One of the greatest challenges in understanding the relationship between genotype and phenotype is to discern how changes in DNA affect the normal functioning of genes. Mutations may generate a new function for a gene, yet it is frequently observed that they inactivate some aspect of a gene’s normal capacity. Investigations focused on understanding the developmental basis for the evolution of anatomical structures has found a prevalent role for mutations that alter developmental gene regulation. In animals, genes are transcriptionally activated in specific tissues during development by regulatory sequences distributed across their expansive non-protein coding regions. Regulatory elements known as silencers act to prevent genes from being expressed in certain tissues, providing a mechanism for precise control. Here, we show how a silencer that prevents expression of a pigment-producing enzyme in certain Drosophila species has repeatedly been subject to inactivating mutations that increased this gene’s expression. This example illustrates how such negative-acting regulatory sequences can represent a convenient target for increasing gene expression through the loss of a genetic element.
Vyšlo v časopise: Genetic Changes to a Transcriptional Silencer Element Confers Phenotypic Diversity within and between Species. PLoS Genet 11(6): e32767. doi:10.1371/journal.pgen.1005279 Kategorie: Research Article prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005279
1. JACOB F, MONOD J (1961) Genetic regulatory mechanisms in the synthesis of proteins. J Mol Biol 3 : 318–356. http://www.ncbi.nlm.nih.gov/pubmed/13718526. Accessed 2 September 2014. 13718526
2. Small S, Levine M (1991) The initiation of pair-rule stripes in the Drosophila blastoderm. Curr Opin Genet Dev 1 : 255–260. http://www.ncbi.nlm.nih.gov/pubmed/1822273. Accessed 18 September 2014. 1822273
3. Gray S, Levine M (1996) Transcriptional repression in development. Curr Opin Cell Biol 8 : 358–364. http://www.ncbi.nlm.nih.gov/pubmed/8743887. Accessed 18 September 2014. 8743887
4. Brand AH, Breeden L, Abraham J, Sternglanz R, Nasmyth K (1985) Characterization of a “silencer” in yeast: a DNA sequence with properties opposite to those of a transcriptional enhancer. Cell 41 : 41–48. http://www.ncbi.nlm.nih.gov/pubmed/3888409. Accessed 18 September 2014. 3888409
5. Carroll SB (2008) Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134 : 25–36. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=18614008. doi: 10.1016/j.cell.2008.06.030 18614008
6. Martin A, Orgogozo V (2013) The loci of repeated evolution: A catalog of genetic hotspots of phenotypic variation. Evolution (N Y) 67 : 1235–1250.
7. Stern DL, Orgogozo V (2008) The loci of evolution: how predictable is genetic evolution? Evolution (N Y) 62 : 2155–2177. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=18616572.
8. Gompel N, Prud’homme B, Wittkopp PJ, Kassner VA, Carroll SB (2005) Chance caught on the wing: cis-regulatory evolution and the origin of pigment patterns in Drosophila. Nature 433 : 481–487. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=15690032. 15690032
9. Chan YF, Marks ME, Jones FC, Villarreal G Jr., Shapiro MD, et al. (2010) Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science (80-) 327 : 302–305. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=20007865.
