orb is required for anteroposterior and dorsoventral patterning during Drosophila oogenesis.
10.1101/gad.8.5.614
Crossref journal-article
Cold Spring Harbor Laboratory
Genes & Development (246)
Abstract

We describe mutations in the orb gene, identified previously as an ovarian-specific member of a large family of RNA-binding proteins. Strong orb alleles arrest oogenesis prior to egg chamber formation, an early step of oogenesis, whereas females mutant for a maternal-effect lethal orb allele lay eggs with ventralized eggshell structures. Embryos that develop within these mutant eggs display posterior patterning defects and abnormal dorsoventral axis formation. Consistent with such embryonic phenotypes, orb is required for the asymmetric distribution of oskar and gurken mRNAs within the oocyte during the later stages of oogenesis. In addition, double heterozygous combinations of orb and grk or orb and top/DER alleles reveal that mutations in these genes interact genetically, suggesting that they participate in a common pathway. Orb protein, which is localized within the oocyte in wild-type females, is distributed ubiquitously in stage 8-10 orb mutant oocytes. These data will be discussed in the context of a model proposing that Orb is a component of the cellular machinery that delivers mRNA molecules to specific locations within the oocyte and that this function contributes to both D/V and A/P axis specification during oogenesis.

Bibliography

Christerson, L. B., & McKearin, D. M. (1994). orb is required for anteroposterior and dorsoventral patterning during Drosophila oogenesis. Genes & Development, 8(5), 614–628.

