Skip to main content
Genetics logoLink to Genetics
. 2001 May;158(1):253–263. doi: 10.1093/genetics/158.1.253

Embryonic expression of the divergent Drosophila beta3-tubulin isoform is required for larval behavior.

R W Dettman 1, F R Turner 1, H D Hoyle 1, E C Raff 1
PMCID: PMC1461636  PMID: 11333234

Abstract

We have sought to define the developmental and cellular roles played by differential expression of distinct beta-tubulins. Drosophila beta3-tubulin (beta3) is a structurally divergent isoform transiently expressed during midembryogenesis. Severe beta3 mutations cause larval lethality resulting from failed gut function and consequent starvation. However, mutant larvae also display behavioral abnormalities consistent with defective sensory perception. We identified embryonic beta3 expression in several previously undefined sites, including different types of sensory organs. We conclude that abnormalities in foraging behavior and photoresponsiveness exhibited by prelethal mutant larvae reflect defective beta3 function in the embryo during development of chordotonal and other mechanosensory organs and of Bolwig's organ and nerve. We show that microtubule organization in the cap cells of chordotonal organs is altered in mutant larvae. Thus transient zygotic beta3 expression has permanent consequences for the architecture of the cap cell microtubule cytoskeleton in the larval sensilla, even when beta3 is no longer present. Our data provide a link between the microtubule cytoskeleton in embryogenesis and the behavioral phenotype manifested as defective proprioreception at the larval stage.

Full Text

The Full Text of this article is available as a PDF (534.3 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Andres A. J., Fletcher J. C., Karim F. D., Thummel C. S. Molecular analysis of the initiation of insect metamorphosis: a comparative study of Drosophila ecdysteroid-regulated transcription. Dev Biol. 1993 Dec;160(2):388–404. doi: 10.1006/dbio.1993.1315. [DOI] [PubMed] [Google Scholar]
  2. Bier E., Vaessin H., Shepherd S., Lee K., McCall K., Barbel S., Ackerman L., Carretto R., Uemura T., Grell E. Searching for pattern and mutation in the Drosophila genome with a P-lacZ vector. Genes Dev. 1989 Sep;3(9):1273–1287. doi: 10.1101/gad.3.9.1273. [DOI] [PubMed] [Google Scholar]
  3. Brendza R. P., Serbus L. R., Duffy J. B., Saxton W. M. A function for kinesin I in the posterior transport of oskar mRNA and Staufen protein. Science. 2000 Sep 22;289(5487):2120–2122. doi: 10.1126/science.289.5487.2120. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Campos A. R., Lee K. J., Steller H. Establishment of neuronal connectivity during development of the Drosophila larval visual system. J Neurobiol. 1995 Nov;28(3):313–329. doi: 10.1002/neu.480280305. [DOI] [PubMed] [Google Scholar]
  5. Carlson S. D., Hilgers S. L., Juang J. L. Ultrastructure and blood-nerve barrier of chordotonal organs in the Drosophila embryo. J Neurocytol. 1997 Jun;26(6):377–388. doi: 10.1023/a:1018564904170. [DOI] [PubMed] [Google Scholar]
  6. Casso D., Ramírez-Weber F. A., Kornberg T. B. GFP-tagged balancer chromosomes for Drosophila melanogaster. Mech Dev. 1999 Nov;88(2):229–232. doi: 10.1016/s0925-4773(99)00174-4. [DOI] [PubMed] [Google Scholar]
  7. Damm C., Wolk A., Buttgereit D., Löher K., Wagner E., Lilly B., Olson E. N., Hasenpusch-Theil K., Renkawitz-Pohl R. Independent regulatory elements in the upstream region of the Drosophila beta 3 tubulin gene (beta Tub60D) guide expression in the dorsal vessel and the somatic muscles. Dev Biol. 1998 Jul 1;199(1):138–149. doi: 10.1006/dbio.1998.8916. [DOI] [PubMed] [Google Scholar]
