Molecular characterization and evolution of a gene family encoding both female-and male-specific reproductive proteins in Drosophila

Molecular Biology and Evolution

Volumn 31, Issue 6, 2014, Pages 1554-1567

  Sirot, Laura K ^a,b   Findlay, Geoffrey D ^a,c   Sitnik, Jessica L ^a   Frasheri, Dorina ^a,d   Avila, Frank W ^a   Wolfner, Mariana F ^a  

^a Department of Obstetrics Gynecology   (United States)

^b 931 College Mall   (United States)

^c Department of Biology   (United States)

^d Neuroscience Center Zurich and Division of Neurosurgery   (Switzerland)

Author keywords

Drosophila; gene duplication; protease; seminal proteins; sex specific expression; spermathecal proteins

Indexed keywords

PROTEINASE; SEMINAL PLASMA PROTEIN; DROSOPHILA PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; COPY NUMBER VARIATION; DROSOPHILA MELANOGASTER; FEMALE; FEMALE GENITAL SYSTEM; FERTILITY; GENE; GENE DUPLICATION; GENE EXPRESSION; GENETIC CODE; GENOTYPE; MALE; MATING; MOLECULAR EVOLUTION; MULTIGENE FAMILY; NONHUMAN; PROTEIN SECRETION; RNA INTERFERENCE; ANIMAL; BIOLOGICAL MODEL; GENETICS; METABOLISM; PHYLOGENY; REPRODUCTION; SEXUAL DEVELOPMENT;

ANIMALS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EVOLUTION, MOLECULAR; FEMALE; FERTILITY; GENE DUPLICATION; GENE EXPRESSION; GENES, INSECT; MALE; MODELS, GENETIC; MULTIGENE FAMILY; PHYLOGENY; REPRODUCTION; SEX CHARACTERISTICS;

EID: 84901427377     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msu114     Document Type: Article

References (93)