Authors 2
  1. L B Christerson (first)
  2. D M McKearin (additional)
References 84 Referenced 165
  1. 10.1093/genetics/126.3.679 / Genetics / The genetics of a small autosomal region of Drosophila melanogaster containing the structural gene for alcohol dehydrogenase. VII. Characterization of the region around the snail and cactus loci. (1990)
  2. 10.1002/j.1460-2075.1988.tb03004.x / EMBO J. / The role of localization of bicoid RNA in organizing the anterior pattern of the Drosophila embryo. (1988)
  3. 10.1002/j.1460-2075.1982.tb01165.x / EMBO J. / Gene-dose titration analysis in the search of trans-regulatory genes in Drosophila. (1982)
  4. {'key': '2021111418130948000_8.5.614.4', 'first-page': '41', 'article-title': 'Studies on the events resulting in the formation of an egg chamber in Drosophila melanogaster.', 'volume': '28', 'year': '1964', 'journal-title': 'Growth'} / Growth / Studies on the events resulting in the formation of an egg chamber in Drosophila melanogaster. (1964)
  5. 10.1242/dev.114.3.653 / Development / Evidence for a highly selective RNA transport system and its role in establishing the dorsoventral axis of the Drosophila egg. (1992)
  6. 10.1093/genetics/123.4.771 / Genetics / Coordinately and differentially mutable activities of torpedo, the Drosophila melanogaster homolog of the vertebrate EGF receptor gene. (1989)
  7. 10.1093/genetics/119.4.829 / Genetics / Evidence that sisterless-a and sisterless-b are two of the several discrete “numerator elements” of the X/A sex determination signal in Drosophila that switch Sx1 between two alternative stable expression states. (1988)
  8. 10.1126/science.2830671
  9. 10.1016/0092-8674(92)90128-Y
  10. 10.1016/0012-1606(84)90162-3
  11. 10.1242/dev.115.4.989 / Development / 3′ Non-translated sequences in Drosophila cyclin B transcripts direct posterior pole accumulation late in oogenesis and peri-nuclear association in syncytial embryos. (1992)
  12. 10.1007/BF00398993
  13. 10.1016/0092-8674(88)90182-1
  14. 10.1038/358387a0
  15. {'key': '2021111418130948000_8.5.614.15', 'first-page': '37', 'article-title': 'oskar organizes the germ plasm and directs localization of the posterior determinant nanos.', 'volume': '766', 'year': '1991', 'journal-title': 'Cell'} / Cell / oskar organizes the germ plasm and directs localization of the posterior determinant nanos. (1991)
  16. 10.1016/0003-2697(84)90381-6
  17. 10.1016/0925-4773(93)90041-U
  18. 10.1016/0092-8674(86)90516-7
  19. 10.1101/gad.1.8.880
  20. {'key': '2021111418130948000_8.5.614.20', 'first-page': '2193', 'article-title': 'Relatedness of an RNA-binding motif in human immunodeficiency virus type 1 TAR RNA-binding protein TRBP to human P1/ds1 kinase and Drosophila Staufen.', 'volume': '13', 'year': '1993', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / Relatedness of an RNA-binding motif in human immunodeficiency virus type 1 TAR RNA-binding protein TRBP to human P1/ds1 kinase and Drosophila Staufen. (1993)
  21. 10.1016/0092-8674(92)90358-J
  22. 10.1073/pnas.77.10.5794
  23. 10.1242/dev.116.1.177 / Development / The neurogenic locus brainiac cooperates with the Drosophila EGF receptor to establish the ovarian follicle and to determine its dorsal-ventral polarity. (1992)
  24. 10.1002/j.1460-2075.1987.tb04822.x / EMBO J. / Oocyte-specific transcription of fs(1)fs(1)K10: A Drosophila gene affecting dorsal-ventral developmental polarity. (1987)
  25. 10.1016/0092-8674(85)90232-6
  26. 10.1016/0168-9525(91)90254-F
  27. 10.1016/0925-4773(91)90047-A
  28. 10.1242/dev.105.3.605 / Development / Patterns of engrailed protein in early Drosophila embryos. (1989)
  29. 10.1101/gad.7.6.948
  30. 10.1016/0968-0004(91)90088-D
  31. {'key': '2021111418130948000_8.5.614.31', 'first-page': '174', 'article-title': 'Isolation of RRM-type RNA-binding protein genes and the analysis of their relatedness by using a numerical approach.', 'volume': '13', 'year': '1993', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / Isolation of RRM-type RNA-binding protein genes and the analysis of their relatedness by using a numerical approach. (1993)
  32. 10.1016/0092-8674(91)90136-M
  33. 10.1242/dev.119.1.169 / Development / Multiple RNA regulatory elements mediate distinct steps in localization of oskar mRNA. (1993)
  34. King, R.C. 1970. Ovarian development in Drosophila melanogaster. Academic Press, New York.
  35. 10.1242/dev.115.1.75 / Development / The Drosophila orb gene is predicted to encode sex-specific germline RNA-binding proteins and has localized transcripts in ovaries and early embryos. (1992)
  36. Lantz, V., Chang, J.S. Horabin, J.I. Bopp, D. and Schedl. P. 1994. The Drosophila orb RNA-binding protein is required for the formation of the egg chamber and establishment of polarity. Genes & Dev. 00: (this issue). (10.1101/gad.8.5.598)
