Skip to main content
PMC home page
Genetics logoLink to Genetics
. 2003 Nov;165(3):1341–1354. doi: 10.1093/genetics/165.3.1341

Genetic and phenotypic analysis of alleles of the Drosophila chromosomal JIL-1 kinase reveals a functional requirement at multiple developmental stages.

Weiguo Zhang 1, Ye Jin 1, Yun Ji 1, Jack Girton 1, Jørgen Johansen 1, Kristen M Johansen 1
PMCID: PMC1462823  PMID: 14668387

Abstract

In this study we provide a cytological and genetic characterization of the JIL-1 locus in Drosophila. JIL-1 is an essential chromosomal tandem kinase and in JIL-1 null animals chromatin structure is severely perturbed. Using a range of JIL-1 hypomorphic mutations, we show that they form an allelic series. JIL-1 has a strong maternal effect and JIL-1 activity is required at all stages of development, including embryonic, larval, and pupal stages. Furthermore, we identified a new allele of JIL-1, JIL-1(h9), that encodes a truncated protein missing COOH-terminal sequences. Remarkably, the truncated JIL-1 protein can partially restore viability without rescuing the defects in polytene chromosome organization. This suggests that sequences within this region of JIL-1 play an important role in establishing and/or maintaining normal chromatin structure. By analyzing the effects of JIL-1 mutations we provide evidence that JIL-1 function is necessary for the normal progression of several developmental processes at different developmental stages such as oogenesis and segment specification. We propose that JIL-1 may exert such effects by a general regulation of chromatin structure affecting gene expression.

Full Text

The Full Text of this article is available as a PDF (287.0 KB).