1. Allen AK, Spradling AC. 2008. The Sf1-related nuclear hormone receptor Hr39 regulates Drosophila female reproductive tract development and function. Development 135:311-321.
2. Arbeitman MN, Fleming AA, Siegal ML, Null BH, Baker BS. 2004. A genomic analysis of Drosophila somatic sexual differentiation and its regulation. Development 131:2007-2021.
3. Avila FW, Sirot LK, LaFlamme BA, Rubinstein CD, Wolfner MF. 2011. Insect seminal fluid proteins: identification and function. Annu Rev Entomol. 56:21-40.
4. Baker RH, Narechania A, Johns PM, Wilkinson GS. 2012. Gene duplication, tissue-specific gene expression and sexual conflict in stalk-eyed flies (Diopsidae). Phil Trans R Soc Lond B Biol Sci. 367: 2357-2375.
5. Begun DJ, Lindfors HA, Thompson ME, Holloway AK. 2006. Recently evolved genes identified from Drosophila yakuba and Drosophila erecta accessory gland expressed sequence tags. Genetics 172: 1675-1681.
6. Benoit P, Papin C, Kwak JE, Wickens M, Simonelig M. 2008. PAP-and GLD-2-type poly(A) polymerases are required sequentially in cytoplasmic polyadenylation and oogenesis in Drosophila. Development 135:1969-1979.
7. Berezikov E. 2011. Evolution of microRNA diversity and regulation in animals. Nat Rev Genet. 12:846-860.
8. Chan YF, Marks ME, Jones FC, Villarreal G Jr, Shapiro MD, Brady SD, Southwick AM, Absher DM, Grimwood J, Schmutz J, et al. 2010. Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science 327:302-305.
9. Chapman T. 2008. The soup in my fly: evolution, form and function of seminal fluid proteins. PLoS Biol. 6:1379-1382.
10. Chapman T, Bangham J, Vinti G, Seifried B, Lung O, Wolfner MF, Smith HK, Partridge L. 2003. The sex peptide of Drosophila melanogaster: Female post-mating responses analyzed by using RNA interference. Proc Natl Acad Sci USA. 100:9923-9928.
11. Chintapalli V, Wang J, Dow J. 2007. Using Flyatlas to identify better Drosophila models of human disease. Comp Biochem Physiol A Mol Integr Physiol. 150:S136-S137.
12. Cirera S, Aguade M. 1998. The sex-peptide gene (Acp70A) is duplicated in Drosophila subobscura. Gene 210:247-254.
13. Clark NL, Findlay GD, Yi XH, MacCoss MJ, Swanson WJ. 2007. Duplication and selection on abalone sperm lysin in an allopatric population. Mol Biol Evol. 24:2081-2090.
14. Clark NL, Swanson WJ. 2005. Pervasive adaptive evolution in primate seminal proteins. PLoS Genet. 1:335-342.
15. Clauss A, Lilja H, Lundwall A. 2005. The evolution of a genetic locus encoding small serine proteinase inhibitors. Biochem Biophys Res Commun. 333:383-389.
16. Connallon T, Clark AG. 2011. The resolution of sexual antagonism by gene duplication. Genetics 187:919-937.
17. Cui J, Sackton KL, Horner VL, Kumar KE, Wolfner MF. 2008. Wispy, the Drosophila homolog of GLD-2, is required during oogenesis and egg activation. Genetics 178:2017-2029.
18. Dietzl G, Chen D, Schnorrer F, Su KC, Barinova Y, Fellner M, Gasser B, Kinsey K, Oppel S, Scheiblauer S, et al. 2007. A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448:151-156.
19. Drosophila 12 Genomes Consortium. 2007. Evolution of genes and genomes on the Drosophila phylogeny. Nature 450:203-218.
20. Drosophila modENCODE Consortium. 2010. Identification of functional elements and regulatory circuits by Drosophila modENCODE. Science 330:1787-1797.
21. Duffy JB. 2002. GAL4 system in Drosophila: a fly geneticist's Swiss army knife. Genesis 34:1-15.
22. Felsenstein J. 2011. PHYLIP (Phylogeny Inference Package) version 3.69. Seattle: University of Washington.
23. Findlay GD, MacCoss MJ, Swanson WJ. 2009. Proteomic discovery of previously unannotated, rapidly evolving seminal fluid genes in Drosophila. Genome Res. 19:886-896.
24. Findlay GD, Sitnik JL, Wang W, Aquadro CA, Clark NL, Wolfner MF. 2014. Evolutionary rate covariation identifies new members of a protein network required for Drosophila melanogaster female post-mating responses. PLoS Genet. 10:e1004108.
