Advertisement
JOURNAL ARTICLES
Oocyte determination and the origin of polarity in Drosophila: the role of the spindle genes
A. Gonzalez-Reyes, H. Elliott, D. St Johnston
Development 1997 124: 4927-4937;

Summary

The two main body axes in Drosophila become polarised as a result of a series of symmetry-breaking steps during oogenesis. Two of the sixteen germline cells in each egg chamber develop as pro-oocytes, and the first asymmetry arises when one of these cells is selected to become the oocyte. Anterior-posterior polarity originates when the oocyte then comes to lie posterior to the nurse cells and signals through the Gurken/Egfr pathway to induce the adjacent follicle cells to adopt a posterior fate. This directs the movement of the germinal vesicle and associated gurken mRNA from the posterior to an anterior corner of the oocyte, where Gurken protein signals for a second time to induce the dorsal follicle cells, thereby polarising the dorsal-ventral axis. Here we describe a group of five genes, the spindle loci, which are required for each of these polarising events. spindle mutants inhibit the induction of both the posterior and dorsal follicle cells by disrupting the localisation and translation of gurken mRNA. Moreover, the oocyte often fails to reach the posterior of mutant egg chambers and differentiates abnormally. Finally, double mutants cause both pro-oocytes to develop as oocytes, by delaying the choice between these two cells. Thus, these mutants reveal a novel link between oocyte selection, oocyte positioning and axis formation in Drosophila, leading us to propose that the spindle genes act in a process that is common to several of these events.