10. Frankel N, Erezyilmaz DF, McGregor AP, Wang S, Payre F, et al. (2011) Morphological evolution caused by many subtle-effect substitutions in regulatory DNA. Nature 474 : 598–603. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=21720363. doi: 10.1038/nature10200 21720363
11. Reed RD, Papa R, Martin A, Hines HM, Counterman BA, et al. (2011) optix drives the repeated convergent evolution of butterfly wing pattern mimicry. Science 333 : 1137–1141. doi: 10.1126/science.1208227 21778360
12. Studer A, Zhao Q, Ross-Ibarra J, Doebley J (2011) Identification of a functional transposon insertion in the maize domestication gene tb1. Nat Genet 43 : 1160–1163. Available: doi: 10.1038/ng.942 21946354
13. McGregor AP, Orgogozo V, Delon I, Zanet J, Srinivasan DG, et al. (2007) Morphological evolution through multiple cis-regulatory mutations at a single gene. Nature 448 : 587–590. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=17632547. 17632547
14. Frankel N, Davis GK, Vargas D, Wang S, Payre F, et al. (2010) Phenotypic robustness conferred by apparently redundant transcriptional enhancers. Nature 466 : 490–493. doi: 10.1038/nature09158 20512118
15. Williams TM, Selegue JE, Werner T, Gompel N, Kopp A, et al. (2008) The regulation and evolution of a genetic switch controlling sexually dimorphic traits in Drosophila. Cell 134 : 610–623. Available: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=18724934. doi: 10.1016/j.cell.2008.06.052 18724934
16. Jeong S, Rokas A, Carroll SB (2006) Regulation of body pigmentation by the Abdominal-B Hox protein and its gain and loss in Drosophila evolution. Cell 125 : 1387–1399. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=16814723. 16814723
17. Jeong S, Rebeiz M, Andolfatto P, Werner T, True J, et al. (2008) The evolution of gene regulation underlies a morphological difference between two Drosophila sister species. Cell 132 : 783–793. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=18329365. doi: 10.1016/j.cell.2008.01.014 18329365
18. Rebeiz M, Pool JE, Kassner VA, Aquadro CF, Carroll SB (2009) Stepwise modification of a modular enhancer underlies adaptation in a Drosophila population. Science (80-) 326 : 1663–1667. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=20019281.
19. Wittkopp PJ, Vaccaro K, Carroll SB (2002) Evolution of yellow gene regulation and pigmentation in Drosophila. Curr Biol 12 : 1547–1556. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=12372246. 12372246
20. Rogers W a, Salomone JR, Tacy DJ, Camino EM, Davis K a, et al. (2013) Recurrent modification of a conserved cis-regulatory element underlies fruit fly pigmentation diversity. PLoS Genet 9: e1003740. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3757066&tool=pmcentrez&rendertype=abstract. doi: 10.1371/journal.pgen.1003740 24009528
21. Ordway AJ, Hancuch KN, Johnson W, Wiliams TM, Rebeiz M (2014) The expansion of body coloration involves coordinated evolution in cis and trans within the pigmentation regulatory network of Drosophila prostipennis. Dev Biol: 1–10. doi: 10.1016/j.ydbio.2014.05.023
22. Wittkopp PJ, Carroll SB, Kopp A (2003) Evolution in black and white: genetic control of pigment patterns in Drosophila. Trends Genet 19 : 495–504. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=12957543. 12957543
23. Keller I, Alexander JM, Holderegger R, Edwards PJ (2013) Widespread phenotypic and genetic divergence along altitudinal gradients in animals. J Evol Biol 26 : 2527–2543. http://www.ncbi.nlm.nih.gov/pubmed/24128377. Accessed 15 September 2014. doi: 10.1111/jeb.12255 24128377
24. Lee T (1963) Genetic analysis of the polymorphism of color pattern in D. auraria. Drosoph Inf Serv 37 : 97–98.
25. True JR, Yeh S-D, Hovemann BT, Kemme T, Meinertzhagen IA, et al. (2005) Drosophila tan Encodes a Novel Hydrolase Required in Pigmentation and Vision. PLoS Genet 1 : 12. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1285064&tool=pmcentrez&rendertype=abstract.
26. Wright TR (1987) The genetics of biogenic amine metabolism, sclerotization, and melanization in Drosophila melanogaster. Adv Genet 24 : 127–222. Available: http://www.ncbi.nlm.nih.gov/pubmed/3124532. Accessed 3 August 2014. 3124532
27. Hovemann BT, Ryseck RP, Walldorf U, Stortkuhl KF, Dietzel ID, et al. (1998) The Drosophila ebony gene is closely related to microbial peptide synthetases and shows specific cuticle and nervous system expression. Gene 221 : 1–9. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=9852943. 9852943
28. Wittkopp PJ, True JR, Carroll SB (2002) Reciprocal functions of the Drosophila yellow and ebony proteins in the development and evolution of pigment patterns. Development 129 : 1849–1858. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=11934851. 11934851
29. Rebeiz M, Williams TM (2011) Experimental approaches to evaluate the contributions of candidate cis-regulatory mutations to phenotypic evolution. Methods Mol Biol 772 : 351–375. Available: http://www.ncbi.nlm.nih.gov/pubmed/22065449. doi: 10.1007/978-1-61779-228-1_21 22065449
30. Olson M V (1999) When less is more: gene loss as an engine of evolutionary change. Am J Hum Genet 64 : 18–23. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1377697&tool=pmcentrez&rendertype=abstract. Accessed 7 September 2014. 9915938
31. Wittkopp PJ, Stewart EE, Arnold LL, Neidert AH, Haerum BK, et al. (2009) Intraspecific polymorphism to interspecific divergence: genetics of pigmentation in Drosophila. Science 326 : 540–544. http://www.ncbi.nlm.nih.gov/pubmed/19900891. Accessed 30 July 2014. doi: 10.1126/science.1176980 19900891
32. Kopp A, Graze RM, Xu S, Carroll SB, Nuzhdin S V (2003) Quantitative trait loci responsible for variation in sexually dimorphic traits in Drosophila melanogaster. Genetics 163 : 771–787. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=12618413. 12618413
33. Watt WB (1969) ADAPTIVE SIGNIFICANCE OF PIGMENT POLYMORPHISMS IN COLIAS BUTTERFLIES, II. THERMOREGULATION AND PHOTOPERIODICALLY CONTROLLED MELANIN VARIATION IN Colias eurytheme. Proc Natl Acad Sci U S A 63 : 767–774. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=223518&tool=pmcentrez&rendertype=abstract. Accessed 24 September 2014. 16591777
34. Ramniwas S, Kajla B, Dev K, Parkash R (2013) Direct and correlated responses to laboratory selection for body melanisation in Drosophila melanogaster: support for the melanisation-desiccation resistance hypothesis. J Exp Biol 216 : 1244–1254. http://www.ncbi.nlm.nih.gov/pubmed/23239892. Accessed 24 September 2014. doi: 10.1242/jeb.076166 23239892
35. Brisson JA, De Toni DC, Duncan I, Templeton AR (2005) Abdominal pigmentation variation in drosophila polymorpha: geographic variation in the trait, and underlying phylogeography. Evolution 59 : 1046–1059. http://www.ncbi.nlm.nih.gov/pubmed/16136804. Accessed 24 September 2014. 16136804
36. Bastide H, Yassin A, Johanning EJ, Pool JE (2014) Pigmentation in Drosophila melanogaster reaches its maximum in Ethiopia and correlates most strongly with ultra-violet radiation in sub-Saharan Africa. BMC Evol Biol 14 : 179. http://www.ncbi.nlm.nih.gov/pubmed/25115161. Accessed 14 August 2014. doi: 10.1186/s12862-014-0179-y 25115161
37. Wittkopp PJ, Smith-Winberry G, Arnold LL, Thompson EM, Cooley AM, et al. (2011) Local adaptation for body color in Drosophila americana. Heredity (Edinb) 106 : 592–602. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3183901&tool=pmcentrez&rendertype=abstract. Accessed 24 September 2014.
38. Matute DR, Harris A (2013) the Influence of Abdominal Pigmentation on Desiccation and Ultraviolet Resistance in Two Species of Drosophila. Evolution (N Y): n/a–n/a. doi: 10.1111/evo.12122 Accessed 18 May 2013.
39. Parkash R, Rajpurohit S, Ramniwas S (2008) Changes in body melanisation and desiccation resistance in highland vs. lowland populations of D. melanogaster. J Insect Physiol 54 : 1050–1056. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=18519137. doi: 10.1016/j.jinsphys.2008.04.008 18519137
40. Munjal A, Karan D, Gibert P, Moreteau B, Parkash R, et al. (1997) Thoracic trident pigmentation in Drosophila melanogaster: latitudinal and altitudinal clines in Indian populations. Genet Sel Evol 29 : 601–610.
