Identification of five new genes on the Y chromosome of Drosophila melanogaster

The heterochromatic state of the Drosophila Y chromosome has made the cloning and identification of Y-linked genes a challenging process. Here, we report application of a procedure to identify Y-linked gene fragments from the unmapped residue of the whole genome sequencing effort. Previously identified Y-linked genes appear in sequenced scaffolds as individual exons, apparently because many introns have become heterochromatic, growing to enormous size and becoming virtually unclonable. A TBLASTN search using all known proteins as query sequences, tested against a blastable database of the unmapped fragments, produced a number of matches consistent with this scenario. Reverse transcription–PCR and genetic methods were used to confirm those that are expressed, Y-linked genes. The five genes reported here include three protein phosphatases (Pp1-Y1, Pp1-Y2, and PPr-Y), an occludin-related gene (ORY), and a coiled-coils gene (CCY). This brings the total to nine protein-coding genes identified on the Drosophila Y chromosome. ORY and CCY may correspond, respectively, to the fertility factors ks-1 and ks-2, whereas the three protein phosphatases represent novel genes. There remains a strong functional coherence to male function among the genes on the Drosophila Y chromosome.

[1]  Thomas Hunt Morgan,et al.  Sex-linked inheritance in Drosophila , 1916 .

[2]  W. Eanes,et al.  Lack of nucleotide polymorphism in the Y-linked sperm flagellar dynein gene Dhc-Yh3 of Drosophila melanogaster and D. simulans. , 1999, Genetics.

[3]  G. Brosseau Genetic Analysis of the Male Fertility Factors on the Y Chromosome of Drosophila Melanogaster. , 1960, Genetics.

[4]  W. Swanson,et al.  The sea urchin sperm receptor for egg jelly is a modular protein with extensive homology to the human polycystic kidney disease protein, PKD1 , 1996, The Journal of cell biology.

[5]  J. Kennison The Genetic and Cytological Organization of the Y Chromosome of DROSOPHILA MELANOGASTER. , 1981, Genetics.

[6]  R. Fisher THE EVOLUTION OF DOMINANCE , 1931 .

[7]  D. Mann,et al.  Cloning of a novel testis specific protein serine/threonine phosphatase, PPN 58A, from Drosophila melanogaster. , 1998, Biochimica et biophysica acta.

[8]  S. Bonaccorsi,et al.  Y chromosome loops in Drosophila melanogaster. , 1988, Genetics.

[9]  L. Goldstein,et al.  Structural genes on the Y chromosome of Drosophila melanogaster. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[10]  P. Cohen,et al.  Novel protein serine/threonine phosphatases: variety is the spice of life. , 1997, Trends in biochemical sciences.

[11]  K. Kaiser,et al.  Drosophila melanogaster male germ line-specific transcripts with autosomal and Y-linked genes. , 1993, Genetics.

[12]  Stephen M. Mount,et al.  The genome sequence of Drosophila melanogaster. , 2000, Science.

[13]  H. Bünemann,et al.  Mega-introns in the dynein gene DhDhc7(Y) on the heterochromatic Y chromosome give rise to the giant threads loops in primary spermatocytes of Drosophila hydei. , 2000, Genetics.

[14]  B. Charlesworth,et al.  Reduced levels of microsatellite variability on the neo-Y chromosome of Drosophila miranda , 2000, Current Biology.

[15]  T. Noda,et al.  Complex phenotype of mice lacking occludin, a component of tight junction strands. , 2000, Molecular biology of the cell.

[16]  D. Hartl,et al.  Selective sweep of a newly evolved sperm-specific gene in Drosophila , 1998, Nature.

[17]  T. Hays,et al.  A fertility region on the Y chromosome of Drosophila melanogaster encodes a dynein microtubule motor. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[18]  V. Reinke,et al.  A global profile of germline gene expression in C. elegans. , 2000, Molecular cell.

[19]  W. Hennig Conventional protein coding genes in the Drosophila Y chromosome: is the puzzle of the fertility gene function solved? , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[20]  G. Bouffard,et al.  Gene discovery using computational and microarray analysis of transcription in the Drosophila melanogaster testis. , 2000, Genome research.

[21]  M. Gomendio,et al.  The Y chromosome as a battle ground for sexual selection. , 1999, Trends in ecology & evolution.

[22]  I. Gibbons Dynein family of motor proteins: present status and future questions. , 1995, Cell motility and the cytoskeleton.

[23]  A. Kajava Structural diversity of leucine-rich repeat proteins. , 1998, Journal of molecular biology.

[24]  A. Clark,et al.  Y chromosomal fertility factors kl-2 and kl-3 of Drosophila melanogaster encode dynein heavy chain polypeptides. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[25]  W. Sale,et al.  Protein phosphatases PP1 and PP2A are located in distinct positions in the Chlamydomonas flagellar axoneme. , 2000, Journal of cell science.

[26]  Sudhir Kumar,et al.  MEGA: Molecular Evolutionary Genetics Analysis software for microcomputers , 1994, Comput. Appl. Biosci..

[27]  R. Trumbly,et al.  Sds22p is a subunit of a stable isolatable form of protein phosphatase 1 (Glc7p) from Saccharomyces cerevisiae. , 2000, Archives of biochemistry and biophysics.

[28]  A. Lupas Coiled coils: new structures and new functions. , 1996, Trends in biochemical sciences.

[29]  R. Patel-King,et al.  Light chain 1 from the Chlamydomonas outer dynein arm is a leucine-rich repeat protein associated with the motor domain of the gamma heavy chain. , 1999, Biochemistry.

[30]  D. Page,et al.  Functional coherence of the human Y chromosome. , 1997, Science.