The Drosophila Gene Interacts Genetically with and Shows Female-Specific Effects of Divergence
Animals need to make gametes–sperm or eggs–in order to reproduce. Gametes are produced from a specialized tissue called the germline that is found within the testes or ovaries. These organs contain a small population of stem cells that are able to both self-renew and differentiate to generate gametes and are thus essential for maintaining gamete production throughout the reproductive lifespan of most animals. Surprisingly, some of the genes that control this process evolve rapidly between Drosophila species. We find for a key germline stem cell regulatory gene, bag of marbles (bam), that its rapid evolution affects only female but not male functions. We further report that the endosymbiont bacterium Wolbachia that infects insects and other species interacts with bam and may be contributing to the wider pattern of rapid evolution of germline stem cell regulatory genes.
Vyšlo v časopise:
The Drosophila Gene Interacts Genetically with and Shows Female-Specific Effects of Divergence. PLoS Genet 11(8): e32767. doi:10.1371/journal.pgen.1005453
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1005453
Souhrn
Animals need to make gametes–sperm or eggs–in order to reproduce. Gametes are produced from a specialized tissue called the germline that is found within the testes or ovaries. These organs contain a small population of stem cells that are able to both self-renew and differentiate to generate gametes and are thus essential for maintaining gamete production throughout the reproductive lifespan of most animals. Surprisingly, some of the genes that control this process evolve rapidly between Drosophila species. We find for a key germline stem cell regulatory gene, bag of marbles (bam), that its rapid evolution affects only female but not male functions. We further report that the endosymbiont bacterium Wolbachia that infects insects and other species interacts with bam and may be contributing to the wider pattern of rapid evolution of germline stem cell regulatory genes.
Zdroje
1. Panhuis TM, Clark NL, Swanson WJ (2006) Rapid evolution of reproductive proteins in abalone and Drosophila. Philos Trans R Soc Lond B Biol Sci 361: 261–268. 16612885
2. Swanson WJ, Vacquier VD (2002) The rapid evolution of reproductive proteins. Nat Rev Genet 3: 137–144. 11836507
3. Turner LM, Hoekstra HE (2008) Causes and consequences of the evolution of reproductive proteins. Int J Dev Biol 52: 769–780. doi: 10.1387/ijdb.082577lt 18649289
4. Haerty W, Jagadeeshan S, Kulathinal RJ, Wong A, Ravi Ram K, et al (2007) Evolution in the fast lane: rapidly evolving sex-related genes in Drosophila. Genetics 177: 1321–1335. 18039869
5. Clark NL, Aagaard JE, Swanson WJ (2006) Evolution of reproductive proteins from animals and plants. Reproduction 131: 11–22. 16388004
6. Swanson WJ, Wong A, Wolfner MF, Aquadro CF (2004) Evolutionary expressed sequence tag analysis of Drosophila female reproductive tracts identifies genes subjected to positive selection. Genetics 168: 1457–1465. 15579698
7. Begun DJ, Holloway AK, Stevens K, Hillier LW, Poh Y-P, et al (2007) Population genomics: whole-genome analysis of polymorphism and divergence in Drosophila simulans. PLoS Biol 5: e310. 17988176
8. Clark AG, Eisen MB, Smith DR, Bergman CM, Oliver B, et al (2007) Evolution of genes and genomes on the Drosophila phylogeny. Nature 450: 203–218. 17994087