Selected References

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

  1. Beisel Christian, Imhof Axel, Greene Jaime, Kremmer Elisabeth, Sauer Frank. Histone methylation by the Drosophila epigenetic transcriptional regulator Ash1. Nature. 2002 Oct 9;419(6909):857–862. doi: 10.1038/nature01126. [DOI] [PubMed] [Google Scholar]
  2. Bellotto Manolo, Bopp Daniel, Senti Kirsten A., Burke Richard, Deak Peter, Maroy Peter, Dickson Barry, Basler Konrad, Hafen Ernst. Maternal-effect loci involved in Drosophila oogenesis and embryogenesis: P element-induced mutations on the third chromosome. Int J Dev Biol. 2002 Jan;46(1):149–157. [PubMed] [Google Scholar]
  3. Campbell S. D., Hilliker A. J., Phillips J. P. Cytogenetic analysis of the cSOD microregion in Drosophila melanogaster. Genetics. 1986 Feb;112(2):205–215. doi: 10.1093/genetics/112.2.205. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cavarec L., Jensen S., Casella J. F., Cristescu S. A., Heidmann T. Molecular cloning and characterization of a transcription factor for the copia retrotransposon with homology to the BTB-containing lola neurogenic factor. Mol Cell Biol. 1997 Jan;17(1):482–494. doi: 10.1128/mcb.17.1.482. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Crosby M. A., Meyerowitz E. M. Lethal mutations flanking the 68C glue gene cluster on chromosome 3 of Drosophila melanogaster. Genetics. 1986 Apr;112(4):785–802. doi: 10.1093/genetics/112.4.785. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Crowner Daniel, Madden Knut, Goeke Scott, Giniger Edward. Lola regulates midline crossing of CNS axons in Drosophila. Development. 2002 Mar;129(6):1317–1325. doi: 10.1242/dev.129.6.1317. [DOI] [PubMed] [Google Scholar]
  7. Czermin Birgit, Melfi Raffaella, McCabe Donna, Seitz Volker, Imhof Axel, Pirrotta Vincenzo. Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell. 2002 Oct 18;111(2):185–196. doi: 10.1016/s0092-8674(02)00975-3. [DOI] [PubMed] [Google Scholar]
  8. Dalby K. N., Morrice N., Caudwell F. B., Avruch J., Cohen P. Identification of regulatory phosphorylation sites in mitogen-activated protein kinase (MAPK)-activated protein kinase-1a/p90rsk that are inducible by MAPK. J Biol Chem. 1998 Jan 16;273(3):1496–1505. doi: 10.1074/jbc.273.3.1496. [DOI] [PubMed] [Google Scholar]
  9. Dingwall A. K., Beek S. J., McCallum C. M., Tamkun J. W., Kalpana G. V., Goff S. P., Scott M. P. The Drosophila snr1 and brm proteins are related to yeast SWI/SNF proteins and are components of a large protein complex. Mol Biol Cell. 1995 Jul;6(7):777–791. doi: 10.1091/mbc.6.7.777. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dobie K. W., Kennedy C. D., Velasco V. M., McGrath T. L., Weko J., Patterson R. W., Karpen G. H. Identification of chromosome inheritance modifiers in Drosophila melanogaster. Genetics. 2001 Apr;157(4):1623–1637. doi: 10.1093/genetics/157.4.1623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Frödin M., Gammeltoft S. Role and regulation of 90 kDa ribosomal S6 kinase (RSK) in signal transduction. Mol Cell Endocrinol. 1999 May 25;151(1-2):65–77. doi: 10.1016/s0303-7207(99)00061-1. [DOI] [PubMed] [Google Scholar]
  12. Giniger E., Tietje K., Jan L. Y., Jan Y. N. lola encodes a putative transcription factor required for axon growth and guidance in Drosophila. Development. 1994 Jun;120(6):1385–1398. doi: 10.1242/dev.120.6.1385. [DOI] [PubMed] [Google Scholar]
  13. Girton J. R., Jeon S. H. Novel embryonic and adult homeotic phenotypes are produced by pleiohomeotic mutations in Drosophila. Dev Biol. 1994 Feb;161(2):393–407. doi: 10.1006/dbio.1994.1040. [DOI] [PubMed] [Google Scholar]
  14. Ishii Kojiro, Laemmli Ulrich K. Structural and dynamic functions establish chromatin domains. Mol Cell. 2003 Jan;11(1):237–248. doi: 10.1016/s1097-2765(03)00010-8. [DOI] [PubMed] [Google Scholar]
  15. Jin Y., Wang Y., Walker D. L., Dong H., Conley C., Johansen J., Johansen K. M. JIL-1: a novel chromosomal tandem kinase implicated in transcriptional regulation in Drosophila. Mol Cell. 1999 Jul;4(1):129–135. doi: 10.1016/s1097-2765(00)80195-1. [DOI] [PubMed] [Google Scholar]
  16. Johansen K. M., Johansen J., Jin Y., Walker D. L., Wang D., Wang Y. Chromatin structure and nuclear remodeling. Crit Rev Eukaryot Gene Expr. 1999;9(3-4):267–277. doi: 10.1615/critreveukargeneexpr.v9.i3-4.110. [DOI] [PubMed] [Google Scholar]
  17. Makunin I. V., Volkova E. I., Belyaeva E. S., Nabirochkina E. N., Pirrotta V., Zhimulev I. F. The Drosophila suppressor of underreplication protein binds to late-replicating regions of polytene chromosomes. Genetics. 2002 Mar;160(3):1023–1034. doi: 10.1093/genetics/160.3.1023. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Meller Victoria H., Kuroda Mitzi I. Sex and the single chromosome. Adv Genet. 2002;46:1–24. doi: 10.1016/s0065-2660(02)46002-6. [DOI] [PubMed] [Google Scholar]
