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PMID: 18245821 Published · ppublish English Comparative Study Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S.

Evidence of spatially varying selection acting on four chromatin-remodeling loci in Drosophila melanogaster.

Genetics ·Vol. 179 ·No. 1 ·2008-05-00 ·Pages 475-85

Levine MT, Begun DJ

Abstract

The packaging of DNA into proper chromatin structure contributes to transcriptional regulation. This packaging is environment sensitive, yet its role in adaptation to novel environmental conditions is completely unknown. We set out to identify candidate chromatin-remodeling loci that are differentiated between tropical and temperate populations in Drosophila melanogaster, an ancestrally equatorial African species that has recently colonized temperate environments around the world. Here we describe sequence variation at seven such chromatin-remodeling loci, four of which (chd1, ssrp, chm, and glu) exhibit strong differentiation between tropical and temperate populations. An in-depth analysis of chm revealed sequence differentiation restricted to a small portion of the gene, as well as evidence of clinal variation along the east coasts of both the United States and Australia. The functions of chd1, chm, ssrp, and glu point to several novel hypotheses for the role of chromatin-based transcriptional regulation in adaptation to a novel environment. Specifically, both stress-induced transcription and developmental homeostasis emerge as potential functional targets of environment-dependent selection.

MeSH Terms
Adaptation, Biological/genetics Animals Base Sequence Chromatin Assembly and Disassembly/genetics Drosophila melanogaster/genetics Gene Expression Regulation/genetics Genetic Variation Genetics, Population Geography Linkage Disequilibrium Molecular Sequence Data Selection, Genetic Sequence Analysis, DNA
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Levine Mia T
Center for Population Biology, University of California, Davis, CA 95616, USA. [email protected]
Begun David J
References (80)
80 references, click to expand
  1. Molecular analysis of an allozyme cline: alcohol dehydrogenase in Drosophila melanogaster on the east coast of North America.
    Genetics. 1993 Jul;134(3):869-93 PMID: 8102342
  2. Drosophila chromosome condensation proteins Topoisomerase II and Barren colocalize with Polycomb and maintain Fab-7 PRE silencing.
    Mol Cell. 2001 Jan;7(1):127-36 PMID: 11172718
  3. Common pattern of evolution of gene expression level and protein sequence in Drosophila.
    Mol Biol Evol. 2004 Jul;21(7):1308-17 PMID: 15034135
  4. Haldane's sieve and adaptation from the standing genetic variation.
    Genetics. 2001 Feb;157(2):875-84 PMID: 11157004
  5. Clinal variation for amino acid polymorphisms at the Pgm locus in Drosophila melanogaster.
    Genetics. 2001 Apr;157(4):1649-63 PMID: 11290720
  6. Chromosome Inversion Polymorphisms in DROSOPHILA MELANOGASTER. I. Latitudinal Clines and Associations between Inversions in Australasian Populations.
    Genetics. 1981 Aug;98(4):833-47 PMID: 17249108
  7. The effects of low temperature and aging on nondisjunction in Drosophila.
    Genetics. 1970 May;65(1):75-94 PMID: 5479391
  8. NATURAL VARIATION IN THE EXPRESSION OF THE HEAT-SHOCK PROTEIN HSP70 IN A POPULATION OF DROSOPHILA MELANOGASTER AND ITS CORRELATION WITH TOLERANCE OF ECOLOGICALLY RELEVANT THERMAL STRESS.
    Evolution. 1997 Feb;51(1):173-179 PMID: 28568793
  9. The role of chromatin structure in regulating stress-induced transcription in Saccharomyces cerevisiae.
    Biochem Cell Biol. 2006 Aug;84(4):477-89 PMID: 16936821
  10. A role for Drosophila SMC4 in the resolution of sister chromatids in mitosis.
    Curr Biol. 2001 Mar 6;11(5):295-307 PMID: 11267866
  11. Evolution of cis-regulatory sequence and function in Diptera.
    Heredity (Edinb). 2006 Sep;97(3):139-47 PMID: 16850038
  12. Aspects of low-temperature-induced meiotic nondisjunction in Drosophila females.
    Genetics. 1970 Dec;66(4):653-61 PMID: 5512767
  13. Polyhomeotic stably associates with molecular chaperones Hsc4 and Droj2 in Drosophila Kc1 cells.
    Dev Biol. 2003 Oct 15;262(2):350-60 PMID: 14550797
  14. Adaptive variation in lactate dehydrogenase-B gene expression: role of a stress-responsive regulatory element.
    Proc Natl Acad Sci U S A. 2000 Jun 6;97(12):6597-602 PMID: 10841559
  15. Molecular variation at the In(2L)t proximal breakpoint site in natural populations of Drosophila melanogaster and D. simulans.
    Genetics. 2000 Apr;154(4):1681-91 PMID: 10747062
  16. Evolution of thermotolerance and the heat-shock response: evidence from inter/intraspecific comparison and interspecific hybridization in the virilis species group of Drosophila. I. Thermal phenotype.
    J Exp Biol. 2003 Jul;206(Pt 14):2399-408 PMID: 12796457
  17. Requirement of JNK for stress-induced activation of the cytochrome c-mediated death pathway.
    Science. 2000 May 5;288(5467):870-4 PMID: 10797012
  18. JNK signaling confers tolerance to oxidative stress and extends lifespan in Drosophila.
    Dev Cell. 2003 Nov;5(5):811-6 PMID: 14602080
  19. Reduced natural selection associated with low recombination in Drosophila melanogaster.
    Mol Biol Evol. 1993 Nov;10(6):1239-58 PMID: 8277853
  20. Geographic variation in diapause incidence, life-history traits, and climatic adaptation in Drosophila melanogaster.
    Evolution. 2005 Aug;59(8):1721-32 PMID: 16331839
  21. A heterodimeric coiled-coil protein required for mitotic chromosome condensation in vitro.
    Cell. 1994 Nov 4;79(3):449-58 PMID: 7954811
  22. A gene complex controlling segmentation in Drosophila.
    Nature. 1978 Dec 7;276(5688):565-70 PMID: 103000
  23. Chance caught on the wing: cis-regulatory evolution and the origin of pigment patterns in Drosophila.
    Nature. 2005 Feb 3;433(7025):481-7 PMID: 15690032
  24. Effect of polymorphism in the Drosophila regulatory gene Ultrabithorax on homeotic stability.
    Science. 1996 Jan 12;271(5246):200-3 PMID: 8539619
  25. The MYST domain acetyltransferase Chameau functions in epigenetic mechanisms of transcriptional repression.
    Curr Biol. 2002 Apr 30;12(9):762-6 PMID: 12007422
  26. Epigenetic regulation of cellular memory by the Polycomb and Trithorax group proteins.
    Annu Rev Genet. 2004;38:413-43 PMID: 15568982
  27. Contrasting histories of three gene regions associated with In(3L)Payne of Drosophila melanogaster.
    Genetics. 1996 Dec;144(4):1565-75 PMID: 8978045
  28. Tracking FACT and the RNA polymerase II elongation complex through chromatin in vivo.
    Science. 2003 Aug 22;301(5636):1094-6 PMID: 12934007
  29. DNA sequence variation and latitudinal associations in hsp23, hsp26 and hsp27 from natural populations of Drosophila melanogaster.
    Mol Ecol. 2003 Aug;12(8):2025-32 PMID: 12859626
  30. Variation in gene expression within and among natural populations.
    Nat Genet. 2002 Oct;32(2):261-6 PMID: 12219088
  31. DnaSP, DNA polymorphism analyses by the coalescent and other methods.
    Bioinformatics. 2003 Dec 12;19(18):2496-7 PMID: 14668244
  32. The chromatin-specific transcription elongation factor FACT comprises human SPT16 and SSRP1 proteins.
    Nature. 1999 Jul 15;400(6741):284-8 PMID: 10421373
  33. DESICCATION AND STARVATION TOLERANCE OF ADULT DROSOPHILA: OPPOSITE LATITUDINAL CLINES IN NATURAL POPULATIONS OF THREE DIFFERENT SPECIES.
    Evolution. 1998 Jun;52(3):825-831 PMID: 28565258
  34. Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster.
    Nature. 1992 Apr 9;356(6369):519-20 PMID: 1560824
  35. Evolution of gene expression in the Drosophila melanogaster subgroup.
    Nat Genet. 2003 Feb;33(2):138-44 PMID: 12548287
  36. Patterns of diversity and linkage disequilibrium within the cosmopolitan inversion In(3R)Payne in Drosophila melanogaster are indicative of coadaptation.
    Genetics. 2006 Mar;172(3):1655-63 PMID: 16322502
  37. Effects of temperature stress and pesticide exposure on fluctuating asymmetry and mortality of Copera annulata (Selys) (Odonata: Zygoptera) larvae.
    Ecotoxicol Environ Saf. 2007 May;67(1):120-7 PMID: 16759703
  38. Polycomb silencing mechanisms and the management of genomic programmes.
    Nat Rev Genet. 2007 Jan;8(1):9-22 PMID: 17173055
  39. Evolutionary relationship of DNA sequences in finite populations.
    Genetics. 1983 Oct;105(2):437-60 PMID: 6628982
  40. Natural hyperthermia and expression of the heat shock protein Hsp70 affect developmental abnormalities in Drosophila melanogaster.
    Oecologia. 1999 Nov;121(3):323-329 PMID: 28308320
  41. DNA sequence polymorphism and divergence at the erect wing and suppressor of sable loci of Drosophila melanogaster and D. simulans.
    Genetics. 2005 Jul;170(3):1153-65 PMID: 15944367
  42. polyhomeotic regulatory sequences induce developmental regulator-dependent variegation and targeted P-element insertions in Drosophila.
    Genes Dev. 1993 Aug;7(8):1508-20 PMID: 8101825
  43. Maternal fever and birth outcome: a prospective study.
    Teratology. 1998 Dec;58(6):251-7 PMID: 9894674
  44. Positive selection drives the evolution of rhino, a member of the heterochromatin protein 1 family in Drosophila.
    PLoS Genet. 2005 Jul;1(1):96-108 PMID: 16103923
  45. Domain-wide displacement of histones by activated heat shock factor occurs independently of Swi/Snf and is not correlated with RNA polymerase II density.
    Mol Cell Biol. 2005 Oct;25(20):8985-99 PMID: 16199876
  46. Interchromosomal effects and the relation between crossing-over and nondisjunction.
    Genetics. 1962 Dec;47:1691-709 PMID: 13974320
  47. Levels of variation in stress resistance in drosophila among strains, local populations, and geographic regions: patterns for desiccation, starvation, cold resistance, and associated traits.
    Evolution. 2001 Aug;55(8):1621-30 PMID: 11580021
  48. Evolutionary changes in cis and trans gene regulation.
    Nature. 2004 Jul 1;430(6995):85-8 PMID: 15229602
  49. Rapid evolution of male-biased gene expression in Drosophila.
    Proc Natl Acad Sci U S A. 2003 Aug 19;100(17):9894-9 PMID: 12907700
  50. Distinct activities of CHD1 and ACF in ATP-dependent chromatin assembly.
    Nat Struct Mol Biol. 2005 Feb;12(2):160-6 PMID: 15643425
  51. Modulation of heat shock gene expression by the TAC1 chromatin-modifying complex.
    Nat Cell Biol. 2004 Feb;6(2):162-7 PMID: 14730313
  52. High-resolution localization of Drosophila Spt5 and Spt6 at heat shock genes in vivo: roles in promoter proximal pausing and transcription elongation.
    Genes Dev. 2000 Oct 15;14(20):2635-49 PMID: 11040217
  53. FACT facilitates transcription-dependent nucleosome alteration.
    Science. 2003 Aug 22;301(5636):1090-3 PMID: 12934006
  54. Patterns of puffing activity in the salivary gland chromosomes of Drosophila. V. Responses to environmental treatments.
    Chromosoma. 1970;31(3):356-76 PMID: 5489366
  55. Inversion Clines in Populations of DROSOPHILA MELANOGASTER.
    Genetics. 1977 Sep;87(1):169-76 PMID: 17248756
  56. Drosophila FACT contributes to Hox gene expression through physical and functional interactions with GAGA factor.
    Genes Dev. 2003 Jul 1;17(13):1605-16 PMID: 12815073
  57. African and North American populations of Drosophila melanogaster are very different at the DNA level.
    Nature. 1993 Oct 7;365(6446):548-50 PMID: 8413609
  58. Genomic analysis of adaptive differentiation in Drosophila melanogaster.
    Genetics. 2008 May;179(1):455-73 PMID: 18493064
  59. Genetic variation and relative catalytic efficiencies: lactate dehydrogenase B allozymes of Fundulus heteroclitus.
    Proc Natl Acad Sci U S A. 1979 May;76(5):2354-8 PMID: 36616
  60. Chameau HAT and DRpd3 HDAC function as antagonistic cofactors of JNK/AP-1-dependent transcription during Drosophila metamorphosis.
    Genes Dev. 2006 Jan 1;20(1):101-12 PMID: 16391236
  61. Differential gene regulation by selective association of transcriptional coactivators and bZIP DNA-binding domains.
    Mol Cell Biol. 2006 Aug;26(16):5969-82 PMID: 16880509
  62. CHD1 interacts with SSRP1 and depends on both its chromodomain and its ATPase/helicase-like domain for proper association with chromatin.
    Chromosoma. 1999 Apr;108(1):10-25 PMID: 10199952
  63. CHD1 is concentrated in interbands and puffed regions of Drosophila polytene chromosomes.
    Proc Natl Acad Sci U S A. 1996 Jul 9;93(14):7137-42 PMID: 8692958
  64. JNK extends life span and limits growth by antagonizing cellular and organism-wide responses to insulin signaling.
    Cell. 2005 Apr 8;121(1):115-25 PMID: 15820683
  65. Expression evolution in yeast genes of single-input modules is mainly due to changes in trans-acting factors.
    Genome Res. 2007 Aug;17(8):1161-9 PMID: 17615293
  66. Adaptive genic evolution in the Drosophila genomes.
    Proc Natl Acad Sci U S A. 2007 Feb 13;104(7):2271-6 PMID: 17284599
  67. Quantitative trait symmetry independent of Hsp90 buffering: distinct modes of genetic canalization and developmental stability.
    Proc Natl Acad Sci U S A. 2003 Nov 11;100(23):13396-401 PMID: 14595030
  68. Adaptive evolution of a candidate gene for aging in Drosophila.
    Proc Natl Acad Sci U S A. 2000 Sep 26;97(20):10861-5 PMID: 10995474
  69. GAGA factor and the TFIID complex collaborate in generating an open chromatin structure at the Drosophila melanogaster hsp26 promoter.
    Mol Cell Biol. 2002 Sep;22(17):6148-57 PMID: 12167709
  70. High levels of oxidative stress globally inhibit gene transcription and histone acetylation.
    DNA Cell Biol. 2006 Feb;25(2):124-34 PMID: 16460236
  71. The structure and population genetics of the breakpoints associated with the cosmopolitan chromosomal inversion In(3R)Payne in Drosophila melanogaster.
    Genetics. 2005 Jul;170(3):1143-52 PMID: 15781702
  72. EFFECT OF TEMPERATURE ON EVERSPORTING EYE COLOR IN DROSOPHILA MELANOGASTER.
    Science. 1933 Mar 24;77(1995):312 PMID: 17820329
  73. Single-locus latitudinal clines and their relationship to temperate adaptation in metabolic genes and derived alleles in Drosophila melanogaster.
    Genetics. 2004 Oct;168(2):923-31 PMID: 15514064
  74. Chromosome studies in wild populations of D. melanogaster.
    Genetics. 1976 Feb;82(2):323-47 PMID: 816707
  75. Expression profiling in primates reveals a rapid evolution of human transcription factors.
    Nature. 2006 Mar 9;440(7081):242-5 PMID: 16525476
  76. Remodeling of yeast genome expression in response to environmental changes.
    Mol Biol Cell. 2001 Feb;12(2):323-37 PMID: 11179418
  77. The heat-shock response.
    Annu Rev Biochem. 1986;55:1151-91 PMID: 2427013
  78. Heat shock induced phenocopies of dominant mutants of the bithorax complex in Drosophila melanogaster.
    Mol Gen Genet. 1979 May 4;172(2):161-3 PMID: 113643
  79. Patterns of puffing activity in the salivary gland chromosomes of Drosophila. I. Autosomal puffing patterns in a laboratory stock of Drosophila melanogaster.
    Chromosoma. 1967;21(4):398-428 PMID: 6056758
  80. Recurrent evolution of DNA-binding motifs in the Drosophila centromeric histone.
    Proc Natl Acad Sci U S A. 2002 Feb 5;99(3):1449-54 PMID: 11805302
Article Info
Journal
Genetics
Abbr.
Genetics
ISSN
0016-6731
Published
2008-05-00
Epub
2008-00-03
Pages
475-85
Language
English
Region
United States
NLM ID
0374636
PMCID
PMC2390624
Subset
IM
Grants
NIGMS NIH HHS · R01 GM071926 · United States
NIGMS NIH HHS · GM071926 · United States
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