9. Kosiol C, Vinar T, da Fonseca RR, Hubisz MJ, Bustamante CD, et al (2008) Patterns of positive selection in six Mammalian genomes. PLoS Genet 4: e1000144. doi: 10.1371/journal.pgen.1000144 18670650
10. Larracuente AM, Sackton TB, Greenberg AJ, Wong A, Singh ND, et al (2008) Evolution of protein-coding genes in Drosophila. Trends Genet 24: 114–123. doi: 10.1016/j.tig.2007.12.001 18249460
11. Dean MD, Clark NL, Findlay GD, Karn RC, Yi X, et al (2009) Proteomics and comparative genomic investigations reveal heterogeneity in evolutionary rate of male reproductive proteins in mice (Mus domesticus). Mol Biol Evol 26: 1733–1743. doi: 10.1093/molbev/msp094 19420050
12. Bauer DuMont VL, Flores HA, Wright MH, Aquadro CF (2007) Recurrent positive selection at bgcn, a key determinant of germ line differentiation, does not appear to be driven by simple coevolution with its partner protein bam. Mol Biol Evol 24: 182–191. 17056645
13. Civetta A, Rajakumar SA, Brouwers B, Bacik JP (2006) Rapid evolution and gene-specific patterns of selection for three genes of spermatogenesis in Drosophila. Mol Biol Evol 23: 655–662. 16357040
14. Langley CH, Stevens K, Cardeno C, Lee YCG, Schrider DR, et al (2012) Genomic variation in natural populations of Drosophila melanogaster. Genetics 192: 533–598. doi: 10.1534/genetics.112.142018 22673804
15. Wong MD, Jin Z, Xie T (2005) Molecular mechanisms of germline stem cell regulation. Annu Rev Genet 39: 173–195. 16285857
16. Xie T, Song X, Jin Z, Pan L, Weng C, et al (2008) Interactions between stem cells and their niche in the Drosophila ovary. Cold Spring Harb Symp Quant Biol 73: 39–47. doi: 10.1101/sqb.2008.73.014 19022749
17. Chen D, McKearin D (2005) Gene circuitry controlling a stem cell niche. Curr Biol 15: 179–184. 15668176
18. Fuller MT, Spradling AC (2007) Male and female Drosophila germline stem cells: two versions of immortality. Science 316: 402–404. 17446390
19. Song X, Wong MD, Kawase E, Xi R, Ding BC, et al (2004) Bmp signals from niche cells directly repress transcription of a differentiation-promoting gene, bag of marbles, in germline stem cells in the Drosophila ovary. Development 131: 1353–1364. 14973291
20. Chen D, McKearin D (2003) Dpp signaling silences bam transcription directly to establish asymmetric divisions of germline stem cells. Curr Biol 13: 1786–1791. 14561403
21. Chen D, McKearin DM (2003) A discrete transcriptional silencer in the bam gene determines asymmetric division of the Drosophila germline stem cell. Development 130: 1159–1170. 12571107
22. McKearin D, Ohlstein B (1995) A role for the Drosophila bag-of-marbles protein in the differentiation of cystoblasts from germline stem cells. Development 121: 2937–2947. 7555720
23. McKearin DM, Spradling AC (1990) bag-of-marbles: a Drosophila gene required to initiate both male and female gametogenesis. Genes Dev 4: 2242–2251. 2279698
24. Gönczy P, Matunis E, DiNardo S (1997) bag-of-marbles and benign gonial cell neoplasm act in the germline to restrict proliferation during Drosophila spermatogenesis. Development 124: 4361–4371. 9334284
25. Insco ML, Leon A, Tam CH, McKearin DM, Fuller MT (2009) Accumulation of a differentiation regulator specifies transit amplifying division number in an adult stem cell lineage. Proc Natl Acad Sci U S A 106: 22311–22316. doi: 10.1073/pnas.0912454106 20018708