REFERENCES

    1. Carpenter A.
    (1975) Electron microscopy of meiosis in Drosophila melanogaster females. I. Structure, arrangement, and temporal change of the synaptonemal complex in wild-type. Chromosoma 51, 157–182
    OpenUrlCrossRefPubMedWeb of Science
    1. Carpenter A.
    (1979) Synaptonemal complex and recombination nodules in wild-type Drosophilamelanogaster females. Genetics 92, 511–541
    OpenUrlAbstract/FREE Full Text
    1. Chou T.-B.,
    2. Noll E.,
    3. Perrimon N.
    (1993) Autosomal P[ovoD1] dominant female-sterile insertions in Drosophila and their use in generating germ-line chimeras. Development 119, 1359–1369
    OpenUrlAbstract
    1. Christerson L.,
    2. McKearin D.
    (1994) orb is required for anteroposterior and dorsoventral patterning during Drosophila oogenesis. Genes Dev 8, 614–628
    OpenUrlAbstract/FREE Full Text
    1. Clark I.,
    2. Giniger E.,
    3. Ruohola-Baker H.,
    4. Jan L.,
    5. Jan Y.
    (1994) Transient posterior localisation of a kinesin fusion protein reflects anteroposterior polarity of the Drosophila oocyte. Current Biology 4, 289–300
    OpenUrlCrossRefPubMedWeb of Science
    1. Clark I.,
    2. Jan L. Y.,
    3. Jan Y. N.
    (1997) Reciprocal localization of Nod and kinesin fusion proteins indicates microtubule polarity in the Drosophila oocyte, epithelium, neuron and muscle. Development 124, 461–470
    OpenUrlAbstract
    1. de Cuevas M.,
    2. Lee J.,
    3. Spradling A.
    (1996) -spectrin is required for germline division and differentiation in the Drosophila ovary. Development 122, 3959–3968
    OpenUrlAbstract
    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. Gavis E. R.,
    2. Lunsford L.,
    3. Bergsten S. E.,
    4. Lehmann R.
    (1996) A conserved 90 nucleotide element mediates translational repression of nanos RNA. Development 122, 2791–2800
    OpenUrlAbstract
    1. Gillespie D.,
    2. Berg C.
    (1995) homeless is required for RNA localization in Drosophila oogenesis and encodes a new member of the DE-H family of RNA-dependent ATPases. Genes Dev 9, 2495–2508
    OpenUrlAbstract/FREE Full Text
    1. González-Reyes A.,
    2. St Johnston D.
    (1994) Role of oocyte positioning in establishment of anterior-posterior polarity in Drosophila. Science 266, 639–642
    OpenUrlAbstract/FREE Full Text
    1. González-Reyes A.,
    2. Elliott H.,
    3. St Johnston D.
    (1995) Polarization of both major body axes in Drosophila by gurken-torpedo signalling. Nature 375, 654–658
    OpenUrlCrossRefPubMedWeb of Science
    1. Goode S.,
    2. Wright D.,
    3. Mahowald A.
    (1992) The neurogenic locus brainiac cooperates with the Drosophila EGF receptor to establish the ovarian follicle and determine its dorsal-ventral polarity. Development 116, 177–192
    OpenUrlAbstract
    1. Keyes L.,
    2. Spradling A.
    (1997) The Drosophila gene fs(2)cup interacts with otu to define a cytoplasmic pathway required for the structure and function of germ-line chromosomes. Development 124, 1419–1431
    OpenUrlAbstract
    1. Kim-Ha J.,
    2. Kerr K.,
    3. Macdonald P.
    (1995) Translational regulation of oskar mRNA by bruno, an ovarian RNA-binding protein, is essential. Cell 81, 403–412
    OpenUrlCrossRefPubMedWeb of Science
    1. Koch E.,
    2. Smith P.,
    3. King R.
    (1967) The division and differentiation of Drosophila cystocytes. J. Morph 121, 55–70
    OpenUrlCrossRefPubMedWeb of Science
    1. Koch E.,
    2. King R.
    (1969) Further studies on the ring canal system of the ovarian cystocytes of Drosophilamelanogaster. Z. Zellforsch 102, 129–152
    OpenUrlCrossRefPubMed
    1. Koch E.,
    2. Spitzer R.
    (1983) Multiple effects of colchicine on oogenesis in Drosophila; Induced sterility and switch of potencial oocyte to nurse-cell developmental pathway. Cell Tissue Res 228, 21–32
    OpenUrlPubMedWeb of Science
    1. Lantz V.,
    2. Chang J.,
    3. Horabin J.,
    4. Bopp D.,
    5. Schedl P.
    (1994) The Drosophila orb RNA-binding protein is required for the formation of the egg chamber and establishment of polarity. Genes Dev 8, 598–613
    OpenUrlAbstract/FREE Full Text
    1. Lilly M.,
    2. Spradling A.
    (1996) The Drosophila endocycle is controlled by cyclin E and lacks a checkpoint ensuring S-phase completition. Genes Dev 10, 2514–2526
    OpenUrlAbstract/FREE Full Text
    1. Lin H.,
    2. Yue L.,
    3. Spradling A.
    (1994) The Drosophila fusome, a germline-specific organelle, contains membrane skeletal proteins and functions in cyst formation. Development 120, 947–956
    OpenUrlAbstract
    1. Lin H.,
    2. Spradling A.
    (1995) Fusome asymmetry and oocyte determination in Drosophila. Dev. Genetics 16, 6–12
    OpenUrlCrossRefPubMedWeb of Science
    1. Mach J. M.,
    2. Lehmann R.
    (1997) An Egalitarian-BicaudalD complex is essential for oocyte specification and axis determination in Drosophila. Genes Dev 11, 423–435
    OpenUrlAbstract/FREE Full Text
    1. Mahowald A. P.,
    2. Strassheim J. M.
    (1970) Intercellular migration of centrioles in the germarium of Drosophila melanogaster. J. Cell. Biol 45, 306–320
    OpenUrlAbstract/FREE Full Text
    1. McKearin D.,
    2. Ohlstein B.
    (1995) A role for the Drosophila Bag-of marbles protein in the differentiation of cystoblast from germline stem cells. Development 121, 2937–2947
    OpenUrlAbstract
    1. Mohler J.,
    2. Wieschaus E.
    (1986) Dominant maternal-effect mutations of Drosophila melanogaster causing the production of double-abdomen embryos. Genetics 112, 803–822
    OpenUrlAbstract/FREE Full Text
    1. Montell D.,
    2. Rorth P.,
    3. Spradling A.
    (1992) slow border cells, a locus required for a developmentally regulated cell migration during oogenesis, encodes Drosophila C/EBP. Cell 71, 51–62
    OpenUrlCrossRefPubMedWeb of Science
    1. Neuman-Silberberg F.,
    2. Schupbach T.
    (1993) The Drosophila dorsoventral patterning gene gurken produces a dorsally localized RNA and encodes a TGFlike protein. Cell 75, 165–174
    OpenUrlCrossRefPubMedWeb of Science
    1. Neuman-Silberberg F. S.,
    2. Schupbach T.
    (1996) The Drosophila TGF-like protein Gurken: expression and cellular localization during Drosophila oogenesis. Mech. Dev 59, 105–113
    OpenUrlCrossRefPubMedWeb of Science
    1. Pokrywka N. J.,
    2. Stephenson E. C.
    (1991) Microtubules mediate the localization of bicoid RNA during Drosophila oogenesis. Development 113, 55–66
    OpenUrlAbstract
    1. Pokrywka N.,
    2. Stephenson E.
    (1995) Microtubules are a general component of mRNA localization systems in Drosophila oocytes. Dev. Biol 167, 363–370
    OpenUrlCrossRefPubMedWeb of Science
    1. Price J.,
    2. Clifford R.,
    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. Ran B.,
    2. Bopp R.,
    3. Suter B.
    (1994) Null alleles reveal novel requirements for Bic-D during Drosophila oogenesis and zygotic development. Development 120, 1233–1242
    OpenUrlAbstract
    1. Rasmussen S.
    (1974) Studies on the development of the synaptinemal complex in Drosophilamelanogaster. C. R. Trav. Lab. Carlsberg 39, 443–468
    OpenUrl
    1. Roth S.,
    2. Neuman-Shilberberg F.,
    3. Barcelo G.,
    4. Schupbach T.
    (1995) cornichon and the EGF receptor signaling process are necessary for both anterior-posterior and dorsal-ventral pattern formation in Drosophila. Cell 81, 967–978
    OpenUrlCrossRefPubMedWeb of Science
    1. Ruohola H.,
    2. Bremer K.,
    3. Baker D.,
    4. Swedlow J.,
    5. Jan L.,
    6. Jan Y.
    (1991) Role of neurogenic genes in establishment of follicle cell fate and oocyte polarity during oogenesis in Drosophila. Cell 66, 433–449
    OpenUrlCrossRefPubMedWeb of Science
    1. Schejter E.,
    2. Shilo B.-Z.
    (1989) The Drosophila EGF receptor homolog (DER) gene is allelic to faint little ball, a locus essential for embryonic development. Cell 56, 1093–1104
    OpenUrlCrossRefPubMedWeb of Science
    1. Schmekel K.,
    2. Wahrman J.,
    3. Daneholt B.
    (1993) Solitary and synaptonemal complex-associated recombination nodules in pro-nurse cells during oogenesis in Drosophilamelanogaster. Chromosoma 102, 396–402
    OpenUrlCrossRefPubMed
    1. Schmid S. R.,
    2. Linder P.
    (1992) D-E-A-D protein family of putative RNA helicases. Mol. Microbiol 6, 283–292
    OpenUrlCrossRefPubMedWeb of Science
    1. Schupbach T.
    (1987) Germ line and soma cooperate during oogenesis to establish the dorsoventral pattern of egg shell and embryo in Drosophila melanogaster. Cell 49, 699–707
    OpenUrlCrossRefPubMedWeb of Science
    1. Schupbach T.,
    2. Wieschaus E.
    (1991) Female sterile mutations on the second chromosome of Drosophilamelanogaster. II. Mutations blocking oogenesis or altering egg morphology. Genetics 129, 1119–1136
    OpenUrlAbstract/FREE Full Text
    1. Serano T.,
    2. Karlin-McGinness M.,
    3. Cohen R.
    (1995) The role of fs(1)K10 in the localization of the mRNA of the TGFhomolog gurken within the Drosophila oocyte. Mech. Dev 51, 183–192
    OpenUrlCrossRefPubMed
    1. St Johnston D.,
    2. Beuchle D.,
    3. Nusslein-Volhard C.
    (1991) staufen, a gene required to localise maternal RNAs in the Drosophila egg. Cell 66, 51–63
    OpenUrlCrossRefPubMedWeb of Science
    1. Suter B.,
    2. Romberg L.,
    3. Steward R.
    (1989) Bicaudal-D, a Drosophila gene involved in developmental asymmetry: localized transcript accumulation in ovaries and sequence similarity to myosin heavy chain tail domains. Genes Dev 3, 1957–1968
    OpenUrlAbstract/FREE Full Text
    1. Suter B.,
    2. Steward R.
    (1991) Requirement for phosphorylation and localization of the Bicaudal-D protein in Drosophila oocyte differentiation. Cell 67, 917–926
    OpenUrlCrossRefPubMedWeb of Science
    1. Swan A.,
    2. Suter B.
    (1996) Role of Bicaudal-D in patterning the Drosophila egg chamber in mid-oogenesis. Development 122, 3577–3586
    OpenUrlAbstract
    1. Tearle R.,
    2. Nusslein-Volhard C.
    (1987) Tubingen mutants stocklist. Drosophila Inform. Service 66, 209–226
    OpenUrl
    1. Theurkauf W.,
    2. Smiley S.,
    3. Wong M.,
    4. Alberts B.
    (1992) Reorganization of the cytoskeleton during Drosophila oogenesis: implications for axis specification and intercellular transport. Development 115, 923–936
    OpenUrlAbstract
    1. Theurkauf W.,
    2. Alberts M.,
    3. Jan Y.,
    4. Jongens T.
    (1993) A central role for microtubules in the differentiation of Drosophila oocytes. Development 118, 1169–1180
    OpenUrlAbstract/FREE Full Text
    1. Theurkauf W.
    (1994) Microtubules and cytoplasmic organization during Drosophila oogenesis. Dev. Biol 165, 352–360
    OpenUrlCrossRefPubMed
    1. Wharton R. P.,
    2. Struhl G.
    (1989) Structure of the DrosophilaBicaudal-D protein and its role in localizing the posterior determinant nanos. Cell 59, 881–892
    OpenUrlCrossRefPubMedWeb of Science
    1. Wilson J.,
    2. Connell J.,
    3. Macdonald P.
    (1996) aubergine enhances oskar translation in the Drosophila ovary. Development 122, 1631–1639
    OpenUrlAbstract
Back to top

