A Pair of Centromeric Proteins Mediates Reproductive Isolation in Drosophila Species

Developmental Cell

Volumn 27, Issue 4, 2013, Pages 412-424

  Thomae, Andreas W ^a   Schade, Georg O M ^b,c   Padeken, Jan ^b,c   Borath, Marc ^a   Vetter, Irene ^a   Kremmer, Elisabeth ^d   Heun, Patrick ^b   Imhof, Axel ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

^c UNIVERSITY OF FREIBURG   (Germany)

^d INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CENTROMERE PROTEIN; NUCLEAR PROTEIN; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; HYBRID MALE RESCUE PROTEIN, DROSOPHILA; LHR PROTEIN, DROSOPHILA; TRANSPOSON;

ARTICLE; CENTROMERE; CHROMOSOME SEGREGATION; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; DROSOPHILA SIMULANS; GENE EXPRESSION; HYBRID; HYBRID MALE RESCUE; LETHAL HYBRID RESCUE; LETHALITY; MALE; NONHUMAN; PRIORITY JOURNAL; REPRODUCTIVE ISOLATION; ANIMAL; CELL CULTURE; CELL PROLIFERATION; CLASSIFICATION; DROSOPHILA; ENZYME IMMUNOASSAY; EVOLUTION; FERTILITY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LARVA; LETHAL GENE; MASS SPECTROMETRY; METABOLISM; TRANSPOSON; WESTERN BLOTTING;

DROSOPHILA MELANOGASTER; DROSOPHILA SIMULANS; DROSOPHILIDAE;

ANIMALS; BIOLOGICAL EVOLUTION; BLOTTING, WESTERN; CELL PROLIFERATION; CELLS, CULTURED; CENTROMERE; CHROMOSOME SEGREGATION; DNA TRANSPOSABLE ELEMENTS; DROSOPHILA; DROSOPHILA PROTEINS; FERTILITY; GENE EXPRESSION REGULATION; GENES, LETHAL; IMMUNOENZYME TECHNIQUES; LARVA; MALE; REPRODUCTIVE ISOLATION; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 84888175603     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2013.10.001     Document Type: Article

References (58)

1. Abel J., Eskeland R., Raffa G.D., Kremmer E., Imhof A. Drosophila HP1c is regulated by an auto-regulatory feedback loop through its binding partner Woc. PLoS ONE 2009, 4:e5089.
2. Allshire R.C., Javerzat J.P., Redhead N.J., Cranston G. Position effect variegation at fission yeast centromeres. Cell 1994, 76:157-169.
3. Aruna S., Flores H.A., Barbash D.A. Reduced fertility of Drosophila melanogaster hybrid male rescue (Hmr) mutant females is partiallycomplemented by Hmr orthologs from sibling species. Genetics 2009, 181:1437-1450.
4. Baker B. Genes controlling essential cell-cycle functions in Drosophila melanogaster. Genes Dev. 1989, 3:438-453.
5. Barbash D.A. Genetic testing of the hypothesis that hybrid male lethality results from a failure in dosage compensation. Genetics 2010, 184:313-316.
6. Barbash D.A., Roote J., Ashburner M. The Drosophila melanogaster hybrid male rescue gene causes inviability in male and female species hybrids. Genetics 2000, 154:1747-1771.
7. Barbash D.A., Siino D.F., Tarone A.M., Roote J. A rapidly evolving MYB-related protein causes species isolation in Drosophila. Proc. Natl. Acad. Sci. USA 2003, 100:5302-5307.
8. Bayes J.J., Malik H.S. Altered heterochromatin binding by a hybrid sterility protein in Drosophila sibling species. Science 2009, 326:1538-1541.
9. Bergman C.M., Quesneville H., Anxolabéhère D., Ashburner M. Recurrent insertion and duplication generate networks of transposable element sequences in the Drosophila melanogaster genome. Genome Biol. 2006, 7:R112.
10. Bolkan B.J., Booker R., Goldberg M.L., Barbash D.A. Developmental and cell cycle progression defects in Drosophila hybrid males. Genetics 2007, 177:2233-2241.
11. Brideau N.J., Barbash D.A. Functional conservation of the Drosophila hybrid incompatibility gene Lhr. BMC Evol. Biol. 2011, 11:57.
12. Brideau N.J., Flores H.A., Wang J., Maheshwari S., Wang X., Barbash D.A. Two Dobzhansky-Muller genes interact to cause hybrid lethality in Drosophila. Science 2006, 314:1292-1295.
13. Brown J.D., O'Neill R.J. Chromosomes, conflict, and epigenetics: chromosomal speciation revisited. Annu. Rev. Genomics Hum. Genet. 2010, 11:291-316.
14. Chen E.S., Zhang K., Nicolas E., Cam H.P., Zofall M., Grewal S.I.S. Cell cycle control of centromeric repeat transcription and heterochromatin assembly. Nature 2008, 451:734-737.
15. Chen C.-C., Greene E., Bowers S.R., Mellone B.G. A role for the CAL1-partner Modulo in centromere integrity and accurate chromosome segregation in Drosophila. PLoS ONE 2012, 7:e45094.
16. Crespi B., Nosil P. Conflictual speciation: species formation via genomic conflict. Trends Ecol. Evol. 2013, 28:48-57.
17. Czech B., Malone C.D., Zhou R., Stark A., Schlingeheyde C., Dus M., Perrimon N., Kellis M., Wohlschlegel J.A., Sachidanandam R., et al. An endogenous small interfering RNA pathway in Drosophila. Nature 2008, 453:798-802.
18. Dalal Y., Furuyama T., Vermaak D., Henikoff S. Structure, dynamics, and evolution of centromeric nucleosomes. Proc. Natl. Acad. Sci. USA 2007, 104:15974-15981.
19. Davis A.W., Roote J., Morley T., Sawamura K., Herrmann S., Ashburner M. Rescue of hybrid sterility in crosses between D.melanogaster and D. simulans. Nature 1996, 380:157-159.
20. Dobzhansky T. Genetics and the Origin of Species 1951, Columbia University Press, New York.
21. Fishman L., Saunders A. Centromere-associated female meiotic drive entails male fitness costs in monkeyflowers. Science 2008, 322:1559-1562.
22. Greil F., de Wit E., Bussemaker H.J., van Steensel B. HP1 controls genomic targeting of four novel heterochromatin proteins in Drosophila. EMBO J. 2007, 26:741-751.
23. Hedges D.J., Belancio V.P. Restless genomes humans as a model organism for understanding host-retrotransposable element dynamics. Adv. Genet. 2011, 73:219-262.
24. Heun P., Erhardt S., Blower M.D., Weiss S., Skora A.D., Karpen G.H. Mislocalization of the Drosophila centromere-specific histone CID promotes formation of functional ectopic kinetochores. Dev. Cell 2006, 10:303-315.
25. Hutter P., Ashburner M. Genetic rescue of inviable hybrids between Drosophila melanogaster and its sibling species. Nature 1987, 327:331-333.
26. Hutter P., Roote J., Ashburner M. A genetic basis for the inviability of hybrids between sibling species of Drosophila. Genetics 1990, 124:909-920.
27. Kharchenko P.V., Alekseyenko A.A., Schwartz Y.B., Minoda A., Riddle N.C., Ernst J., Sabo P.J., Larschan E., Gorchakov A.A., Gu T., et al. Comprehensive analysis of the chromatin landscape in Drosophila melanogaster. Nature 2011, 471:480-485.
28. Khurana J.S., Wang J., Xu J., Koppetsch B.S., Thomson T.C., Nowosielska A., Li C., Zamore P.D., Weng Z., Theurkauf W.E. Adaptation toPelement transposon invasion in Drosophila melanogaster. Cell 2011, 147:1551-1563.
29. Kidwell M.G., Kidwell J.F., Sved J.A. Hybrid dysgenesis in Drosophila melanogaster: a syndrome of aberrant traits including mutation, sterility and male recombination. Genetics 1977, 86:813-833.
30. Lerat E., Burlet N., Biémont C., Vieira C. Comparative analysis of transposable elements in the melanogaster subgroup sequenced genomes. Gene 2011, 473:100-109.
31. Long Y., Zhao L., Niu B., Su J., Wu H., Chen Y., Zhang Q., Guo J., Zhuang C., Mei M., et al. Hybrid male sterility in rice controlled by interaction between divergent alleles of two adjacent genes. Proc. Natl. Acad. Sci. USA 2008, 105:18871-18876.
32. Maheshwari S., Barbash D.A. Cis-by-Trans regulatory divergence causes the asymmetric lethal effects of an ancestral hybrid incompatibility gene. PLoS Genet. 2012, 8:e1002597.
33. Maheshwari S., Wang J., Barbash D.A. Recurrent positive selection of the Drosophila hybrid incompatibility gene Hmr. Mol. Biol. Evol. 2008, 25:2421-2430.
34. Malik H.S., Henikoff S. Adaptive evolution of Cid, a centromere-specific histone in Drosophila. Genetics 2001, 157:1293-1298.
35. Malik H.S., Henikoff S. Major evolutionary transitions in centromere complexity. Cell 2009, 138:1067-1082.
36. Mellone B.G., Grive K.J., Shteyn V., Bowers S.R., Oderberg I., Karpen G.H. Assembly of Drosophila centromeric chromatin proteins during mitosis. PLoS Genet. 2011, 7:e1002068.
37. Mihola O., Trachtulec Z., Vlcek C., Schimenti J.C., Forejt J. A mouse speciation gene encodes a meiotic histone H3 methyltransferase. Science 2009, 323:373-375.
38. Olszak A.M., van Essen D., Pereira A.J., Diehl S., Manke T., Maiato H., Saccani S., Heun P. Heterochromatin boundaries are hotspots for de novo kinetochore formation. Nat. Cell Biol. 2011, 13:799-808.
39. Padeken J., Mendiburo M.J., Chlamydas S., Schwarz H.-J., Kremmer E., Heun P. The nucleoplasmin homolog NLP mediates centromere clustering and anchoring to the nucleolus. Mol. Cell 2013, 50:236-249.
40. Pal-Bhadra M., Leibovitch B.A., Gandhi S.G., Chikka M.R., Bhadra U., Birchler J.A., Elgin S.C.R. Heterochromatic silencing and HP1 localization in Drosophila are dependent on the RNAi machinery. Science 2004, 303:669-672.
41. Pardo-Manuel de Villena F., Sapienza C. Female meiosis drives karyotypic evolution in mammals. Genetics 2001, 159:1179-1189.
42. Partridge J.F., Borgstrøm B., Allshire R.C. Distinct protein interaction domains and protein spreading in a complex centromere. Genes Dev. 2000, 14:783-791.
43. Phadnis N., Orr H.A. A single gene causes both male sterility and segregation distortion in Drosophila hybrids. Science 2009, 323:376-379.
44. Pontecorvo G. Viability interactions between chromosomes ofDrosophila melanogaster andDrosophila simulans. J.Genet. 1943, 45:51-66.
45. Rodriguez M.A., Vermaak D., Bayes J.J., Malik H.S. Species-specific positive selection of the male-specific lethal complex that participates in dosage compensation in Drosophila. Proc. Natl. Acad. Sci. USA 2007, 104:15412-15417.
46. Ross B.D., Rosin L., Thomae A.W., Hiatt M.A., Vermaak D., de la Cruz A.F., Imhof A., Mellone B.G., Malik H.S. Stepwise evolution of essential centromere function in a Drosophila neogene. Science 2013, 340:1211-1214.
47. Schartl M. Evolution of Xmrk: an oncogene, but also a speciation gene?. Bioessays 2008, 30:822-832.
48. Scott K.C., Merrett S.L., Willard H.F. A heterochromatin barrier partitions the fission yeast centromere into discrete chromatin domains. Curr. Biol. 2006, 16:119-129.
49. Scott K.C., White C.V., Willard H.F. An RNA polymerase III-dependent heterochromatin barrier at fission yeast centromere 1. PLoS ONE 2007, 2:e1099.
50. Spierer A., Seum C., Delattre M., Spierer P. Loss of the modifiers of variegation Su(var)3-7 or HP1 impacts male X polytene chromosome morphology and dosage compensation. J.Cell Sci. 2005, 118:5047-5057.
51. Spierer A., Begeot F., Spierer P., Delattre M. SU(VAR)3-7 links heterochromatin and dosage compensation in Drosophila. PLoS Genet. 2008, 4:e1000066.
52. Sturtevant A.H. Genetic studies on Drosophila simulans. I. Introduction. Hybrids with Drosophila melanogaster. Genetics 1920, 5:488-500.
53. Sun X., Wahlstrom J., Karpen G. Molecular structure of a functional Drosophila centromere. Cell 1997, 91:1007-1019.
54. Sun X., Le H.D., Wahlstrom J.M., Karpen G.H. Sequence analysis of a functional Drosophila centromere. Genome Res. 2003, 13:182-194.
55. Tang S., Presgraves D.C. Evolution of the Drosophila nuclear pore complex results in multiple hybrid incompatibilities. Science 2009, 323:779-782.
56. Vermaak D., Malik H.S. Multiple roles for heterochromatin protein 1 genes in Drosophila. Annu. Rev. Genet. 2009, 43:467-492.
57. Watanabe T.K. A gene that rescues the lethal hybrids between Drosophila melanogaster and D.simulans. Jpn. J. Genet. 1979, 54:325-331.
58. Yoshioka K., Kanda H., Takamatsu N., Togashi S., Kondo S., Miyake T., Sakaki Y., Shiba T. Efficient amplification of Drosophila simulans copia directed by high-level reverse transcriptase activity associated with copia virus-like particles. Gene 1992, 120:191-196.