26. de Cuevas M, Spradling AC (1998) Morphogenesis of the Drosophila fusome and its implications for oocyte specification. Development 125: 2781–2789. 9655801
27. Lavoie CA, Ohlstein B, McKearin DM (1999) Localization and function of Bam protein require the benign gonial cell neoplasm gene product. Dev Biol 212: 405–413. 10433830
28. Hawkins NC, Thorpe J, Schüpbach T (1996) Encore, a gene required for the regulation of germ line mitosis and oocyte differentiation during Drosophila oogenesis. Development 122: 281–290. 8565840
29. Lilly MA, de Cuevas M, Spradling AC (2000) Cyclin A associates with the fusome during germline cyst formation in the Drosophila ovary. Dev Biol 218: 53–63. 10644410
30. Insco ML, Bailey AS, Kim J, Olivares GH, Wapinski OL, et al (2012) A self-limiting switch based on translational control regulates the transition from proliferation to differentiation in an adult stem cell lineage. Cell Stem Cell 11: 689–700. doi: 10.1016/j.stem.2012.08.012 23122292
31. Ohlstein B, Lavoie CA, Vef O, Gateff E, McKearin DM (2000) The Drosophila cystoblast differentiation factor, benign gonial cell neoplasm, is related to DExH-box proteins and interacts genetically with bag-of-marbles. Genetics 155: 1809–1819. 10924476
32. Shen R, Weng C, Yu J, Xie T (2009) eIF4A controls germline stem cell self-renewal by directly inhibiting BAM function in the Drosophila ovary. Proc Natl Acad Sci U S A 106: 11623–11628. doi: 10.1073/pnas.0903325106 19556547
33. Li Y, Minor NT, Park JK, McKearin DM, Maines JZ (2009) Bam and Bgcn antagonize Nanos-dependent germ-line stem cell maintenance. Proc Natl Acad Sci U S A 106: 9304–9309. doi: 10.1073/pnas.0901452106 19470484
34. Chau J, Kulnane LS, Salz HK (2009) Sex-lethal facilitates the transition from germline stem cell to committed daughter cell in the Drosophila ovary. Genetics 182: 121–132. doi: 10.1534/genetics.109.100693 19237687
35. Chau J, Kulnane LS, Salz HK (2012) Sex-lethal enables germline stem cell differentiation by down-regulating Nanos protein levels during Drosophila oogenesis. Proc Natl Acad Sci U S A 109: 9465–9470. doi: 10.1073/pnas.1120473109 22645327
36. Li Y, Zhang Q, Carreira-Rosario A, Maines JZ, McKearin DM, Buszczak M (2013) Mei-p26 cooperates with Bam, Bgcn and Sxl to promote early germline development in the Drosophila ovary. PLoS One 8: e58301. doi: 10.1371/journal.pone.0058301 23526974
37. Veneti Z, Bentley JK, Koana T, Braig HR, Hurst GDD (2005) A functional dosage compensation complex required for male killing in Drosophila. Science 307: 1461–1463. 15746426
38. Hornett EA, Charlat S, Duplouy AMR, Davies N, Roderick GK, et al (2006) Evolution of male-killer suppression in a natural population. PLoS Biol 4: e283. 16933972
39. Werren JH, Baldo L, Clark ME (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6: 741–751. doi: 10.1038/nrmicro1969 18794912
40. Serbus LR, Casper-Lindley C, Landmann F, Sullivan W (2008) The genetics and cell biology of Wolbachia-host interactions. Annu Rev Genet 42: 683–707. doi: 10.1146/annurev.genet.41.110306.130354 18713031
41. Starr DJ, Cline TW (2002) A host parasite interaction rescues Drosophila oogenesis defects. Nature 418: 76–79. 12097909
42. Sun S, Cline TW (2009) Effects of Wolbachia infection and ovarian tumor mutations on Sex-lethal germline functioning in Drosophila. Genetics 181: 1291–1301. doi: 10.1534/genetics.108.099374 19171941