 Download PDF

Email
JOURNAL ARTICLES
Oocyte determination and the origin of polarity in Drosophila: the role of the spindle genes
A. Gonzalez-Reyes, H. Elliott, D. St Johnston
Development 1997 124: 4927-4937;
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
Alerts

Article navigation

Other journals from The Company of Biologists

Advertisement

An interview with Swathi Arur

Swathi Arur joined the team at Development as an Academic Editor in 2020. Her lab uses multidisciplinary approaches to understand female germline development and fertility. We met with her over Zoom to hear more about her life, her career and her love for C. elegans.

Jim Wells and Hanna Mikkola join our team of Editors

We are pleased to welcome James (Jim) Wells and Hanna Mikkola to our team of Editors. Jim joins us a new Academic Editor, taking over from Gordan Keller, and Hanna joins our team of Associate Editors. Find out more about their research interests and areas of expertise.

New funding scheme supports sustainable events

As part of our Sustainable Conferencing Initiative, we are pleased to announce funding for organisers that seek to reduce the environmental footprint of their event. The next deadline to apply for a Scientific Meeting grant is 26 March 2021.

Read & Publish participation continues to grow

“I’d heard of Read & Publish deals and knew that many universities, including mine, had signed up to them but I had not previously understood the benefits that these deals bring to authors who work at those universities.”

Professor Sally Lowell (University of Edinburgh) shares her experience of publishing Open Access as part of our growing Read & Publish initiative. We now have over 150 institutions in 15 countries and four library consortia taking part – find out more and view our full list of participating institutions.

Upcoming special issues

Imaging Development, Stem Cells and Regeneration
Submission deadline: 30 March 2021
Publication: mid-2021

The Immune System in Development and Regeneration
Guest editors: Florent Ginhoux and Paul Martin
Submission deadline: 1 September 2021
Publication: Spring 2022

Both special issues welcome Review articles as well as Research articles, and will be widely promoted online and at key global conferences.

Development presents...

Our successful webinar series continues into 2021, with early-career researchers presenting their papers and a chance to virtually network with the developmental biology community afterwards. Here, Brandon Carpenter talks about how inherited histone methylation defines the germline versus soma decision in C. elegans. 

Sign up to join our next session:

10 March
Time: TBC
Chaired by: Thomas Lecuit