  19. Müller J., Bienz M. Sharp anterior boundary of homeotic gene expression conferred by the fushi tarazu protein. EMBO J. 1992 Oct;11(10):3653–3661. doi: 10.1002/j.1460-2075.1992.tb05450.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Müller Jürg, Hart Craig M., Francis Nicole J., Vargas Marcus L., Sengupta Aditya, Wild Brigitte, Miller Ellen L., O'Connor Michael B., Kingston Robert E., Simon Jeffrey A. Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell. 2002 Oct 18;111(2):197–208. doi: 10.1016/s0092-8674(02)00976-5. [DOI] [PubMed] [Google Scholar]
  21. Orlando V., Paro R. Chromatin multiprotein complexes involved in the maintenance of transcription patterns. Curr Opin Genet Dev. 1995 Apr;5(2):174–179. doi: 10.1016/0959-437x(95)80005-0. [DOI] [PubMed] [Google Scholar]
  22. Papoulas O., Beek S. J., Moseley S. L., McCallum C. M., Sarte M., Shearn A., Tamkun J. W. The Drosophila trithorax group proteins BRM, ASH1 and ASH2 are subunits of distinct protein complexes. Development. 1998 Oct;125(20):3955–3966. doi: 10.1242/dev.125.20.3955. [DOI] [PubMed] [Google Scholar]
  23. Paro R. Imprinting a determined state into the chromatin of Drosophila. Trends Genet. 1990 Dec;6(12):416–421. doi: 10.1016/0168-9525(90)90303-n. [DOI] [PubMed] [Google Scholar]
  24. Pirrotta V., Rastelli L. White gene expression, repressive chromatin domains and homeotic gene regulation in Drosophila. Bioessays. 1994 Aug;16(8):549–556. doi: 10.1002/bies.950160808. [DOI] [PubMed] [Google Scholar]
  25. Preston C. R., Engels W. R. P-element-induced male recombination and gene conversion in Drosophila. Genetics. 1996 Dec;144(4):1611–1622. doi: 10.1093/genetics/144.4.1611. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Qian S., Capovilla M., Pirrotta V. The bx region enhancer, a distant cis-control element of the Drosophila Ubx gene and its regulation by hunchback and other segmentation genes. EMBO J. 1991 Jun;10(6):1415–1425. doi: 10.1002/j.1460-2075.1991.tb07662.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Rudenko Andrey, Bennett Daimark, Alphey Luke. Trithorax interacts with type 1 serine/threonine protein phosphatase in Drosophila. EMBO Rep. 2003 Jan;4(1):59–63. doi: 10.1038/sj.embor.embor712. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Rørth P., Szabo K., Bailey A., Laverty T., Rehm J., Rubin G. M., Weigmann K., Milán M., Benes V., Ansorge W. Systematic gain-of-function genetics in Drosophila. Development. 1998 Mar;125(6):1049–1057. doi: 10.1242/dev.125.6.1049. [DOI] [PubMed] [Google Scholar]
  29. Shearn A., Rice T., Garen A., Gehring W. Imaginal disc abnormalities in lethal mutants of Drosophila. Proc Natl Acad Sci U S A. 1971 Oct;68(10):2594–2598. doi: 10.1073/pnas.68.10.2594. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Shearn A. The ash-1, ash-2 and trithorax genes of Drosophila melanogaster are functionally related. Genetics. 1989 Mar;121(3):517–525. doi: 10.1093/genetics/121.3.517. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Shimell M. J., Simon J., Bender W., O'Connor M. B. Enhancer point mutation results in a homeotic transformation in Drosophila. Science. 1994 May 13;264(5161):968–971. doi: 10.1126/science.7909957. [DOI] [PubMed] [Google Scholar]
  32. Simon J. Locking in stable states of gene expression: transcriptional control during Drosophila development. Curr Opin Cell Biol. 1995 Jun;7(3):376–385. doi: 10.1016/0955-0674(95)80093-x. [DOI] [PubMed] [Google Scholar]
  33. Simon J., Peifer M., Bender W., O'Connor M. Regulatory elements of the bithorax complex that control expression along the anterior-posterior axis. EMBO J. 1990 Dec;9(12):3945–3956. doi: 10.1002/j.1460-2075.1990.tb07615.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Smith E. R., Pannuti A., Gu W., Steurnagel A., Cook R. G., Allis C. D., Lucchesi J. C. The drosophila MSL complex acetylates histone H4 at lysine 16, a chromatin modification linked to dosage compensation. Mol Cell Biol. 2000 Jan;20(1):312–318. doi: 10.1128/mcb.20.1.312-318.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Spradling A. C., de Cuevas M., Drummond-Barbosa D., Keyes L., Lilly M., Pepling M., Xie T. The Drosophila germarium: stem cells, germ line cysts, and oocytes. Cold Spring Harb Symp Quant Biol. 1997;62:25–34. [PubMed] [Google Scholar]
  36. Staveley B. E., Hilliker A. J., Phillips J. P. Genetic organization of the cSOD microregion of Drosophila melanogaster. Genome. 1991 Apr;34(2):279–282. doi: 10.1139/g91-044. [DOI] [PubMed] [Google Scholar]
  37. Tamkun J. W., Deuring R., Scott M. P., Kissinger M., Pattatucci A. M., Kaufman T. C., Kennison J. A. brahma: a regulator of Drosophila homeotic genes structurally related to the yeast transcriptional activator SNF2/SWI2. Cell. 1992 Feb 7;68(3):561–572. doi: 10.1016/0092-8674(92)90191-e. [DOI] [PubMed] [Google Scholar]
  38. Zhang Weiguo, Wang Yanming, Long Jin, Girton Jack, Johansen Jørgen, Johansen Kristen M. A developmentally regulated splice variant from the complex lola locus encoding multiple different zinc finger domain proteins interacts with the chromosomal kinase JIL-1. J Biol Chem. 2003 Jan 21;278(13):11696–11704. doi: 10.1074/jbc.M213269200. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES