Toward a Molecular Genetic Analysis of Spermatogenesis in Drosophila melanogaster: Characterization of Male-Sterile Mutants Generated by Single P Element Mutagenesis

INVESTIGATIONS

Toward a Molecular Genetic Analysis of Spermatogenesis in Drosophila melanogaster: Characterization of Male-Sterile Mutants Generated by Single P Element Mutagenesis

D. H. Castrillon, P. Gonczy, S. Alexander, R. Rawson, C. G. Eberhart, S. Viswanathan, S. DiNardo and S. A. Wasserman
Department of Biochemistry, University of Texas Southwestern Medical Center, Dallas, Texas 75235-9038

We describe 83 recessive autosomal male-sterile mutations, generated by single P element mutagenesis in Drosophila melanogaster. Each mutation has been localized to a lettered subdivision of the polytene map. Reversion analyses, as well as complementation tests using available chromosomal deficiencies, indicate that the insertions are responsible for the mutant phenotypes. These mutations represent 63 complementation groups, 58 of which are required for spermatogenesis. Phenotypes of the spermatogenesis mutants were analyzed by light microscopy. Mutations in 12 loci affect germline proliferation, spermatocyte growth, or meiosis. Mutations in 46 other loci disrupt differentiation and maturation of spermatids into motile sperm. This collection of male-sterile mutants provides the basis for a molecular genetic analysis of spermatogenesis.

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				C. Rathke, W. M. Baarends, S. Jayaramaiah-Raja, M. Bartkuhn, R. Renkawitz, and R. Renkawitz-Pohl Transition from a nucleosome-based to a protamine-based chromatin configuration during spermiogenesis in Drosophila J. Cell Sci., May 1, 2007; 120(9): 1689 - 1700. [Abstract] [Full Text] [PDF]

				L. M. Mikhaylova, A. M. Boutanaev, and D. I. Nurminsky Transcriptional regulation by Modulo integrates meiosis and spermatid differentiation in male germ line PNAS, August 8, 2006; 103(32): 11975 - 11980. [Abstract] [Full Text] [PDF]

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				K. D. Curtin, I. A. Meinertzhagen, and R. J. Wyman Basigin (EMMPRIN/CD147) interacts with integrin to affect cellular architecture J. Cell Sci., June 15, 2005; 118(12): 2649 - 2660. [Abstract] [Full Text] [PDF]

				Y. M. Lin, P. L. Kuo, Y. H. Lin, Y. N. Teng, and J. S. N. Lin Messenger RNA transcripts of the meiotic regulator BOULE in the testis of azoospermic men and their application in predicting the success of sperm retrieval Hum. Reprod., March 1, 2005; 20(3): 782 - 788. [Abstract] [Full Text] [PDF]

				K. Weber, N. Johnson, D. Champlin, and A. Patty Many P-Element Insertions Affect Wing Shape in Drosophila melanogaster Genetics, March 1, 2005; 169(3): 1461 - 1475. [Abstract] [Full Text] [PDF]

				Y.-M. Kuo, J. L. Duncan, S. K. Westaway, H. Yang, G. Nune, E. Y. Xu, S. J. Hayflick, and J. Gitschier Deficiency of pantothenate kinase 2 (Pank2) in mice leads to retinal degeneration and azoospermia Hum. Mol. Genet., January 1, 2005; 14(1): 49 - 57. [Abstract] [Full Text] [PDF]

				L. Dorstyn, K. Mills, Y. Lazebnik, and S. Kumar The two cytochrome c species, DC3 and DC4, are not required for caspase activation and apoptosis in Drosophila cells J. Cell Biol., November 8, 2004; 167(3): 405 - 410. [Abstract] [Full Text] [PDF]

				A. B. Milchanowski, A. L. Henkenius, M. Narayanan, V. Hartenstein, and U. Banerjee Identification and Characterization of Genes Involved in Embryonic Crystal Cell Formation During Drosophila Hematopoiesis Genetics, September 1, 2004; 168(1): 325 - 339. [Abstract] [Full Text] [PDF]

				B. A. Pannebakker, L. W. Beukeboom, J. J. M. van Alphen, P. M. Brakefield, and B. J. Zwaan The Genetic Basis of Male Fertility in Relation to Haplodiploid Reproduction in Leptopilina clavipes (Hymenoptera: Figitidae) Genetics, September 1, 2004; 168(1): 341 - 349. [Abstract] [Full Text] [PDF]

				A. Matyash, H.-R. Chung, and H. Jackle Genome-wide Mapping of in Vivo Targets of the Drosophila Transcription Factor Kruppel J. Biol. Chem., July 16, 2004; 279(29): 30689 - 30696. [Abstract] [Full Text] [PDF]

				S. Sun, C.-T. Ting, and C.-I Wu The Normal Function of a Speciation Gene, Odysseus, and Its Hybrid Sterility Effect Science, July 2, 2004; 305(5680): 81 - 83. [Abstract] [Full Text] [PDF]

				A. J. Moehring and T. F. C. Mackay The Quantitative Genetic Basis of Male Mating Behavior in Drosophila melanogaster Genetics, July 1, 2004; 167(3): 1249 - 1263. [Abstract] [Full Text] [PDF]

				K. Raymond, E. Bergeret, A. Avet-Rochex, R. Griffin-Shea, and M.-O. Fauvarque A screen for modifiers of RacGAP(84C) gain-of-function in the Drosophila eye revealed the LIM kinase Cdi/TESK1 as a downstream effector of Rac1 during spermatogenesis J. Cell Sci., June 1, 2004; 117(13): 2777 - 2789. [Abstract] [Full Text] [PDF]

				B. T. Wakimoto, D. L. Lindsley, and C. Herrera Toward a Comprehensive Genetic Analysis of Male Fertility in Drosophila melanogaster Genetics, May 1, 2004; 167(1): 207 - 216. [Abstract] [Full Text] [PDF]

				S. T. Harbison, A. H. Yamamoto, J. J. Fanara, K. K. Norga, and T. F. C. Mackay Quantitative Trait Loci Affecting Starvation Resistance in Drosophila melanogaster Genetics, April 1, 2004; 166(4): 1807 - 1823. [Abstract] [Full Text] [PDF]

				P. J. Clyne, J. S. Brotman, S. T. Sweeney, and G. Davis Green Fluorescent Protein Tagging Drosophila Proteins at Their Native Genomic Loci With Small P Elements Genetics, November 1, 2003; 165(3): 1433 - 1441. [Abstract] [Full Text] [PDF]

				J. Z. Morris, C. Navarro, and R. Lehmann Identification and Analysis of Mutations in bob, Doa and Eight New Genes Required for Oocyte Specification and Development in Drosophila melanogaster Genetics, August 1, 2003; 164(4): 1435 - 1446. [Abstract] [Full Text] [PDF]

				T. Noguchi and K. G. Miller A role for actin dynamics in individualization during spermatogenesis in Drosophila melanogaster Development, May 1, 2003; 130(9): 1805 - 1816. [Abstract] [Full Text] [PDF]

				A. D. Rogat and K. G. Miller A role for myosin VI in actin dynamics at sites of membrane remodeling during Drosophila spermatogenesis J. Cell Sci., March 14, 2003; 115(24): 4855 - 4865. [Abstract] [Full Text] [PDF]

				D. A. Dansereau, M. D. Lunke, A. Finkielsztein, M. A. Russell, and W. J. Brook hephaestus encodes a polypyrimidine tract binding protein that regulates Notch signalling during wing development in Drosophila melanogaster Development, March 14, 2003; 129(24): 5553 - 5566. [Abstract] [Full Text] [PDF]

				I. M. Adham, M. A. Sallam, G. Steding, M. Korabiowska, U. Brinck, S. Hoyer-Fender, C. Oh, and W. Engel Disruption of the Pelota Gene Causes Early Embryonic Lethality and Defects in Cell Cycle Progression Mol. Cell. Biol., February 15, 2003; 23(4): 1470 - 1476. [Abstract] [Full Text] [PDF]

				Q. Lin, D. Wu, and J. Zhou The promoter targeting sequence facilitates and restricts a distant enhancer to a single promoter in the Drosophila embryo Development, February 1, 2003; 130(3): 519 - 526. [Abstract] [Full Text] [PDF]

				E. Y. Xu, D. F. Lee, A. Klebes, P. J. Turek, T. B. Kornberg, and R. A. Reijo Pera Human BOULE gene rescues meiotic defects in infertile flies Hum. Mol. Genet., January 15, 2003; 12(2): 169 - 175. [Abstract] [Full Text] [PDF]

				H.-J. Song, J.-C. Billeter, E. Reynaud, T. Carlo, E. P. Spana, N. Perrimon, S. F. Goodwin, B. S. Baker, and B. J. Taylor The fruitless Gene Is Required for the Proper Formation of Axonal Tracts in the Embryonic Central Nervous System of Drosophila Genetics, December 1, 2002; 162(4): 1703 - 1724. [Abstract] [Full Text] [PDF]

				E. Betran, K. Thornton, and M. Long Retroposed New Genes Out of the X in Drosophila Genome Res., December 1, 2002; 12(12): 1854 - 1859. [Abstract] [Full Text] [PDF]

				B. Dauwalder, S. Tsujimoto, J. Moss, and W. Mattox The Drosophila takeout gene is regulated by the somatic sex-determination pathway and affects male courtship behavior Genes & Dev., November 15, 2002; 16(22): 2879 - 2892. [Abstract] [Full Text] [PDF]

				J.-Y. Ji, M. Haghnia, C. Trusty, L. S. B. Goldstein, and G. Schubiger A Genetic Screen for Suppressors and Enhancers of the Drosophila Cdk1-Cyclin B Identifies Maternal Factors That Regulate Microtubule and Microfilament Stability Genetics, November 1, 2002; 162(3): 1179 - 1195. [Abstract] [Full Text] [PDF]