  8. Fackenthal J. D., Turner F. R., Raff E. C. Tissue-specific microtubule functions in Drosophila spermatogenesis require the beta 2-tubulin isotype-specific carboxy terminus. Dev Biol. 1993 Jul;158(1):213–227. doi: 10.1006/dbio.1993.1180. [DOI] [PubMed] [Google Scholar]
  9. Foe V. E., Field C. M., Odell G. M. Microtubules and mitotic cycle phase modulate spatiotemporal distributions of F-actin and myosin II in Drosophila syncytial blastoderm embryos. Development. 2000 May;127(9):1767–1787. doi: 10.1242/dev.127.9.1767. [DOI] [PubMed] [Google Scholar]
  10. Fujita S. C., Zipursky S. L., Benzer S., Ferrús A., Shotwell S. L. Monoclonal antibodies against the Drosophila nervous system. Proc Natl Acad Sci U S A. 1982 Dec;79(24):7929–7933. doi: 10.1073/pnas.79.24.7929. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gasch A., Hinz U., Leiss D., Renkawitz-Pohl R. The expression of beta 1 and beta 3 tubulin genes of Drosophila melanogaster is spatially regulated during embryogenesis. Mol Gen Genet. 1988 Jan;211(1):8–16. doi: 10.1007/BF00338387. [DOI] [PubMed] [Google Scholar]
  12. Gasch A., Hinz U., Renkawitz-Pohl R. Intron and upstream sequences regulate expression of the Drosophila beta 3-tubulin gene in the visceral and somatic musculature, respectively. Proc Natl Acad Sci U S A. 1989 May;86(9):3215–3218. doi: 10.1073/pnas.86.9.3215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gorczyca M. G., Phillis R. W., Budnik V. The role of tinman, a mesodermal cell fate gene, in axon pathfinding during the development of the transverse nerve in Drosophila. Development. 1994 Aug;120(8):2143–2152. doi: 10.1242/dev.120.8.2143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hartenstein V., Posakony J. W. Development of adult sensilla on the wing and notum of Drosophila melanogaster. Development. 1989 Oct;107(2):389–405. doi: 10.1242/dev.107.2.389. [DOI] [PubMed] [Google Scholar]
  15. Hinz U., Wolk A., Renkawitz-Pohl R. Ultrabithorax is a regulator of beta 3 tubulin expression in the Drosophila visceral mesoderm. Development. 1992 Nov;116(3):543–554. doi: 10.1242/dev.116.3.543. [DOI] [PubMed] [Google Scholar]
  16. Hoyle H. D., Hutchens J. A., Turner F. R., Raff E. C. Regulation of beta-tubulin function and expression in Drosophila spermatogenesis. Dev Genet. 1995;16(2):148–170. doi: 10.1002/dvg.1020160208. [DOI] [PubMed] [Google Scholar]
  17. Hoyle H. D., Raff E. C. Two Drosophila beta tubulin isoforms are not functionally equivalent. J Cell Biol. 1990 Sep;111(3):1009–1026. doi: 10.1083/jcb.111.3.1009. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hoyle H. D., Turner F. R., Raff E. C. A transient specialization of the microtubule cytoskeleton is required for differentiation of the Drosophila visual system. Dev Biol. 2000 May 15;221(2):375–389. doi: 10.1006/dbio.2000.9674. [DOI] [PubMed] [Google Scholar]
  19. Hummel T., Krukkert K., Roos J., Davis G., Klämbt C. Drosophila Futsch/22C10 is a MAP1B-like protein required for dendritic and axonal development. Neuron. 2000 May;26(2):357–370. doi: 10.1016/s0896-6273(00)81169-1. [DOI] [PubMed] [Google Scholar]
  20. Hutchens J. A., Hoyle H. D., Turner F. R., Raff E. C. Structurally similar Drosophila alpha-tubulins are functionally distinct in vivo. Mol Biol Cell. 1997 Mar;8(3):481–500. doi: 10.1091/mbc.8.3.481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Iyengar B., Roote J., Campos A. R. The tamas gene, identified as a mutation that disrupts larval behavior in Drosophila melanogaster, codes for the mitochondrial DNA polymerase catalytic subunit (DNApol-gamma125). Genetics. 1999 Dec;153(4):1809–1824. doi: 10.1093/genetics/153.4.1809. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kimble M., Dettman R. W., Raff E. C. The beta 3-tubulin gene of Drosophila melanogaster is essential for viability and fertility. Genetics. 1990 Dec;126(4):991–1005. doi: 10.1093/genetics/126.4.991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kimble M., Incardona J. P., Raff E. C. A variant beta-tubulin isoform of Drosophila melanogaster (beta 3) is expressed primarily in tissues of mesodermal origin in embryos and pupae, and is utilized in populations of transient microtubules. Dev Biol. 1989 Feb;131(2):415–429. doi: 10.1016/s0012-1606(89)80014-4. [DOI] [PubMed] [Google Scholar]
  24. Lehmann R. Cell-cell signaling, microtubules, and the loss of symmetry in the Drosophila oocyte. Cell. 1995 Nov 3;83(3):353–356. doi: 10.1016/0092-8674(95)90111-6. [DOI] [PubMed] [Google Scholar]
  25. Leiss D., Hinz U., Gasch A., Mertz R., Renkawitz-Pohl R. Beta 3 tubulin expression characterizes the differentiating mesodermal germ layer during Drosophila embryogenesis. Development. 1988 Dec;104(4):525–531. doi: 10.1242/dev.104.4.525. [DOI] [PubMed] [Google Scholar]
  26. Lüer K., Urban J., Klämbt C., Technau G. M. Induction of identified mesodermal cells by CNS midline progenitors in Drosophila. Development. 1997 Jul;124(14):2681–2690. doi: 10.1242/dev.124.14.2681. [DOI] [PubMed] [Google Scholar]
  27. Mathe E., Boros I., Josvay K., Li K., Puro J., Kaufman T. C., Szabad J. The Tomaj mutant alleles of alpha Tubulin67C reveal a requirement for the encoded maternal specific tubulin isoform in the sperm aster, the cleavage spindle apparatus and neurogenesis during embryonic development in Drosophila. J Cell Sci. 1998 Apr;111(Pt 7):887–896. doi: 10.1242/jcs.111.7.887. [DOI] [PubMed] [Google Scholar]
  28. Matthews K. A., Rees D., Kaufman T. C. A functionally specialized alpha-tubulin is required for oocyte meiosis and cleavage mitoses in Drosophila. Development. 1993 Mar;117(3):977–991. doi: 10.1242/dev.117.3.977. [DOI] [PubMed] [Google Scholar]
  29. Nogales E., Whittaker M., Milligan R. A., Downing K. H. High-resolution model of the microtubule. Cell. 1999 Jan 8;96(1):79–88. doi: 10.1016/s0092-8674(00)80961-7. [DOI] [PubMed] [Google Scholar]
  30. Nogales E., Wolf S. G., Downing K. H. Structure of the alpha beta tubulin dimer by electron crystallography. Nature. 1998 Jan 8;391(6663):199–203. doi: 10.1038/34465. [DOI] [PubMed] [Google Scholar]
  31. Osborne K. A., Robichon A., Burgess E., Butland S., Shaw R. A., Coulthard A., Pereira H. S., Greenspan R. J., Sokolowski M. B. Natural behavior polymorphism due to a cGMP-dependent protein kinase of Drosophila. Science. 1997 Aug 8;277(5327):834–836. doi: 10.1126/science.277.5327.834. [DOI] [PubMed] [Google Scholar]
  32. Raff E. C., Fackenthal J. D., Hutchens J. A., Hoyle H. D., Turner F. R. Microtubule architecture specified by a beta-tubulin isoform. Science. 1997 Jan 3;275(5296):70–73. doi: 10.1126/science.275.5296.70. [DOI] [PubMed] [Google Scholar]
  33. Raff E. C., Fuller M. T., Kaufman T. C., Kemphues K. J., Rudolph J. E., Raff R. A. Regulation of tubulin gene expression during embryogenesis in Drosophila melanogaster. Cell. 1982 Jan;28(1):33–40. doi: 10.1016/0092-8674(82)90372-5. [DOI] [PubMed] [Google Scholar]
  34. Raff E. C., Hutchens J. A., Hoyle H. D., Nielsen M. G., Turner F. R. Conserved axoneme symmetry altered by a component beta-tubulin. Curr Biol. 2000 Nov 2;10(21):1391–1394. doi: 10.1016/s0960-9822(00)00784-3. [DOI] [PubMed] [Google Scholar]
  35. Sarov-Blat L., So W. V., Liu L., Rosbash M. The Drosophila takeout gene is a novel molecular link between circadian rhythms and feeding behavior. Cell. 2000 Jun 9;101(6):647–656. doi: 10.1016/s0092-8674(00)80876-4. [DOI] [PubMed] [Google Scholar]
