Drosophila mojoless, a retroposed GSK-3, has functionally diverged to acquire an essential role in male fertility

Molecular Biology and Evolution

Volumn 24, Issue 3, 2007, Pages 732-742

  Kalamegham, Rasika ^a,b   Sturgill, David ^a   Siegfried, Esther ^b,c   Oliver, Brian ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

Adaptive evolution; Gene duplication; Germ cell; GSK 3; Male germ line; Male sterile; Retroposition

Indexed keywords

ARTICLE; DNA REPAIR; DROSOPHILA MELANOGASTER; GENE; GENE EXPRESSION; GENE FUNCTION; GENETIC SELECTION; GENETIC STABILITY; GENETIC VARIABILITY; GENUS; GERM LINE; GLYCOGEN SYNTHASE KINASE 3 GENE; MALE FERTILITY; MOJOLESS GENE; NONHUMAN; RETROPOSON; SOMATIC CELL; TRANSGENE;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CLUSTER ANALYSIS; DNA PRIMERS; DROSOPHILA; DROSOPHILA PROTEINS; FERTILITY; GERM CELLS; GLYCOGEN SYNTHASE KINASE 3; IMMUNOBLOTTING; LIKELIHOOD FUNCTIONS; MALE; MICROSCOPY, CONFOCAL; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; RETROELEMENTS; RNA INTERFERENCE; SELECTION (GENETICS); SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; TESTIS;

DROSOPHILA MELANOGASTER;

EID: 33847615104     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msl201     Document Type: Article

References (64)

1. Adams MD, Celniker SE, Holt RA, et al. (195 co-authors). 2000. The genome sequence of Drosophila melanogaster. Science. 287:2185-2195.
2. Andrews J, Bouffard GG, Cheadle C, Lu J, Becker KG, Oliver B. 2000. Gene discovery using computational and microarray analysis of transcription in the Drosophila melanogaster testis. Genome Res. 10:2030-2043.
3. Asaoka M, Sano H, Obara Y, Kobayashi S. 1998. Maternal Nanos regulates zygotic gene expression in germline progenitors of Drosophila melanogaster. Mech Dev. 78:153-158.
4. Betran E, Emerson JJ, Kaessmann H, Long M. 2004. Sex chromosomes and male functions: where do new genes go? Cell Cycle. 3:873-875.
5. Betran E, Long M. 2002. Expansion of genome coding regions by acquisition of new genes. Genetica. 115:65-80.
6. Betran E, Thornton K, Long M. 2002. Retroposed new genes out of the X in Drosophila. Genome Res. 12:1854-1859.
7. Bourouis M, Moore P, Ruel L, Grau Y, Heitzler P, Simpson P. 1990. An early embryonic product of the gene shaggy encodes a serine/threonine protein kinase related to the CDC28/cdc21 subfamily. EMBO J. 9:2877-2884.
8. Brand AH, Perrimon N. 1993. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development. 118:401-415.
9. Brent R, Kingston RE, Seidman JG, Struhl K, Ansubel FM, Chanda VB, Moore DD. 1987. Current protocols in molecular biology. Hoboken (NJ): Wiley and Sons.
10. Brosius J. 1991. Retroposons - seeds of evolution. Science. 251:753.
11. Burnett C, Howard K. 2003. Fly and mammalian lipid phosphate phosphatase isoforms differ in activity both in vitro and in vivo. EMBO Rep. 4:793-799.
12. Celniker SE, Wheeler DA, Kronmiller B, et al. (32 co-authors). 2002. Finishing a whole-genome shotgun: release 3 of the Drosophila melanogaster euchromatic genome sequence. Genome Biol. 3:RESEARCH0079.
13. Clamp M, Cuff J, Searle SM, Barton GJ. 2004. The Jalview Java alignment editor. Bioinformatics. 20:426-427.
14. Cohen P, Frame S. 2001. The renaissance of GSK3. Nat Rev Mol Cell Biol. 2:769-776.
15. Dajani R, Fraser E, Roe SM, Young N, Good V, Dale TC, Pearl LH. 2001. Crystal structure of glycogen synthase kinase 3 beta: structural basis for phosphate-primed substrate specificity and autoinhibition. Cell. 105:721-732.
16. Eldar-Finkelman H. 2002. Glycogen synthase kinase 3: an emerging therapeutic target. Trends Mol Med. 8:126-132.
17. Emerson JJ, Kaessmann H, Betran E, Long M. 2004. Extensive gene traffic on the mammalian X chromosome. Science. 303:537-540.
18. Fabrizio JJ, Boyle M, DiNardo S. 2003. A somatic role for eyes absent (eya) and sine oculis (so) in Drosophila spermatocyte development. Dev Biol. 258:117-128.
19. FlyBase. 2003. The FlyBase database of the Drosophila genome projects and community literature. Nucleic Acids Res. 31:172-175.
20. Frame S, Cohen P. 2001. GSK3 takes centre stage more than 20 years after its discovery. Biochem J. 359:1-16.
21. Fuller MT. 1993. Spermatogenesis. In: Bate M, Martinez-Arias A, editors. The development of Drosophila. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press. p. 71-148.
22. Hisano M, Yamada S, Tanaka H, Nishimune Y, Nozaki M. 2003. Genomic structure and promoter activity of the testis haploid germ cell-specific intronless genes, Tact1 and Tact2. Mol Reprod Dev. 65:148-156.
23. Hughes AL. 1994. The evolution of functionally novel proteins after gene duplication. Proc Biol Sci. 256:119-124.
24. Hurst LD. 2002. The Ka/Ks ratio: diagnosing the form of sequence evolution. Trends Genet. 18:486.
25. Jope RS, Johnson GV. 2004. The glamour and gloom of glycogen synthase kinase-3. Trends Biochem Sci. 29:95-102.
26. Kennerdell JR, Carthew RW. 2000. Heritable gene silencing in Drosophila using double-stranded RNA. Nat Biotechnol. 18:896-898.
27. Khil PP, Oliver B, Camerini-Otero RD. 2005. X for intersection: retrotransposition both on and off the X chromosome is more frequent. Trends Genet. 21:3-7.
28. Kiger AA, Jones DL, Schulz C, Rogers MB, Fuller MT. 2001. Stem cell self-renewal specified by JAK-STAT activation in response to a support cell cue. Science. 294:2542-2545.
29. Kumar S, Tamura K, Nei M. 2004. MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform. 5:150-163.
30. Le Bras S, Van Doren M. 2006. Development of the male germline stem cell niche in Drosophila. Dev Biol. 294(1):92-103.
31. Li WH, Yang J, Gu X. 2005. Expression divergence between duplicate genes. Trends Genet. 21:602-607.
32. Long M, Betran E, Thornton K, Wang W. 2003. The origin of new genes: glimpses from the young and old. Nat Rev Genet 4:865-875.
33. Long M, Deutsch M, Wang W, Betran E, Brunet FG, Zhang J. 2003. Origin of new genes: evidence from experimental and computational analyses. Genetica. 118:171-182.