43. Boyle L, O'Neill SL, Robertson HM, Karr TL (1993) Interspecific and intraspecific horizontal transfer of Wolbachia in Drosophila. Science 260: 1796–1799. 8511587
44. McGraw EA, Merritt DJ, Droller JN, O'Neill SL (2002) Wolbachia density and virulence attenuation after transfer into a novel host. Proc Natl Acad Sci U S A 99: 2918–2923. 11880639
45. Serbus LR, Ferreccio A, Zhukova M, McMorris CL, Kiseleva E, Sullivan W (2011) A feedback loop between Wolbachia and the Drosophila gurken mRNP complex influences Wolbachia titer. J Cell Sci 124: 4299–4308. doi: 10.1242/jcs.092510 22193955
46. Fast EM, Toomey ME, Panaram K, Desjardins D, Kolaczyk ED, Frydman HM (2011) Wolbachia enhance Drosophila stem cell proliferation and target the germline stem cell niche. Science 334: 990–992. doi: 10.1126/science.1209609 22021671
47. Albertson R, Tan V, Leads RR, Reyes M, Sullivan W, Casper-Lindley C (2013) Mapping Wolbachia distributions in the adult Drosophila brain. Cell Microbiol 15: 1527–1544. doi: 10.1111/cmi.12136 23490256
48. Toomey ME, Panaram K, Fast EM, Beatty C, Frydman HM (2013) Evolutionarily conserved Wolbachia-encoded factors control pattern of stem-cell niche tropism in Drosophila ovaries and favor infection. Proc Natl Acad Sci U S A 110: 10788–10793. doi: 10.1073/pnas.1301524110 23744038
49. Frydman HM, Li JM, Robson DN, Wieschaus E (2006) Somatic stem cell niche tropism in Wolbachia. Nature 441: 509–512. 16724067
50. Poinsot D, Bourtzis K, Markakis G, Savakis C, Merçot H (1998) Wolbachia transfer from Drosophila melanogaster into D. simulans: Host effect and cytoplasmic incompatibility relationships. Genetics 150: 227–237. 9725842
51. Chen D, Wang Q, Huang H, Xia L, Jiang X, et al (2009) Effete-mediated degradation of Cyclin A is essential for the maintenance of germline stem cells in Drosophila. Development 136: 4133–4142. doi: 10.1242/dev.039032 19906849
52. Xia L, Jia S, Huang S, Wang H, Zhu Y, et al (2010) The Fused/Smurf complex controls the fate of Drosophila germline stem cells by generating a gradient BMP response. Cell 143: 978–990. doi: 10.1016/j.cell.2010.11.022 21145463
53. Kirilly D, Xie T (2007) The Drosophila ovary: an active stem cell community. Cell Res 17: 15–25. 17199109
54. Yue L, Spradling AC (1992) hu-li tai shao, a gene required for ring canal formation during Drosophila oogenesis, encodes a homolog of adducin. Genes Dev 6: 2443–2454. 1340461
55. de Cuevas M, Lee JK, Spradling AC (1996) alpha-spectrin is required for germline cell division and differentiation in the Drosophila ovary. Development 122: 3959–3968. 9012516
56. Maheshwari S, Barbash DA (2011) The genetics of hybrid incompatibilities. Annu Rev Genet 45: 331–355. doi: 10.1146/annurev-genet-110410-132514 21910629
57. Maheshwari S, Barbash DA (2012) Cis-by-Trans regulatory divergence causes the asymmetric lethal effects of an ancestral hybrid incompatibility gene. PLoS Genet 8: e1002597. doi: 10.1371/journal.pgen.1002597 22457639
58. Pan L, Wang S, Lu T, Weng C, Song X, et al (2014) Protein competition switches the function of COP9 from self-renewal to differentiation. Nature 514: 233–236. doi: 10.1038/nature13562 25119050
59. Ferree PM, Frydman HM, Li JM, Cao J, Wieschaus E, Sullivan W (2005) Wolbachia utilizes host microtubules and Dynein for anterior localization in the Drosophila oocyte. PLoS Pathog 1: e14. 16228015
60. Serbus LR, Sullivan W (2007) A cellular basis for Wolbachia recruitment to the host germline. PLoS Pathog 3: e190. 18085821
61. Groth AC, Fish M, Nusse R, Calos MP (2004) Construction of transgenic Drosophila by using the site-specific integrase from phage phiC31. Genetics 166: 1775–1782. 15126397
62. Landry CR, Wittkopp PJ, Taubes CH, Ranz JM, Clark AG, Hartl DL (2005) Compensatory cis-trans evolution and the dysregulation of gene expression in interspecific hybrids of Drosophila. Genetics 171: 1813–1822. 16143608
63. Takahasi KR, Matsuo T, Takano-Shimizu-Kouno T (2011) Two types of cis-trans compensation in the evolution of transcriptional regulation. Proc Natl Acad Sci U S A 108: 15276–15281. doi: 10.1073/pnas.1105814108 21876147
64. Masly JP, Presgraves DC (2007) High-resolution genome-wide dissection of the two rules of speciation in Drosophila. PLoS Biol 5: e243. 17850182
65. Tao Y, Chen S, Hartl DL, Laurie CC (2003) Genetic dissection of hybrid incompatibilities between Drosophila simulans and D. mauritiana. I. Differential accumulation of hybrid male sterility effects on the X and autosomes. Genetics 164: 1383–1397. 12930747
66. Hollocher H, Wu CI (1996) The genetics of reproductive isolation in the Drosophila simulans clade: X vs. autosomal effects and male vs. female effects. Genetics 143: 1243–1255. 8807297
67. Llopart A (2012) The rapid evolution of X-linked male-biased gene expression and the large-X effect in Drosophila yakuba, D. santomea, and their hybrids. Mol Biol Evol 29: 3873–3886. doi: 10.1093/molbev/mss190 22844069
68. Meiklejohn CD, Parsch J, Ranz JM, Hartl DL (2003) Rapid evolution of male-biased gene expression in Drosophila. Proc Natl Acad Sci U S A 100: 9894–9899. 12907700
69. Wong A, Turchin MC, Wolfner MF, Aquadro CF (2008) Evidence for positive selection on Drosophila melanogaster seminal fluid protease homologs. Mol Biol Evol 25: 497–506. 18056920
70. Begun DJ, Whitley P, Todd BL, Waldrip-Dail HM, Clark AG (2000) Molecular population genetics of male accessory gland proteins in Drosophila. Genetics 156: 1879–1888. 11102381
71. Ohlstein B, McKearin D (1997) Ectopic expression of the Drosophila Bam protein eliminates oogenic germline stem cells. Development 124: 3651–3662. 9342057
72. Schulz C, Kiger AA, Tazuke SI, Yamashita YM, Pantalena-Filho LC, et al (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. 15238523
73. Kawase E, Wong MD, Ding BC, Xie T (2004) Gbb/Bmp signaling is essential for maintaining germline stem cells and for repressing bam transcription in the Drosophila testis. Development 131: 1365–1375. 14973292
74. Sheng XR, Brawley CM, Matunis EL (2009) Dedifferentiating spermatogonia outcompete somatic stem cells for niche occupancy in the Drosophila testis. Cell Stem Cell 5: 191–203. doi: 10.1016/j.stem.2009.05.024 19664993
75. Jin Z, Kirilly D, Weng C, Kawase E, Song X, et al (2008) Differentiation-defective stem cells outcompete normal stem cells for niche occupancy in the Drosophila ovary. Cell Stem Cell 2: 39–49. doi: 10.1016/j.stem.2007.10.021 18371420
76. León A, McKearin D (1999) Identification of TER94, an AAA ATPase protein, as a Bam-dependent component of the Drosophila fusome. Mol Biol Cell 10: 3825–3834. 10564274
77. Lighthouse DV, Buszczak M, Spradling AC (2008) New components of the Drosophila fusome suggest it plays novel roles in signaling and transport. Dev Biol 317: 59–71. doi: 10.1016/j.ydbio.2008.02.009 18355804
78. Salz HK (2013) Sex, stem cells and tumors in the Drosophila ovary. Fly (Austin) 7: 3–7.
79. Choi JY, Aquadro CF (2014) The coevolutionary period of Wolbachia pipientis infecting Drosophila ananassae and its impact on the evolution of the host germline stem cell regulating genes. Mol Biol Evol 31: 2457–2471. doi: 10.1093/molbev/msu204 24974378
80. Ellegaard KM, Klasson L, Näslund K, Bourtzis K, Andersson SGE (2013) Comparative genomics of Wolbachia and the bacterial species concept. PLoS Genet 9: e1003381. doi: 10.1371/journal.pgen.1003381 23593012
81. Richardson MF, Weinert LA, Welch JJ, Linheiro RS, Magwire MM, et al (2012) Population genomics of the Wolbachia endosymbiont in Drosophila melanogaster. PLoS Genet 8: e1003129. doi: 10.1371/journal.pgen.1003129 23284297
82. Early AM, Clark AG (2013) Monophyly of Wolbachia pipientis genomes within Drosophila melanogaster: geographic structuring, titre variation and host effects across five populations. Mol Ecol 22: 5765–5778. doi: 10.1111/mec.12530 24118111
83. Teixeira L, Ferreira A, Ashburner M (2008) The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol 6: e2.
84. Hedges LM, Brownlie JC, O'Neill SL, Johnson KN (2008) Wolbachia and virus protection in insects. Science 322: 702. doi: 10.1126/science.1162418 18974344
85. Osborne SE, Iturbe-Ormaetxe I, Brownlie JC, O'Neill SL, Johnson KN (2012) Antiviral protection and the importance of Wolbachia density and tissue tropism in Drosophila simulans. Appl Environ Microbiol 78: 6922–6929. doi: 10.1128/AEM.01727-12 22843518
86. Martinez J, Longdon B, Bauer S, Chan Y-S, Miller WJ, et al (2014) Symbionts commonly provide broad spectrum resistance to viruses in insects: a comparative analysis of Wolbachia strains. PLoS Pathog 10: e1004369. doi: 10.1371/journal.ppat.1004369 25233341
87. Riegler M, Sidhu M, Miller WJ, O'Neill SL (2005) Evidence for a global Wolbachia replacement in Drosophila melanogaster. Curr Biol 15: 1428–1433. 16085497
88. Kriesner P, Hoffmann AA, Lee SF, Turelli M, Weeks AR (2013) Rapid sequential spread of two Wolbachia variants in Drosophila simulans. PLoS Pathog 9: e1003607. doi: 10.1371/journal.ppat.1003607 24068927
89. Chrostek E, Marialva MSP, Esteves SS, Weinert LA, Martinez J, et al (2013) Wolbachia variants induce differential protection to viruses in Drosophila melanogaster: a phenotypic and phylogenomic analysis. PLoS Genet 9: e1003896. doi: 10.1371/journal.pgen.1003896 24348259
90. Dedeine F, Vavre F, Fleury F, Loppin B, Hochberg ME, Bouletreau M (2001) Removing symbiotic Wolbachia bacteria specifically inhibits oogenesis in a parasitic wasp. Proc Natl Acad Sci U S A 98: 6247–6252. 11353833
91. Dedeine F, Boulétreau M, Vavre F (2005) Wolbachia requirement for oogenesis: occurrence within the genus Asobara (Hymenoptera, Braconidae) and evidence for intraspecific variation in A. tabida. Heredity 95: 394–400. 16118660
92. Pannebakker BA, Loppin B, Elemans CPH, Humblot L, Vavre F (2007) Parasitic inhibition of cell death facilitates symbiosis. Proc Natl Acad Sci U S A 104: 213–215. 17190825
93. Brennan LJ, Keddie BA, Braig HR, Harris HL (2008) The endosymbiont Wolbachia pipientis induces the expression of host antioxidant proteins in an Aedes albopictus cell line. PLoS One 3: e2083. doi: 10.1371/journal.pone.0002083 18461124
94. Xi Z, Gavotte L, Xie Y, Dobson SL (2008) Genome-wide analysis of the interaction between the endosymbiotic bacterium Wolbachia and its Drosophila host. BMC Genomics 9: 1. doi: 10.1186/1471-2164-9-1 18171476
95. Kremer N, Voronin D, Charif D, Mavingui P, Mollereau B, Vavre F (2009) Wolbachia interferes with ferritin expression and iron metabolism in insects. PLoS Pathog 5: e1000630. doi: 10.1371/journal.ppat.1000630 19851452
96. Kremer N, Charif D, Henri H, Gavory F, Wincker P, et al (2012) Influence of Wolbachia on host gene expression in an obligatory symbiosis. BMC Microbiol 12 Suppl 1: S7. doi: 10.1186/1471-2180-12-S1-S7 22376153
97. Pan L, Chen S, Weng C, Call G, Zhu D, et al (2007) Stem cell aging is controlled both intrinsically and extrinsically in the Drosophila ovary. Cell Stem Cell 1: 458–469. doi: 10.1016/j.stem.2007.09.010 18371381
98. LaFever L, Drummond-Barbosa D (2005) Direct control of germline stem cell division and cyst growth by neural insulin in Drosophila. Science 309: 1071–1073. 16099985
99. Hsu H-J, Drummond-Barbosa D (2009) Insulin levels control female germline stem cell maintenance via the niche in Drosophila. Proc Natl Acad Sci U S A 106: 1117–1121. doi: 10.1073/pnas.0809144106 19136634
100. Drummond-Barbosa D (2008) Stem cells, their niches and the systemic environment: an aging network. Genetics 180: 1787–1797. doi: 10.1534/genetics.108.098244 19087970
101. Boyle M, Wong C, Rocha M, Jones DL (2007) Decline in self-renewal factors contributes to aging of the stem cell niche in the Drosophila testis. Cell Stem Cell 1: 470–478. doi: 10.1016/j.stem.2007.08.002 18371382
102. Wu M, Sun LV, Vamathevan J, Riegler M, Deboy R, et al (2004) Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: a streamlined genome overrun by mobile genetic elements. PLoS Biol 2: E69. 15024419
103. Klasson L, Westberg J, Sapountzis P, Näslund K, Lutnaes Y, et al (2009) The mosaic genome structure of the Wolbachia wRi strain infecting Drosophila simulans. Proc Natl Acad Sci U S A 106: 5725–5730. doi: 10.1073/pnas.0810753106 19307581
104. Caturegli P, Asanovich KM, Walls JJ, Bakken JS, Madigan JE, et al (2000) ankA: an Ehrlichia phagocytophila group gene encoding a cytoplasmic protein antigen with ankyrin repeats. Infect Immun 68: 5277–5283. 10948155
105. Flores HA, Bauer DuMont VL, Fatoo A, Hubbard D, Hijji M, et al (2015) Adaptive Evolution of Genes Involved in the Regulation of Germline Stem Cells in Drosophila melanogaster and Drosophila simulans. G3 (Bethesda).
106. St Pierre SE, Ponting L, Stefancsik R, McQuilton P, FlyBase Consortium (2014) FlyBase 102—advanced approaches to interrogating FlyBase. Nucleic Acids Res 42: D780–D788. doi: 10.1093/nar/gkt1092 24234449
107. Zhou W, Rousset F, O'Neil S (1998) Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Proc Biol Sci 265: 509–515. 9569669
108. Brideau NJ, Flores HA, Wang J, Maheshwari S, Wang X, Barbash DA (2006) Two Dobzhansky-Muller genes interact to cause hybrid lethality in Drosophila. Science 314: 1292–1295. 17124320
109. Venken KJT, He Y, Hoskins RA, Bellen HJ (2006) P[acman]: a BAC transgenic platform for targeted insertion of large DNA fragments in D. melanogaster. Science 314: 1747–1751. 17138868
110. Newell PD, Douglas AE (2014) Interspecies interactions determine the impact of the gut microbiota on nutrient allocation in Drosophila melanogaster. Appl Environ Microbiol 80: 788–796. doi: 10.1128/AEM.02742-13 24242251
111. McGraw EA, Merritt DJ, Droller JN, O'Neill SL (2001) Wolbachia-mediated sperm modification is dependent on the host genotype in Drosophila. Proc Biol Sci 268: 2565–2570. 11749711
112. Aruna S, Flores HA, Barbash DA (2009) Reduced fertility of Drosophila melanogaster hybrid male rescue (Hmr) mutant females is partially complemented by Hmr orthologs from sibling species. Genetics 181: 1437–1450. doi: 10.1534/genetics.108.100057 19153254
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Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
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