Skip to main content
NCBI home page
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1986 May;6(5):1464–1470. doi: 10.1128/mcb.6.5.1464

The memory gene dunce+ encodes a remarkable set of RNAs with internal heterogeneity.

R L Davis, N Davidson
PMCID: PMC367671  PMID: 2431279

Abstract

We have previously isolated the region of the Drosophila melanogaster X chromosome which contains the dunce+ gene and mapped the dunce2 mutation by recombination to a 10- to 12-kilobase (kb) interval (R. L. Davis and N. Davidson, Mol. Cell. Biol. 4:358-367, 1984). Here, we examine the expression of the dunce+ chromosomal region and identify the dunce+ gene within that region. A region of ca. 25 kb which contains the 10- to 12-kb interval to which dunce2 was mapped codes for polyadenylated RNAs of 9.6, 7.4, 7.2, 7.0, 5.4, and 4.5 kb in adult flies. These transcripts are encoded by the same DNA strand and share sequences of some exons, indicating that the transcripts arise from the same gene. Some genome probes internal to the ca. 25-kb coding region show transcript-specific hybridization, demonstrating alternate usage of exonic sequence information in the formation of the mature transcripts. The basis for this internal heterogeneity in RNAs is most likely alternative splicing. Two dunce mutants examined show aberrant RNA expression from this coding region, confirming that this region is the dunce gene. The developmental expression of these transcripts has been examined. The 5.4-kb RNA is present at all developmental stages. The 9.6-, 7.4-, 7.2-, and 7.0-kb RNAs are not expressed at detectable levels in embryos, but are detected in late embryogenesis and in later developmental stages. The 4.5-kb species is found in early embryos and adults, but not in intermediate stages. We discuss the remarkable transcript heterogeneity and expression pattern with respect to the important function this gene performs in neurobiological and other physiological processes.

Full text

PDF
1464

Images in this article

1465Image
on p.1465
1466Image
on p.1466
1467Image
on p.1467
1467Image
on p.1467
1467Image
on p.1467
1467Image
on p.1467
1468Image
on p.1468