25. Findlay GD, Yi XH, MacCoss MJ, Swanson WJ. 2008. Proteomics reveals novel Drosophila seminal fluid proteins transferred at mating. PLoS Biol. 6:1417-1426.
26. Gallach M, Betran E. 2011. Intralocus sexual conflict resolved through gene duplication. Trends Ecol Evol. 26:222-228.
27. Gao GJ, Cheng Y, Wesolowska N, Rong YKS. 2011. Paternal imprint essential for the inheritance of telomere identity in Drosophila. Proc Natl Acad Sci USA. 108:4932-4937.
28. Graham LA, Davies PL. 2002. The odorant-binding proteins of Drosophila melanogaster: annotation and characterization of a divergent gene family. Gene 292:43-55.
29. Harano T, Okada K, Nakayama S, Miyatake T, Hosken DJ. 2010. Intralocus sexual conflict unresolved by sex-limited trait expression. Curr Biol. 20:2036-2039.
30. Heifetz Y, Lung O, Frongillo EA, Wolfner MF. 2000. The Drosophila seminal fluid protein Acp26Aa stimulates release of oocytes by the ovary. Curr Biol. 10:99-102.
31. Hekmat-Scafe DS, Scafe CR, McKinney AJ, Tanouye MA. 2002. Genomewide analysis of the odorant-binding protein gene family in Drosophila melanogaster. Genome Res. 12:1357-1369.
32. Herndon LA, Wolfner MF. 1995. A Drosophila seminal fluid protein, Acp26Aa, stimulates egg laying in females for 1 day after mating. Proc Natl Acad Sci USA. 92:10114-10118.
33. Holland PWH, García-Fernández J. 1996. Hox genes and chordate evolution. Dev Biol. 173:382-395.
34. Horne I, Haritos VS, Oakeshott JG. 2009. Comparative and functional genomics of lipases in holometabolous insects. Insect Biochem Mol Biol. 39:547-567.
35. Hosken DJ. 2011. Gene duplication might not resolve intralocus sexual conflict. Trends Ecol Evol. 26:558-559.
36. Houck LD, Reagan NL. 1990. Male courtship pheromones increase female receptivity in a plethodontid salamander. Anim Behav. 39: 729-734.
37. Hurle B, Swanson W, Green ED, Sequencing NC. 2007. Comparative sequence analyses reveal rapid and divergent evolutionary changes of the WFDC locus in the primate lineage. Genome Res. 17:276-286.
38. Imhof M, Harr B, Brem G, Schlotterer C. 1998. Multiple mating in wild Drosophila melanogaster revisited bymicrosatellite analysis. Mol Ecol. 7:915-917.
39. Karn RC, Clark NL, Nguyen ED, SwansonWJ. 2008. Adaptive evolution in rodent seminal vesicle secretion proteins. Mol Biol Evol. 25: 2301-2310.
40. Kelleher ES, Markow TA. 2009. Duplication, selection and gene conversion in a Drosophila mojavensis female reproductive protein family. Genetics 181:1451-1465.
41. Kelleher ES, Pennington JE. 2009. Protease gene duplication and proteolytic activity in Drosophila female reproductive tracts.Mol Biol Evol. 26:2125-2134.
42. Kelleher ES, Swanson WJ, Markow TA. 2007. Gene duplication and adaptive evolution of digestive proteases in Drosophila arizonae female reproductive tracts. PLoS Genet. 3:1541-1549.
43. Kelleher ES, Watts TD, LaFlamme BA, Haynes PD, Markow TA. 2009. Proteomic analysis of Drosophila mojavensis male accessory glands suggests novel classes of seminal fluid proteins. Insect Biochem Mol Biol. 39:366-371.
44. Kresge N, Vacquier VD, Stout CD. 2001. Abalone lysin: the dissolving and evolving sperm protein. Bioessays 23:95-103.
45. LaFlamme BA, Ravi Ram K, Wolfner MF. 2012. The Drosophila melanogaster seminal fluid protease "Seminase" regulates proteolytic and post-mating reproductive processes. PLoS Genet. 8: e1002435.
46. Letunic I, Doerks T, Bork P. 2012. SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res. 40:D302-D305.
47. Lewis CA, Talbot CF, Vacquier VD. 1982. A protein from abalone sperm dissolves the vitelline layer by a non-enzymatic mechanism. Dev Biol. 92:227-239.
48. Lin HJ, Lee CM, Luo CW, Chen YH. 2005. Functional preservation of duplicated pair for RSVS III gene in the REST locus of rat 3q42. Biochem Biophys Res Commun. 326: 355-363.
49. Liu HF, Kubli E. 2003. Sex-peptide is the molecular basis of the sperm effect in Drosophila melanogaster. Proc Natl Acad Sci USA. 100: 9929-9933.
50. Lynch M, Conery JS. 2000. The evolutionary fate and consequences of duplicate genes. Science 290:1151-1155.
51. Lynch M, Force A. 2000. The probability of duplicate gene preservation by subfunctionalization. Genetics 154:459-473.
52. Makino T, McLysaght A. 2010. Ohnologs in the human genome are dosage balanced and frequently associated with disease. Proc Natl Acad Sci USA. 107:9270-9274.
53. Mancini E, Baldini F, Tammaro F, Calzetta M, Serrao A, George P,Morlais I, Masiga D, Sharakhov IV, Rogers DW, et al. 2011. Molecular characterization and evolution of a gene family encoding male-specific reproductive proteins in the African malaria vector Anopheles gambiae. BMC Evol Biol. 11:292.
54. Mancini E, Tammaro F, Baldini F, Via A, Raimondo D, George P, Audisio P, Sharakhov IV, Tramontano A, Catteruccia F, et al. 2011. Molecular evolution of a gene cluster of serine proteases expressed in the Anopheles gambiae female reproductive tract. BMC Evol Biol. 11:72.
55. Marygold SJ, Leyland PC, Seal RL, Goodman JL, Thurmond J, Strelets VB, Wilson RJ, FlyBase C. 2013. FlyBase: improvements to the bibliography. Nucleic Acids Res. 41:D751-D757.
56. Mueller JL, Linklater JR, Ram KR, Chapman T, Wolfner MR. 2008. Targeted gene deletion and phenotypic analysis of the Drosophila melanogaster seminal fluid protease inhibitor Acp62F. Genetics 178: 1605-1614.
57. NielsenMG, Caserta JM, Kidd SJ, Phillips CM. 2006. Functional constraint underlies 60 million year stasis of Dipteran testis-specific beta-tubulin. Evol Dev. 8:23-29.
58. Nielsen MG, Gadagkar SR, Gutzwiller L. 2010. Tubulin evolution in insects: gene duplication and subfunctionalization provide specialized isoforms in a functionally constrained gene family. BMC Evol Biol. 10: 113.
59. Ohno S. 1970. Evolution by gene duplication. New York: Springer-Verlag.
60. Ohta T. 2003. Evolution by gene duplication revisited: differentiation of regulatory elements versus proteins. Genetica 118:209-216.
61. Parsch J, Meiklejohn CD, Hauschteck-Jungen E, Hunziker P, Hartl DL. 2001. Molecular evolution of the ocnus and janus genes in the Drosophila melanogaster species subgroup. Mol Biol Evol. 18: 801-811.
62. Prokupek AM, Kachman SD, Ladunga I, Harshman LG. 2009. Transcriptional profiling of the sperm storage organs of Drosophila melanogaster. Insect Mol Biol. 18:465-475.
63. Punta M, Coggill PC, Eberhardt RY,Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, et al. 2012. The Pfam protein families database. Nucleic Acids Res. 40:D290-D301.
64. Raff EC, Hutchens JA, Hoyle HD, Nielsen MG, Turner FR. 2000. Conserved axoneme symmetry altered by a component beta-tubulin. Curr Biol. 10:1391-1394.
65. Ravi Ram K, Wolfner MF. 2007a. Seminal influences: Drosophila Acps and the molecular interplay between males and females during reproduction. Integr Comp Biol. 47:427-445.
66. Ravi Ram K, Wolfner MF. 2007b. Sustained post-mating response in Drosophila melanogaster requires multiple seminal fluid proteins. PLoS Genet. 3:2428-2438.
67. Rebeiz M, Jikomes N, Kassner VA, Carroll SB. 2011. Evolutionary origin of a novel gene expression pattern through co-option of the latent activities of existing regulatory sequences. Proc Natl Acad Sci USA. 108:10036-10043.
68. Rodin SN, Riggs AD. 2003. Epigenetic silencing may aid evolution by gene duplication. J Mol Evol. 56:718-729.
69. Rogers DW, Baldini F, Battaglia F, Panico M, Dell A, Morris HR, Catteruccia F. 2009. Transglutaminase-mediated semen coagulation controls sperm storage in the malaria mosquito. PLoS Biol. 7: e1000272.
70. Rollmann SM, Houck LD, Feldhoff RC. 1999. Proteinaceous pheromone affecting female receptivity in a terrestrial salamander. Science 285: 1907-1909.
71. Ross J, Jiang H, Kanost MR, Wang Y. 2003. Serine proteases and their homologs in the Drosophila melanogaster genome: an initial analysis of sequence conservation and phylogenetic relationships. Gene 304: 117-131.