  37. 10.1002/bies.950140802
  38. 10.1016/S0959-437X(05)80169-8
  39. 10.1016/0092-8674(86)90375-2
  40. Lindsley, D.L. and G.G. Zimm. 1992. The genome of Drosophila melanogaster. Academic Press, San Diego, CA.
  41. Mahowald, A.P. and M.P. Kambysellis. 1980. Oogenesis. In The genetics and biology of Drosophila (ed. M. Ashburner and T.R.F. Wright), vol. 2, pp. 141–224. Academic Press, New York.
  42. 10.1083/jcb.45.2.306
  43. 10.1101/gad.3.9.1437
  44. 10.1101/gad.4.12b.2242
  45. 10.1126/science.1925585
  46. 10.1016/0092-8674(93)90688-M
  47. Pirrotta, V. 1986. Cloning Drosophila genes. In Drosophila: A practical approach (ed. D.B. Roberts), pp. 83–110. IRL Press, Washington, D.C.
  48. 10.1016/0092-8674(89)90641-7
  49. 10.1093/genetics/125.1.77 / Genetics / Interacting genes that affect microtubule function in Drosophila melanogaster: Two classes of mutation revert the failure to complement between haync2 and mutations in tubulin genes. (1990)
  50. 10.1007/BF00333281
  51. {'key': '2021111418130948000_8.5.614.51', 'first-page': '84', 'article-title': 'Exon definition may facilitate splice site selection in RNAs with multiple exons.', 'volume': '10', 'year': '1990', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / Exon definition may facilitate splice site selection in RNAs with multiple exons. (1990)
  52. 10.1093/genetics/118.3.461 / Genetics / A stable genomic source of P element transposase in Drosophila melanogaster. (1988)
  53. 10.1016/0092-8674(89)90774-5
  54. 10.1016/0168-9525(91)90258-R
  55. 10.1016/0092-8674(93)90273-S
  56. 10.1016/0092-8674(89)90772-1
  57. Sambrook, J., E.F. Fritsch, and T. Maniatis. 1989. Molecular cloning: A laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
  58. 10.1016/0092-8674(89)90642-9
  59. 10.1016/0092-8674(87)90546-0
  60. 10.1007/BF00376063
  61. 10.1093/genetics/129.4.1119 / Genetics / Female sterile mutations on the second chromosome of Drosophila melanogaster. II. Mutations blocking oogenesis or altering egg morphology. (1991)
  62. Schüpbach, T., R.J. Clifford, L.J. Manseau, and J.V. Price. 1991. Dorsoventral signaling processes in Drosophila oogenesis. In Cell-cell interactions in early development (ed. J. Gerhart), pp. 163–174. Wiley and Sons, Inc., New York.
  63. 10.1016/0092-8674(93)90393-5
  64. Spradling, A.C. Developmental genetics of oogenesis. In The development of Drosophila melanogaster (ed. M. Bate and A. Martinez-Arias), pp. 1–70. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
  65. 10.1016/0092-8674(92)90181-B
  66. 10.1016/0092-8674(91)90381-8
  67. 10.1016/0012-1606(71)90043-1
  68. 10.1016/0092-8674(89)90773-3
  69. 10.1016/0092-8674(88)90035-9
  70. 10.1016/0092-8674(92)90466-P
  71. 10.1242/dev.107.Supplement.13 / Development / Multiple steps in the localization of bicoid RNA to the anterior pole of the Drosophila oocyte. (1989)
  72. 10.1016/0092-8674(91)90138-O
  73. 10.1073/pnas.89.22.10979
  74. 10.1101/gad.3.12a.1957
  75. {'key': '2021111418130948000_8.5.614.75', 'first-page': '6299', 'article-title': 'Effect of 5′ splice site mutations on splicing of the preceding intron.', 'volume': '10', 'year': '1990', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / Effect of 5′ splice site mutations on splicing of the preceding intron. (1990)
  76. 10.1016/0092-8674(92)90191-E
  77. 10.1007/BF00291041
  78. 10.1242/dev.115.4.923 / Development / Reorganization of the cytoskeleton during Drosophila oogenesis: Implications for axis specification and intercellular transport. (1992)
  79. 10.1002/j.1460-2075.1989.tb08459.x / EMBO J. / The scute (T4) gene acts as a numerator element of the X:A signal that determines the state of activity of Sex-lethal in Drosophila. (1989)
  80. 10.1016/0092-8674(91)90110-K
  81. Wieschaus, E. and C. Nüsslein-Volhard. 1986. Looking at embryos. In Drosophila: A practical approach (ed. D.B. Roberts), pp. 199–227. IRL Press, Washington D.C.
  82. 10.1007/BF00848670
  83. 10.1016/0092-8674(93)90397-9
  84. 10.1101/gad.6.12b.2443
Dates
Type When
Created 18 years, 2 months ago (June 5, 2007, 5:15 p.m.)
Deposited 3 years, 9 months ago (Nov. 14, 2021, 9:19 p.m.)
Indexed 2 weeks, 3 days ago (Aug. 7, 2025, 4:56 a.m.)
Issued 31 years, 5 months ago (March 1, 1994)
Published 31 years, 5 months ago (March 1, 1994)
Published Online 31 years, 5 months ago (March 1, 1994)
Published Print 31 years, 5 months ago (March 1, 1994)
Funders 0

None

@article{Christerson_1994, title={orb is required for anteroposterior and dorsoventral patterning during Drosophila oogenesis.}, volume={8}, ISSN={1549-5477}, url={http://dx.doi.org/10.1101/gad.8.5.614}, DOI={10.1101/gad.8.5.614}, number={5}, journal={Genes & Development}, publisher={Cold Spring Harbor Laboratory}, author={Christerson, L B and McKearin, D M}, year={1994}, month=mar, pages={614–628} }