Selected References

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

  1. Aceves-Piña E. O., Booker R., Duerr J. S., Livingstone M. S., Quinn W. G., Smith R. F., Sziber P. P., Tempel B. L., Tully T. P. Learning and memory in Drosophila, studied with mutants. Cold Spring Harb Symp Quant Biol. 1983;48(Pt 2):831–840. doi: 10.1101/sqb.1983.048.01.086. [DOI] [PubMed] [Google Scholar]
  2. Booker R., Quinn W. G. Conditioning of leg position in normal and mutant Drosophila. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3940–3944. doi: 10.1073/pnas.78.6.3940. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Breitbart R. E., Nguyen H. T., Medford R. M., Destree A. T., Mahdavi V., Nadal-Ginard B. Intricate combinatorial patterns of exon splicing generate multiple regulated troponin T isoforms from a single gene. Cell. 1985 May;41(1):67–82. doi: 10.1016/0092-8674(85)90062-5. [DOI] [PubMed] [Google Scholar]
  4. Byers D., Davis R. L., Kiger J. A., Jr Defect in cyclic AMP phosphodiesterase due to the dunce mutation of learning in Drosophila melanogaster. Nature. 1981 Jan 1;289(5793):79–81. doi: 10.1038/289079a0. [DOI] [PubMed] [Google Scholar]
  5. Darnell J. E., Jr Transcription units for mRNA production in eukaryotic cells and their DNA viruses. Prog Nucleic Acid Res Mol Biol. 1979;22:327–353. doi: 10.1016/s0079-6603(08)60803-x. [DOI] [PubMed] [Google Scholar]
  6. Davis R. L., Davidson N. Isolation of the Drosophila melanogaster dunce chromosomal region and recombinational mapping of dunce sequences with restriction site polymorphisms as genetic markers. Mol Cell Biol. 1984 Feb;4(2):358–367. doi: 10.1128/mcb.4.2.358. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Davis R. L., Kauvar L. M. Drosophila cyclic nucleotide phosphodiesterases. Adv Cyclic Nucleotide Protein Phosphorylation Res. 1984;16:393–402. [PubMed] [Google Scholar]
  8. Davis R. L., Kiger J. A., Jr Dunce mutants of Drosophila melanogaster: mutants defective in the cyclic AMP phosphodiesterase enzyme system. J Cell Biol. 1981 Jul;90(1):101–107. doi: 10.1083/jcb.90.1.101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dawid I. B. DNA-DNA hybridization on membrane filters: a convenient method using formamide. Biochim Biophys Acta. 1977 Jul 15;477(2):191–194. doi: 10.1016/0005-2787(77)90235-0. [DOI] [PubMed] [Google Scholar]
  10. Dudai Y. Mutations affect storage and use of memory differentially in Drosophila. Proc Natl Acad Sci U S A. 1983 Sep;80(17):5445–5448. doi: 10.1073/pnas.80.17.5445. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Duerr J. S., Quinn W. G. Three Drosophila mutations that block associative learning also affect habituation and sensitization. Proc Natl Acad Sci U S A. 1982 Jun;79(11):3646–3650. doi: 10.1073/pnas.79.11.3646. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Falkenthal S., Parker V. P., Davidson N. Developmental variations in the splicing pattern of transcripts from the Drosophila gene encoding myosin alkali light chain result in different carboxyl-terminal amino acid sequences. Proc Natl Acad Sci U S A. 1985 Jan;82(2):449–453. doi: 10.1073/pnas.82.2.449. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Fyrberg E. A., Kindle K. L., Davidson N., Kindle K. L. The actin genes of Drosophila: a dispersed multigene family. Cell. 1980 Feb;19(2):365–378. doi: 10.1016/0092-8674(80)90511-5. [DOI] [PubMed] [Google Scholar]
  14. Fyrberg E. A., Mahaffey J. W., Bond B. J., Davidson N. Transcripts of the six Drosophila actin genes accumulate in a stage- and tissue-specific manner. Cell. 1983 May;33(1):115–123. doi: 10.1016/0092-8674(83)90340-9. [DOI] [PubMed] [Google Scholar]
  15. Gailey D. A., Jackson F. R., Siegel R. W. Male courtship in Drosophila: the conditioned response to immature males and its genetic control. Genetics. 1982 Dec;102(4):771–782. doi: 10.1093/genetics/102.4.771. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hu N., Messing J. The making of strand-specific M13 probes. Gene. 1982 Mar;17(3):271–277. doi: 10.1016/0378-1119(82)90143-3. [DOI] [PubMed] [Google Scholar]
  17. Kandel E. R., Schwartz J. H. Molecular biology of learning: modulation of transmitter release. Science. 1982 Oct 29;218(4571):433–443. doi: 10.1126/science.6289442. [DOI] [PubMed] [Google Scholar]
  18. Kauvar L. M. Defective cyclic adenosine 3':5'-monophosphate phosphodiesterase in the Drosophila memory mutant dunce. J Neurosci. 1982 Oct;2(10):1347–1358. doi: 10.1523/JNEUROSCI.02-10-01347.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kiger J. A., Jr, Golanty E. A cytogenetic analysis of cyclic nucleotide phosphodiesterase activities in Drosophila. Genetics. 1977 Apr;85(4):609–622. doi: 10.1093/genetics/85.4.609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Livingstone M. S., Sziber P. P., Quinn W. G. Loss of calcium/calmodulin responsiveness in adenylate cyclase of rutabaga, a Drosophila learning mutant. Cell. 1984 May;37(1):205–215. doi: 10.1016/0092-8674(84)90316-7. [DOI] [PubMed] [Google Scholar]
  21. Nawa H., Kotani H., Nakanishi S. Tissue-specific generation of two preprotachykinin mRNAs from one gene by alternative RNA splicing. Nature. 1984 Dec 20;312(5996):729–734. doi: 10.1038/312729a0. [DOI] [PubMed] [Google Scholar]
  22. Rosenfeld M. G., Amara S. G., Evans R. M. Alternative RNA processing: determining neuronal phenotype. Science. 1984 Sep 21;225(4668):1315–1320. doi: 10.1126/science.6089345. [DOI] [PubMed] [Google Scholar]
  23. Rozek C. E., Davidson N. Drosophila has one myosin heavy-chain gene with three developmentally regulated transcripts. Cell. 1983 Jan;32(1):23–34. doi: 10.1016/0092-8674(83)90493-2. [DOI] [PubMed] [Google Scholar]
  24. Salz H. K., Davis R. L., Kiger J. A. Genetic Analysis of Chromomere 3d4 in DROSOPHILA MELANOGASTER: The DUNCE and SPERM-AMOTILE Genes. Genetics. 1982 Apr;100(4):587–596. doi: 10.1093/genetics/100.4.587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Salz H. K., Kiger J. A., Jr Genetic analysis of chromomere 3D4 in Drosophila melanogaster. II. Regulatory sites for the dunce gene. Genetics. 1984 Oct;108(2):377–392. doi: 10.1093/genetics/108.2.377. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Shotwell S. L. Cyclic adenosine 3':5'-monophosphate phosphodiesterase and its role in learning in Drosophila. J Neurosci. 1983 Apr;3(4):739–747. doi: 10.1523/JNEUROSCI.03-04-00739.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Stark G. R., Williams J. G. Quantitative analysis of specific labelled RNA'S using DNA covalently linked to diazobenzyloxymethyl-paper. Nucleic Acids Res. 1979 Jan;6(1):195–203. doi: 10.1093/nar/6.1.195. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis

RESOURCES