the posterior group. Here, the molecular analysis of one posterior group gene, mago nashi, is presented. Restriction fragment length polymorphisms and transcript alterations associated with mago nashi mutations were used to identify the mago nashi locus within a chromosomal walk. The mago nashi locus was sequenced and found to encode a 147 amino acid protein with no similarity to proteins of known or suspected function. The identification of the mago nashi locus was confirmed by sequencing mutant alleles and by P element-mediated transformation. Nonsense mutations in mago nashi, as well as a deletion of the 5′ coding sequences, result in zygotic lethality. The original mago nashi allele disrupts the localization of oskar mRNA and staufen protein to the posterior pole of the oocyte during oogenesis; anterior localization of bicoid mRNA is unaffected by the mutation. These results demonstrate that mago nashi encodes an essential product necessary for the localization of germ plasm components to the posterior pole of the oocyte.

REFERENCES

    1. Altschul S. F.,
    2. Gish W.,
    3. Miller W.,
    4. Myers E. W.,
    5. Lipman D. J.
    (1990) Basic local alignment search tool. J. Mol. Biol 215, 403–410
    OpenUrlCrossRefPubMedWeb of Science
    1. Ambrosio L.,
    2. Mahowald A. P.,
    3. Perrimon N.
    (1989) Requirement of the Drosophilaraf homologue for torso function. Nature 342, 288–291
    OpenUrlCrossRefPubMed
    1. Bardsley A.,
    2. McDonald K.,
    3. Boswell R. E.
    (1993) Distribution of tudor protein in the Drosophila embryo suggests separation of functions based on the site of localization. Development 119, 207–219
    OpenUrlAbstract
    1. Barker D. D.,
    2. Wang C.,
    3. Moore J.,
    4. Dickinson L. K.,
    5. Lehmann R.
    (1992) pumilio is essential for function but not for distribution of the Drosophila abdominal determinant nanos. Genes Dev 6, 2312–2326
    OpenUrlAbstract/FREE Full Text
    1. Beams H. W.,
    2. Kessel R. G.
    (1974) The problem of germ cell determinants. Int. Rev. Cytol 39, 413–479
    OpenUrlPubMedWeb of Science
    1. Bingham P. M.,
    2. Levis R.,
    3. Rubin G. M.
    (1981) Cloning of DNA sequences from the white locus of D. melanogaster by a novel and general method. Cell 25, 693–704
    OpenUrlCrossRefPubMedWeb of Science
    1. Boswell R. E.,
    2. Mahowald A. P.
    (1985) tudor, a gene required for assembly of the germ plasm in Drosophila melanogaster. Cell 43, 97–104
    OpenUrlCrossRefPubMedWeb of Science
    1. Boswell R. E.,
    2. Prout M. E.,
    3. Steichen J. C.
    (1991) Mutations in a newly identified Drosophila melanogaster gene, mago nashi, disrupt germ cell formation and result in the formation of mirror-image symmetrical double abdomen embryos. Development 113, 373–384
    OpenUrlAbstract
    1. Brown N. H.,
    2. Kafatos F. C.
    (1988) Functional cDNA libraries from Drosophila embryos. J. Mol. Biol 203, 425–437
    OpenUrlCrossRefPubMedWeb of Science
    1. Brown N. H.,
    2. King D. L.,
    3. Wilcox M.,
    4. Kafatos F. C.
    (1989) Developmentally regulated alternative splicing of Drosophila integrin Ps2-Alpha transcripts. Cell 59, 185–195
    OpenUrlCrossRefPubMedWeb of Science
    1. Chomczynski P.,
    2. Sacchi N.
    (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem 162, 156–159
    OpenUrlCrossRefPubMedWeb of Science
    1. Counce S. J.
    (1963) Developmental morphology of polar granules in Drosophila including observations on pole cell behavior and distribution during embryogenesis. J. Morphol 112, 129–145
    OpenUrlCrossRef
    1. Eddy E. M.
    (1975) Germ plasm and differentiation of the germ line. Int. Rev. Cytol 43, 229–280
    OpenUrlCrossRefPubMedWeb of Science
    1. Ephrussi A.,
    2. Dickinson L. K.,
    3. Lehmann R.
    (1991) oskar organizes the germ plasm and directs localization of the posterior determinant nanos. Cell 66, 37–50
    OpenUrlCrossRefPubMedWeb of Science
    1. Ephrussi A.,
    2. Lehmann R.
    (1992) Induction of germ cell formation by oskar. Nature 358, 387–392
    OpenUrlCrossRefPubMedWeb of Science
    1. Frohnhöfer H. G.,
    2. Lehmann R.,
    3. Nusslein-Volhard C.
    (1986) Manipulating the anteroposterior pattern of the Drosophila embryo. J. Embryol. Exp. Morph 97, 169–179
    OpenUrl
    1. Gerttula S.,
    2. Jin Y. S.,
    3. Anderson K. V.
    (1988) Zygotic expression and activity of the Drosophila Toll gene, a gene required maternally for embryonic dorsal-ventral pattern formation. Genetics 119, 123–133
    OpenUrlAbstract/FREE Full Text
    1. Golic K. G.,
    2. Lindquist S.
    (1989) The Flp recombinase of yeast catalyzes site-specific recombination in the Drosophila genome. Cell 59, 499–509
    OpenUrlCrossRefPubMedWeb of Science
    1. Golumbeski G. S.,
    2. Bardsley A.,
    3. Tax F.,
    4. Boswell R. E.
    (1991) tudor, a posterior-group gene in Drosophila melanogaster, encodes a novel protein and an mRNA that is localized during mid-oogenesis. Genes Dev 5, 2060–2070
    OpenUrlAbstract/FREE Full Text
    1. Hay B.,
    2. Ackerman L.,
    3. Barbel S.,
    4. Jan L. Y.,
    5. Jan Y. N.
    (1988) Identification of a component of Drosophila polar granules. Development 103, 625–640
    OpenUrlAbstract/FREE Full Text
    1. Hay B.,
    2. Jan L. Y.,
    3. Jan Y. N.
    (1988) A protein component of Drosophila polar granules is encoded by vasa and has extensive sequence similarity to ATP-dependent helicases. Cell 55, 577–587
    OpenUrlCrossRefPubMedWeb of Science
    1. Hegner R. W.
    (1909) The effects of centrifugal force upon the eggs of some Chrysomelid beetles. J. Exp. Zool 6, 507–552
    OpenUrlCrossRef
    1. Henikoff S.,
    2. Henikoff J. G.
    (1991) Automated assembly of protein blocks for database searching. Nucl. Acids Res 19, 6565–6572
    OpenUrlAbstract/FREE Full Text
    1. Illmensee K.,
    2. Mahowald A. P.
    (1974) Transplantation of posterior polar plasm in Drosophila. Induction of germ cells at the anterior pole of the egg. Proc. Natl. Acad. Sci. USA 71, 1016–1020
    OpenUrlAbstract/FREE Full Text
    1. Illmensee K.,
    2. Mahowald A. P.,
    3. Loomis M. R.
    (1976) The ontogeny of germ plasm during oogenesis in Drosophila. Dev. Biol 49, 40–65
    OpenUrlCrossRefPubMedWeb of Science
    1. Kim-Ha J.,
    2. Smith J. L.,
    3. Macdonald P. M.
    (1991) oskar messenger RNA is localized to the posterior pole of the Drosophila oocyte. Cell 66, 23–35
    OpenUrlCrossRefPubMedWeb of Science
    1. Kretz K. A.,
    2. Carson G. S.,
    3. O' Brien J. S.
    (1989) Direct sequencing from low-melt agarose with Sequenase. Nucl. Acids Res 117, 5864–.
    OpenUrl
    1. Lasko P. F.,
    2. Ashburner M.
    (1988) The product of the Drosophila gene vasa is very similar to eukaryotic initiation factor-4A. Nature 335, 611–617
    OpenUrlCrossRefPubMedWeb of Science
    1. Lasko P. F.,
    2. Ashburner M.
    (1990) Posterior localization of vasa protein correlates with, but is not sufficient for, pole cell development. Genes Dev 4, 905–921
    OpenUrlAbstract/FREE Full Text
    1. Lehmann R.,
    2. Nusslein-Volhard C.
    (1986) Abdominal segmentation, pole cell formation, and embryonic polarity require the localized activity of oskar, a maternal gene in Drosophila. Cell 47, 141–152
    OpenUrlCrossRefPubMedWeb of Science
    1. Lehmann R.,
    2. Nusslein-Volhard C.
    (1987) Involvement of the pumilio gene in the transport of an abdominal signal in the Drosophila embryo. Nature 329, 167–170
    OpenUrlCrossRef
    1. Lehmann R.,
    2. Nusslein-Volhard C.
    (1991) The maternal gene nanos has a central role in posterior pattern formation of the Drosophila embryo. Development 112, 679–691
    OpenUrlAbstract
    1. Macdonald P. M.
    (1992) The Drosophila pumilio gene: an unusually long transcription unit and an unusual protein. Development 114, 221–232
    OpenUrlAbstract
    1. Mahowald A. P.
    (1962) Fine structure of pole cells and polar granules in Drosophila melanogaster. J. Exp. Zool 151, 201–215
    OpenUrlCrossRef
    1. Manseau L. J.,
    2. Schupbach T.
    (1989) cappuccino and spire: two unique maternal-effect loci required for both the anteroposterior and dorsoventral patterns of the Drosophila embryo. Genes Dev 3, 1437–1452
    OpenUrlAbstract/FREE Full Text
    1. Mclean J. R.,
    2. Boswell R.,
    3. O'Donnell J.
    (1990) Cloning and molecular characterization of a metabolic gene with developmental functions in Drosophila. 1. Analysis of the head function of Punch. Genetics 126, 1007–1019
    OpenUrlAbstract/FREE Full Text
    1. O'Connell P.,
    2. Rosbash M.
    (1984) Sequence, structure, and codon preference of the Drosophila ribosomal protein 49 gene. Nucl. Acids Res 12, 5495–5513
    OpenUrlAbstract/FREE Full Text
    1. O'Donnell J.,
    2. Boswell R.,
    3. Reynolds T.,
    4. Mackay W.
    (1989) A cytogenetic analysis of the Punch-tudor region of chromosome 2R in Drosophila melanogaster. Genetics 121, 273–280
    OpenUrlAbstract/FREE Full Text
    1. Price J. V.,
    2. Clifford R. J.,
    3. Schupbach T.
    (1989) The maternal ventralizing locus torpedo is allelic to faint little ball, an embryonic lethal, and encodes the Drosophila EGF receptor homolog. Cell 56, 1085–1092
    OpenUrlCrossRefPubMed
    1. Robertson H. M.,
    2. Preston C. R.,
    3. Phillis R. W.,
    4. Johnson-Schlitz D. M.,
    5. Benz W. K.,
    6. Engels W. R.
    (1988) A stable genomic source of P element transposase in Drosophila melanogaster. Genetics 118, 461–470
    OpenUrlAbstract/FREE Full Text
    1. Roth S.,
    2. Hiromi Y.,
    3. Godt D.,
    4. Nusslein-Volhard C.
    (1991) cactus, a maternal gene required for proper formation of the dorsoventral morphogen gradient in Drosophila embryos. Development 112, 371–388
    OpenUrlAbstract
    1. Sander K.,
    2. Lehmann R.
    (1988) Drosophila nurse cells produce a posterior signal required for embryonic segmentation and polarity. Nature 335, 68–70
    OpenUrlCrossRefPubMed
    1. Sanger F.,
    2. Nicklen S.,
    3. Coulson A. R.
    (1977) DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74, 5463–5467
    OpenUrlAbstract/FREE Full Text
    1. Schauer I. E.,
    2. Wood W. B.
    (1990) Early C. elegans embryos are transcriptionally active. Development 110, 1303–1317
    OpenUrlAbstract/FREE Full Text
    1. Shaw G.,
    2. Kamen R.
    (1986) A conserved AU sequence from the 3untranslated region of GM-CSF mRNA mediates selective mRNA degradation. Cell 46, 659–667
    OpenUrlCrossRefPubMedWeb of Science
    1. St. Johnston D.,
    2. Driever W.,
    3. Berleth T.,
    4. Richstein S.,
    5. Nusslein-Volhard C.
    (1989) Multiple steps in the localization of bicoid RNA to the anterior pole of the Drosophila oocyte. Development 107, 13–19
    1. St. Johnston D.,
    2. Beuchle D.,
    3. Nusslein-Volhard C.
    (1991) staufen, a gene required to localize maternal RNAs in the Drosophila egg. Cell 66, 51–63
    OpenUrlCrossRefPubMedWeb of Science
    1. St. Johnston D.,
    2. Nusslein-Volhard C.
    (1992) The origin of pattern and polarity in the Drosophila embryo. Cell 68, 201–219
    OpenUrlCrossRefPubMedWeb of Science
    1. Tamkun J. W.,
    2. Kahn R. A.,
    3. Kissinger M.,
    4. Brizuela B. J.,
    5. Rulka C.,
    6. Scott M. P.,
    7. Kennison J. A.
    (1991) The arflike gene encodes an essential GTP-binding protein in Drosophila. Proc. Natl. Acad. Sci. USA 88, 3120–3124
    OpenUrlAbstract/FREE Full Text
    1. Tautz D.,
    2. Pfeifle C.
    (1989) A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma 98, 81–85
    OpenUrlCrossRefPubMedWeb of Science
    1. Wang C.,
    2. Lehmann R.
    (1991) nanos is the localized posterior determinant in Drosophila. Cell 66, 637–647
    OpenUrlCrossRefPubMedWeb of Science
    1. Wolf N.,
    2. Priess J.,
    3. Hirsch D.
    (1983) Segregation of germline granules in early embryos of Caenorhabditis elegans: an electron microscopic analysis. J. Embryol. Exp. Morph 73, 297–306
    OpenUrlPubMedWeb of Science
    1. Xue F.,
    2. Cooley L.
    (1993) kelch encodes a component of intercellular bridges in Drosophila egg chambers. Cell 72, 681–693
    OpenUrlCrossRefPubMedWeb of Science
    1. Zabin I.,
    2. Villarejo M. R.
    (1975) Protein complementation. Ann. Rev. Biochem 44, 295–313
    OpenUrlCrossRefPubMed
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JOURNAL ARTICLES
The mago nashi locus encodes an essential product required for germ plasm assembly in Drosophila
P.A. Newmark, R.E. Boswell
Development 1994 120: 1303-1313;
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