34. Luo C, Lu X, Stubbs L, Kim J. 2006. Rapid evolution of a recently retroposed transcription factor YY2 in mammalian genomes. Genomics. 87:348-355.
35. Lynch M, Conery JS. 2000. The evolutionary fate and consequences of duplicate genes. Science. 290:1151-1155.
36. Nei M, Gojobori T. 1986. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol. 3:418-426.
37. Nei M, Kumar S. 2000. Molecular evolution and phylogenetics. Oxford: Oxford University Press.
38. Ohta T. 2002. Near-neutrality in evolution of genes and gene regulation. Proc Natl Acad Sci USA. 99:16134-16137.
39. Parisi M, Nuttall R, Edwards P, et al. (12 co-authors). 2004. A survey of ovary-, testis-, and soma-biased gene expression in Drosophila melanogaster adults. Genome Biol. 5:R40.
40. Parisi M, Nuttall R, Naiman D, Bouffard G, Malley J, Andrews J, Eastman S, Oliver B. 2003. Paucity of genes on the Drosophila X chromosome showing male-biased expression. Science. 299:697-700.
41. Robertson HM, Preston CR, Phillis RW, Johnson-Schlitz DM, Benz WK, Engels WR. 1988. A stable genomic source of P element transposase in Drosophila melanogaster. Genetics. 118:461-470.
42. Rohozinski J, Bishop CE. 2004. The mouse juvenile spermatogonial depletion (jsd) phenotype is due to a mutation in the X-derived retrogene, mUtp14b. Proc Natl Acad Sci USA. 101:11695-11700.
43. Rongo C, Broihier HT, Moore L, Van Doren M, Forbes A, Lehmann R. 1997. Germ plasm assembly and germ cell migration in Drosophila. Cold Spring Harbor Symp Quant Biol. 62:1-11.
44. Russo CA, Takezaki N, Nei M. 1995. Molecular phylogeny and divergence times of drosophilid species. Mol Biol Evol. 12:391-404.
45. Schulz C, Kiger AA, Tazuke SI, Yamashita YM, Pantalena-Filho LC, Jones DL, Wood CG, Fuller MT. 2004. A misexpression screen reveals effects of bag-of-marbles and TGF beta class signaling on the Drosophila male germ-line stem cell lineage. Genetics. 167:707-723.
46. Siegfried E, Chou TB, Perrimon N. 1992. Wingless signaling acts through zeste-white 3, the Drosophila homolog of glycogen synthase kinase-3, to regulate engrailed and establish cell fate. Cell. 71:1167-1179.
47. Siegfried E, Perkins LA, Capaci TM, Perrimon N. 1990. Putative protein kinase product of the Drosophila segment-polarity gene zeste-white3. Nature. 345:825-829.
48. Siegfried E, Wilder EL, Perrimon N. 1994. Components of wingless signalling in Drosophila. Nature. 367:76-80.
49. Stanewsky R. 2002. Clock mechanisms in Drosophila. Cell Tissue Res. 309:11-26.
50. Stapleton M, Carlson J, Brokstein P, et al. (13 co-authors). 2002. A Drosophila full-length cDNA resource. Genome Biol. 3:RESEARCH0080.
51. Steitz MC. 2000. An investigation of Zeste white-3 inactivation by wingless signalling. University Park (PA): Department of Biochemistry, Microbiology and Molecular Biology. The Pennsylvania State University. p. 173.
52. Steitz MC, Wickenheisser JK, Siegfried E. 1998. Overexpression of zeste white 3 blocks wingless signaling in the Drosophila embryonic midgut. Dev Biol. 197:218-233.
53. Tamura K, Subramanian S, Kumar S. 2004. Temporal patterns of fruit fly (Drosophila) evolution revealed by mutation clocks. Mol Biol Evol. 21:36-44.
54. ter Haar E, Coll JT, Austen DA, Hsiao HM, Swenson L, Jain J. 2001. Structure of GSK3beta reveals a primed phosphorylation mechanism. Nat Struct Biol. 8:593-596.
55. Tulina N, Matunis E. 2001. Control of stem cell self-renewal in Drosophila spermatogenesis by JAK-STAT signaling. Science. 294:2546-2549.
56. Vinckenbosch N, Dupanloup I, Kaessmann H. 2006. Evolutionary fate of retroposed gene copies in the human genome. Proc Natl Acad Sci USA. 103:3220-3225.
57. Wang W, Yu H, Long M. 2004. Duplication-degeneration as a mechanism of gene fission and the origin of new genes in Drosophila species. Nat Genet. 36:523-527.
58. Wernersson R, Pedersen AG. 2003. RevTrans: multiple alignment of coding DNA from aligned amino acid sequences. Nucleic Acids Res. 31:3537-3539.
59. Woodgett JR. 1990. Molecular cloning and expression of glycogen synthase kinase-3/factor A. EMBO J. 9:2431-2438.
60. Wu CI, Xu EY. 2003. Sexual antagonism and X inactivation - the SAXI hypothesis. Trends Genet. 19:243-247.
61. Xing Y, Lee C. 2006. Can RNA selection pressure distort the measurement of Ka/Ks? Gene. 370:1-5.
62. Yang Z, Nielsen R. 2000. Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol Biol Evol. 17:32-43.
63. Zhang J, Dean AM, Brunet F, Long M. 2004. Evolving protein functional diversity in new genes of Drosophila. Proc Natl Acad Sci USA. 101:16246-16250.
64. Zhang J, Rosenberg HF, Nei M. 1998. Positive Darwinian selection after gene duplication in primate ribonuclease genes. Proc Natl Acad Sci USA. 95:3708-3713.