72. Roth C, Rastogi S, Arvestad L, Dittmar K, Light S, Ekman D, Liberles DA. 2007. Evolution after gene duplication: models, mechanisms, sequences, systems, and organisms. J Exp Zool Part B. 308B: 58-73.
73. Sartain CV, Cui J, Meisel RP, Wolfner MF. 2011. The poly(A) polymerase GLD2 is required for spermatogenesis in Drosophila melanogaster. Development 138:1619-1629.
74. Schnakenberg SL, Matias WR, Siegal ML. 2011. Sperm-storage defects and live birth in Drosophila females lacking spermathecal secretory cells. PLoS Biol. 9:e1001192.
75. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li WZ, Lopez R, McWilliam H, Remmert M, Soding J, et al. 2011. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol. 7:539.
76. Sirot LK, Hardstone MC, Helinski MEH, Ribeiro JMC, Kimura M, Deewatthanawong P, Wolfner MF, Harrington LC. 2011. Towards a semen proteome of the Dengue vector mosquito: protein identification and potential functions. PLoS Negl Trop Dis. 5: e989.
77. Sirot LK, LaFlamme BA, Sitnik JL, Rubinstein CD, Avila FW, Chow CY, Wolfner MF. 2009. Molecular social interactions: Drosophila melanogaster seminal fluid proteins as a case study. Adv Genet. 68: 23-56.
78. Sirot LK, Poulson RL, McKenna MC, Girnary H, Wolfner MF, Harrington LC. 2008. Identity and transfer of male reproductive gland proteins of the dengue vector mosquito, Aedes aegypti: potential tools for control of female feeding and reproduction. Insect Biochem Mol Biol. 38:176-189.
79. Smith RC, Walter MF, Hice RH, O'Brochta DA, Atkinson PW. 2007. Testis-specific expression of the beta 2 tubulin promoter of Aedes aegypti and its application as a genetic sex-separation marker. Insect Mol Biol. 16:61-71.
80. St Pierre SE, Ponting L, Stefancsik R, McQuilton P, the FlyBase Consortium. 2013. FlyBase 102-advanced approaches to interrogating FlyBase. Nucleic Acids Res. 42:D780-D788.
81. Stewart AD, Pischedda A, Rice WR. 2010. Resolving intralocus sexual conflict: genetic mechanisms and time frame. J Hered. 101: S94-S99.
82. Stewart F, Allen WR. 1995. Comparative aspects of the evolution and function of the chorionic gonadotrophins. Reprod Domest Anim. 30: 231-239.
83. Swanson WJ, Clark AG, Waldrip-Dail HM, Wolfner MF, Aquadro CF. 2001. Evolutionary EST analysis identifies rapidly evolving male reproductive proteins in Drosophila. Proc Natl Acad Sci USA. 98: 7375-7379.
84. Swanson WJ, Vacquier VD. 1995. Extraordinary divergence and positive Darwinian selection in a fusagenic protein coating the acrosomal process of abalone spermatozoa. Proc Natl Acad Sci USA. 92: 4957-4961.
85. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 28:2731-2739.
86. Tian X, Pascal G, Monget P. 2009. Evolution and functional divergence of NLRP genes in mammalian reproductive systems. BMC Evol Biol. 9:202.
87. Torgerson DG, Singh RS. 2004. Rapid evolution through gene duplication and subfunctionalization of the testesspecific alpha 4 proteasome subunits in Drosophila. Genetics 168: 1421-1432.
88. Vacquier VD, Swanson WJ, Lee YH. 1997. Positive Darwinian selection on two homologous fertilization proteins: What is the selective pressure driving their divergence? J Mol Evol. 44: S15-S22.
89. Wagstaff BJ, Begun DJ. 2005. Comparative genomics of accessory gland protein genes in Drosophila melanogaster and D. pseudoobscura. Mol Biol Evol. 22:818-832.
90. Wagstaff BJ, Begun DJ. 2007. Adaptive evolution of recently duplicated accessory gland protein genes in desert Drosophila. Genetics 177: 1023-1030.
91. Wolfner MF. 2009. Battle and ballet: molecular interactions between the sexes in Drosophila. J Hered. 100:399-410.
92. Yapici N, Kim YJ, Ribeiro C, Dickson BJ. 2008. A receptor that mediates the post-mating switch in Drosophila reproductive behaviour. Nature 451:33-37.
93. Zhang JZ. 2003. Evolution by gene duplication: an update. Trends Ecol Evol. 18:292-298.