  36. Savage C., Hamelin M., Culotti J. G., Coulson A., Albertson D. G., Chalfie M. mec-7 is a beta-tubulin gene required for the production of 15-protofilament microtubules in Caenorhabditis elegans. Genes Dev. 1989 Jun;3(6):870–881. doi: 10.1101/gad.3.6.870. [DOI] [PubMed] [Google Scholar]
  37. Sawin-McCormack E. P., Sokolowski M. B., Campos A. R. Characterization and genetic analysis of Drosophila melanogaster photobehavior during larval development. J Neurogenet. 1995 Nov;10(2):119–135. doi: 10.3109/01677069509083459. [DOI] [PubMed] [Google Scholar]
  38. Schmucker D., Taubert H., Jäckle H. Formation of the Drosophila larval photoreceptor organ and its neuronal differentiation require continuous Krüppel gene activity. Neuron. 1992 Dec;9(6):1025–1039. doi: 10.1016/0896-6273(92)90063-j. [DOI] [PubMed] [Google Scholar]
  39. Serrano N., Brock H. W., Maschat F. beta3-tubulin is directly repressed by the engrailed protein in Drosophila. Development. 1997 Jul;124(13):2527–2536. doi: 10.1242/dev.124.13.2527. [DOI] [PubMed] [Google Scholar]
  40. Sullivan W., Theurkauf W. E. The cytoskeleton and morphogenesis of the early Drosophila embryo. Curr Opin Cell Biol. 1995 Feb;7(1):18–22. doi: 10.1016/0955-0674(95)80040-9. [DOI] [PubMed] [Google Scholar]
  41. Tavernarakis N., Driscoll M. Molecular modeling of mechanotransduction in the nematode Caenorhabditis elegans. Annu Rev Physiol. 1997;59:659–689. doi: 10.1146/annurev.physiol.59.1.659. [DOI] [PubMed] [Google Scholar]
  42. Theurkauf W. E., Hazelrigg T. I. In vivo analyses of cytoplasmic transport and cytoskeletal organization during Drosophila oogenesis: characterization of a multi-step anterior localization pathway. Development. 1998 Sep;125(18):3655–3666. doi: 10.1242/dev.125.18.3655. [DOI] [PubMed] [Google Scholar]
  43. Tully T. Discovery of genes involved with learning and memory: an experimental synthesis of Hirschian and Benzerian perspectives. Proc Natl Acad Sci U S A. 1996 Nov 26;93(24):13460–13467. doi: 10.1073/pnas.93.24.13460. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Varnam C. J., Strauss R., Belle J. S., Sokolowski M. B. Larval behavior of Drosophila central complex mutants: interactions between no bridge, foraging, and Chaser. J Neurogenet. 1996 Dec;11(1-2):99–115. doi: 10.3109/01677069609107065. [DOI] [PubMed] [Google Scholar]
  45. Wang J. W., Sylwester A. W., Reed D., Wu D. A., Soll D. R., Wu C. F. Morphometric description of the wandering behavior in Drosophila larvae: aberrant locomotion in Na+ and K+ channel mutants revealed by computer-assisted motion analysis. J Neurogenet. 1997 Nov;11(3-4):231–254. doi: 10.3109/01677069709115098. [DOI] [PubMed] [Google Scholar]
  46. Yang P., Shaver S. A., Hilliker A. J., Sokolowski M. B. Abnormal turning behavior in Drosophila larvae. Identification and molecular analysis of scribbler (sbb). Genetics. 2000 Jul;155(3):1161–1174. doi: 10.1093/genetics/155.3.1161. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Young P. E., Pesacreta T. C., Kiehart D. P. Dynamic changes in the distribution of cytoplasmic myosin during Drosophila embryogenesis. Development. 1991 Jan;111(1):1–14. doi: 10.1242/dev.111.1.1. [DOI] [PubMed] [Google Scholar]
  48. Zipursky S. L., Venkatesh T. R., Teplow D. B., Benzer S. Neuronal development in the Drosophila retina: monoclonal antibodies as molecular probes. Cell. 1984 Jan;36(1):15–26. doi: 10.1016/0092-8674(84)90069-2. [DOI] [PubMed] [Google Scholar]
  49. de Cuevas M., Spradling A. C. Morphogenesis of the Drosophila fusome and its implications for oocyte specification. Development. 1998 Aug;125(15):2781–2789. doi: 10.1242/dev.125.15.2781. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES