Segregating variation in the polycomb group gene cramped alters the effect of temperature on multiple traits

PLoS Genetics

Volumn 7, Issue 1, 2011, Pages

  Gibert, Jean Michel ^a   Karch, François ^a   Schlötterer, Christian ^b  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b Institut fur Populationsgenetik   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

CRAMPED PROTEIN; POLYCOMB GROUP PROTEIN; SONIC HEDGEHOG PROTEIN; UNCLASSIFIED DRUG; WNT1 PROTEIN; CRAMPED PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; HEDGEHOG PROTEIN, DROSOPHILA; HOMEODOMAIN PROTEIN; REPRESSOR PROTEIN; TRANSCRIPTION FACTOR; WG PROTEIN, DROSOPHILA;

ARTICLE; CONSTITUTIVE HETEROCHROMATIN; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; ENVIRONMENTAL TEMPERATURE; EVOLUTIONARY ADAPTATION; FEMALE; GENE REGULATORY NETWORK; GENE SEGREGATION; GENE SILENCING; GENE STRUCTURE; GENETIC CONSERVATION; GENETIC HETEROGENEITY; GENETIC TRAIT; GENETIC VARIABILITY; HIGH TEMPERATURE; INSECT GENETICS; LOW TEMPERATURE; MALE; NONHUMAN; PHENOTYPIC PLASTICITY; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE; TEMPERATURE ACCLIMATIZATION; TEMPERATURE SENSITIVITY; ADAPTATION; ANIMAL; EVOLUTION; GENETICS; HETEROCHROMATIN; HISTOLOGY; METABOLISM; PHYSIOLOGY; TEMPERATURE;

DROSOPHILA MELANOGASTER; ERINACEIDAE;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BIOLOGICAL EVOLUTION; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; GENE SILENCING; GENETIC VARIATION; HEDGEHOG PROTEINS; HETEROCHROMATIN; HOMEODOMAIN PROTEINS; MALE; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; TEMPERATURE; TRANSCRIPTION FACTORS; WNT1 PROTEIN;

EID: 79851496149     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1001280     Document Type: Article

References (68)

1. Crickmore MA, Ranade V, Mann RS (2009) Regulation of Ubx expression by epigenetic enhancer silencing in response to Ubx levels and genetic variation. PLoS Genet 5: e1000633 doi:10.1371/journal.pgen.1000633.
2. Meireles-Filho AC, Stark A (2009) Comparative genomics of gene regulation-conservation and divergence of cis-regulatory information. Curr Opin Genet Dev 19: 565-570.
3. Frankel N, Davis GK, Vargas D, Wang S, Payre F, et al. (2010) Phenotypic robustness conferred by apparently redundant transcriptional enhancers. Nature.
4. Perry MW, Boettiger AN, Bothma JP, Levine M (2010) Shadow enhancers foster robustness of Drosophila gastrulation. Curr Biol 20: 1562-1567.
5. Waddington CH (1959) Canalization of development and genetic assimilation of acquired characters. Nature 183: 1654-1655.
6. Grether GF (2005) Environmental change, phenotypic plasticity, and genetic compensation. Am Nat 166: E115-123.
7. Via S, Gomulkievicz R, de Jong G, Scheiner SM, Schlichting CD, et al. (1995) Adaptive phenotypic plasticity: consensus and controversy. TREE 10: 212-217.
8. Suzuki Y, Nijhout HF (2006) Evolution of a polyphenism by genetic accommodation. Science 311: 650-652.
9. Gibson G, Hogness DS (1996) Effect of polymorphism in the Drosophila regulatory gene Ultrabithorax on homeotic stability. Science 271: 200-203.
10. Moczek AP (2007) Developmental capacitance, genetic accommodation, and adaptive evolution. Evol Dev 9: 299-305.
11. Price TD, Qvarnström A, Irwin DE (2003) The role of phenotypic plasticity in driving genetic evolution. Proc R Soc Lond B 270: 1433-1440.
12. West-Eberhard MJ (2005) Developmental plasticity and the origin of species differences. Proc Natl Acad Sci U S A 102 (Suppl 1): 6543-6549.
13. Trotta V, Calboli FCF, Ziosi M, Guerra D, Pezzoli MC, et al. (2006) Thermal plasticity in Drosophila melanogaster: a comparison of geographical population. BMC Evolutionary Biology 6.
14. Bouletreau-Merle J, Fouillet P, Varaldi J (2003) Divergent strategies in low temperature environment for the sibling species Drosophila melanogaster and D. simulans: overwintering in extension borders area of France and comparison with African populations,. Evolutionary Ecology 17: 523-548.
15. Gibert P, Capy P, Imasheva A, Moreteau B, Morin JP, et al. (2004) Comparative analysis of morphological traits among Drosophila melanogaster and D. simulans: genetic variability, clines and phenotypic plasticity. Genetica 120: 165-179.
16. Harr B, Kauer M, Schlotterer C (2002) Hitchhiking mapping: a population-based fine-mapping strategy for adaptive mutations in Drosophilamelanogaster. Proc Natl Acad Sci U S A 99: 12949-12954.
17. Yamamoto Y, Girard F, Bello B, Affolter M, Gehring WJ (1997) The cramped gene of Drosophila is a member of the Polycomb-group, and interacts with mus209, the gene encoding Proliferating Cell Nuclear Antigen. Development 124: 3385-3394.
18. Fauvarque MO, Dura JM (1993) polyhomeotic regulatory sequences induce developmental regulator-dependent variegation and targeted P-element insertions in Drosophila. Genes Dev 7: 1508-1520.
19. Dosztanyi Z, Csizmok V, Tompa P, Simon I (2005) IUPred: web server for the prediction of intrinsically unstructured regions of proteins based on estimated energy content. Bioinformatics 21: 3433-3434.
20. Hegyi H, Schad E, Tompa P (2007) Structural disorder promotes assembly of protein complexes. BMC Struct Biol 7: 65.
21. Mittag T, Kay LE, Forman-Kay JD (2009) Protein dynamics and conformational disorder in molecular recognition. J Mol Recognit.
22. Pattatucci AM, Kaufman TC (1991) The homeotic gene Sex combs reduced of Drosophila melanogaster is differentially regulated in the embryonic and imaginal stages of development. Genetics 129: 443-461.
23. Gibert JM, Peronnet F, Schlotterer C (2007) Phenotypic Plasticity in Drosophila Pigmentation Caused by Temperature Sensitivity of a Chromatin Regulator Network. PLoS Genet 3: e30 doi:10.1371/journal.pgen.0030030.
24. Schotta G, Ebert A, Krauss V, Fischer A, Hoffmann J, et al. (2002) Central role of Drosophila SU(VAR)3-9 in histone H3-K9 methylation and heterochromatic gene silencing. Embo J 21: 1121-1131.
25. Ehsan H, Reichheld JP, Durfee T, Roe JL (2004) TOUSLED kinase activity oscillates during the cell cycle and interacts with chromatin regulators. Plant Physiol 134: 1488-1499.
26. Chanas G, Lavrov S, Iral F, Cavalli G, Maschat F (2004) Engrailed and polyhomeotic maintain posterior cell identity through cubitus-interruptus regulation. Dev Biol 272: 522-535.
27. Ryder E, Blows F, Ashburner M, Bautista-Llacer R, Coulson D, et al. (2004) The DrosDel collection: a set of P-element insertions for generating custom chromosomal aberrations in Drosophila melanogaster. Genetics 167: 797-813.
28. de Wit E, Greil F, van Steensel B (2007) High-resolution mapping reveals links of HP1 with active and inactive chromatin components. PLoS Genet 3: e38 doi:10.1371/journal.pgen.0030038.
29. Dubinin NP, Sidorov BN (1934) Relation between the effect of a gene and its position in the system. Am Naturalist 18: 377-381.
30. Demakova OV, Belyaeva ES, Zhimulev IF (1998) The somatic pairing of homologues of chromosome 4 causes the suppression of the Dubinin effect in Drosophila melanogaster. Russian Journal of Genetics 34: 511-516.
31. Locke J, Tartof KD (1994) Molecular analysis of cubitus interruptus (ci) mutations suggests an explanation for the unusual ci position effects. Mol Gen Genet 243: 234-243.
32. Wallrath LL, Elgin SC (1995) Position effect variegation in Drosophila is associated with an altered chromatin structure. Genes Dev 9: 1263-1277.
33. Minakuchi C, Zhou X, Riddiford LM (2008) Kruppel homolog 1 (Kr-h1) mediates juvenile hormone action during metamorphosis of Drosophila melanogaster. Mech Dev 125: 91-105.
34. Parker DS, Jemison J, Cadigan KM (2002) Pygopus, a nuclear PHD-finger protein required for Wingless signaling in Drosophila. Development 129: 2565-2576.
35. Svendsen PC, Marshall SD, Kyba M, Brook WJ (2000) The combgap locus encodes a zinc-finger protein that regulates cubitus interruptus during limb development in Drosophila melanogaster. Development 127: 4083-4093.
36. Lawrence PA, Casal J, Struhl G (2002) Towards a model of the organisation of planar polarity and pattern in the Drosophila abdomen. Development 129: 2749-2760.
37. Kopp A, Duncan I (1997) Control of cell fate and polarity in the adult abdominal segments of Drosophila by optomotor-blind. Development 124: 3715-3726.
38. Kopp A, Blackman RK, Duncan I (1999) Wingless, decapentaplegic and EGF receptor signaling pathways interact to specify dorso-ventral pattern in the adult abdomen of Drosophila. Development 126: 3495-3507.
39. Scharloo W (1962) The influence of selection and temperature on a mutant character (ciD) in Drosophila melanogaster. Arch Neerl Zool 14: 433-511.
40. Rebeiz M, Pool JE, Kassner VA, Aquadro CF, Carroll SB (2009) Stepwise modification of a modular enhancer underlies adaptation in a Drosophila population. Science 326: 1663-1667.
41. Gibert P, Moreteau B, David JR (2004) Phenotypic plasticity of body pigmentation in Drosophila melanogaster: genetic repeatability of quantitative parameters in two successive generations. Heredity 92: 499-507.
42. Pool JE, Aquadro CF (2007) The genetic basis of adaptive pigmentation variation in Drosophila melanogaster. Mol Ecol 16: 2844-2851.
43. Gibert P, Moreteau B, Moreteau J-C, Parkash R, David JR (1998) Light body pigmentation in Indian Drosophila melanogaster: a likely adaptation to a hot and arid climate. Journal of Genetics 77: 13-20.
44. Caracristi G, Schlotterer C (2003) Genetic differentiation between American and European Drosophila melanogaster populations could be attributed to admixture of African alleles. Mol Biol Evol 20: 792-799.
45. Yukilevich R, True JR (2008) African morphology, behavior and phermones underlie incipient sexual isolation between us and Caribbean Drosophila melanogaster. Evolution 62: 2807-2828.
46. Prud'homme B, Gompel N, Carroll SB (2007) Emerging principles of regulatory evolution. Proc Natl Acad Sci U S A 104 (Suppl 1): 8605-8612.
47. Sawyer SA, Parsch J, Zhang Z, Hartl DL (2007) Prevalence of positive selection among nearly neutral amino acid replacements in Drosophila. Proc Natl Acad Sci U S A 104: 6504-6510.
48. Levine MT, Begun DJ (2008) Evidence of Spatially Varying Selection Acting on Four Chromatin-Remodeling Loci in Drosophila melanogaster. Genetics 179: 475-485.
49. Beisswanger S, Stephan W (2008) Evidence that strong positive selection drives neofunctionalization in the tandemly duplicated polyhomeotic genes in Drosophila. Proc Natl Acad Sci U S A 105: 5447-5452.
50. Kopp A, Graze RM, Xu S, Carroll SB, Nuzhdin SV (2003) Quantitative trait loci responsible for variation in sexually dimorphic traits in Drosophila melanogaster. Genetics 163: 771-787.
51. Kopp A, Barmina O (2005) Evolutionary history of the Drosophila bipectinata species complex. Genet Res 85: 23-46.
52. Kopp A, True JR (2002) Evolution of male sexual characters in the oriental Drosophila melanogaster species group. Evol Dev 4: 278-291.
53. Wittkopp PJ, Carroll SB, Kopp A (2003) Evolution in black and white: genetic control of pigment patterns in Drosophila. Trends Genet 19: 495-504.
54. Rohmer C, David JR, Moreteau B, Joly D (2004) Heat induced male sterility in Drosophila melanogaster: adaptive genetic variations among geographic populations and role of the Y chromosome. J Exp Biol 207: 2735-2743.
55. Ng CS, Kopp A (2008) Sex Combs are Important for Male Mating Success in Drosophila melanogaster. Behav Genet 38: 195-201.
56. Adams MD, Celniker SE, Holt RA, Evans CA, Gocayne JD, et al. (2000) The genome sequence of Drosophila melanogaster. Science 287: 2185-2195.
57. Schmidt HA, Strimmer K, Vingron M, von Haeseler A (2002) TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18: 502-504.
58. Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19: 2496-2497.
59. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
60. Roca AI, Almada AE, Abajian AC (2008) ProfileGrids as a new visual representation of large multiple sequence alignments: a case study of the RecA protein family. BMC Bioinformatics 9: 554.
61. Nagai T, Ibata K, Park ES, Kubota M, Mikoshiba K, et al. (2002) A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat Biotechnol 20: 87-90.
62. Bischof J, Maeda RK, Hediger M, Karch F, Basler K (2007) An optimized transgenesis system for Drosophila using germ-line-specific {varphi}C31 integrases. Proc Natl Acad Sci U S A 104: 3312-3317.
63. Lawrence PA, Casal J, Struhl G (1999) hedgehog and engrailed: pattern formation and polarity in the Drosophila abdomen. Development 126: 2431-2439.
64. Dytham C (2003) Choosing and using statistics: a biologist's guide, 2nd Edition Wiley-Blackwell.
65. Boyer LA, Latek RR, Peterson CL (2004) The SANT domain: a unique histone-tail-binding module? Nat Rev Mol Cell Biol 5: 158-163.
66. Bushey D, Locke J (2004) Mutations in Su(var)205 and Su(var)3-7 suppress P-element-dependent silencing in Drosophila melanogaster. Genetics 168: 1395-1411.
67. Sun FL, Haynes K, Simpson CL, Lee SD, Collins L, et al. (2004) cis-Acting determinants of heterochromatin formation on Drosophila melanogaster chromosome four. Mol Cell Biol 24: 8210-8220.
68. Sun FL, Cuaycong MH, Craig CA, Wallrath LL, Locke J, et al. (2000) The fourth chromosome of Drosophila melanogaster: interspersed euchromatic and heterochromatic domains. Proc Natl Acad Sci U S A 97: 5340-5345.