41. Rogers W a, Grover S, Stringer SJ, Parks J, Rebeiz M, et al. (2014) A survey of the trans-regulatory landscape for Drosophila melanogaster abdominal pigmentation. Dev Biol 385 : 417–432. http://www.ncbi.nlm.nih.gov/pubmed/24269556. Accessed 11 January 2014. doi: 10.1016/j.ydbio.2013.11.013 24269556
42. Gompel N, Prud’homme B (2009) The causes of repeated genetic evolution. Dev Biol 332 : 36–47. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=19433086. doi: 10.1016/j.ydbio.2009.04.040 19433086
43. Prud’homme B, Gompel N, Rokas A, Kassner VA, Williams TM, et al. (2006) Repeated morphological evolution through cis-regulatory changes in a pleiotropic gene. Nature 440 : 1050–1053. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=16625197. 16625197
44. Wittkopp PJ, Williams BL, Selegue JE, Carroll SB (2003) Drosophila pigmentation evolution: divergent genotypes underlying convergent phenotypes. Proc Natl Acad Sci U S A 100 : 1808–1813. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=12574518. 12574518
45. Prud’homme B, Gompel N, Carroll SB (2007) Emerging principles of regulatory evolution. Proc Natl Acad Sci U S A 104 Suppl: 8605–8612. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=17494759.
46. Frankel N, Wang S, Stern DL (2012) Conserved regulatory architecture underlies parallel genetic changes and convergent phenotypic evolution. Proc Natl Acad Sci. Available: http://www.pnas.org/content/early/2012/11/28/1207715109.abstract.
47. Laimins L, Holmgren-König M, Khoury G (1986) Transcriptional “silencer” element in rat repetitive sequences associated with the rat insulin 1 gene locus. Proc Natl Acad Sci U S A 83 : 3151–3155. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=323470&tool=pmcentrez&rendertype=abstract. Accessed 29 September 2014. 3010279
48. Udvardy A, Maine E, Schedl P (1985) The 87A7 chromomere. Identification of novel chromatin structures flanking the heat shock locus that may define the boundaries of higher order domains. J Mol Biol 185 : 341–358. http://www.ncbi.nlm.nih.gov/pubmed/2997449. Accessed 29 September 2014. 2997449
49. Burgess-Beusse B, Farrell C, Gaszner M, Litt M, Mutskov V, et al. (2002) The insulation of genes from external enhancers and silencing chromatin. Proc Natl Acad Sci U S A 99 Suppl 4 : 16433–16437. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=12154228. 12154228
50. Akbari OS, Bae E, Johnsen H, Villaluz A, Wong D, et al. (2008) A novel promoter-tethering element regulates enhancer-driven gene expression at the bithorax complex in the Drosophila embryo. Development 135 : 123–131. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=18045839. 18045839
51. Calhoun VC, Stathopoulos A, Levine M (2002) Promoter-proximal tethering elements regulate enhancer-promoter specificity in the Drosophila Antennapedia complex. Proc Natl Acad Sci U S A 99 : 9243–9247. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=12093913. 12093913
52. Frankel N (2012) Multiple layers of complexity in cis-regulatory regions of developmental genes. Dev Dyn 241 : 1857–1866. http://www.ncbi.nlm.nih.gov/pubmed/22972751. Accessed 16 September 2014. doi: 10.1002/dvdy.23871 22972751
53. Barolo S (2011) Shadow enhancers: Frequently asked questions about distributed cis-regulatory information and enhancer redundancy. BioEssays news Rev Mol Cell Dev Biol 34 : 135–141. http://www.ncbi.nlm.nih.gov/pubmed/22083793.
54. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9 : 671–675. http://www.ncbi.nlm.nih.gov/pubmed/22930834. Accessed 17 July 2014. 22930834
55. Bischof J, Maeda RK, Hediger M, Karch F, Basler K (2007) An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc Natl Acad Sci U S A 104 : 3312–3317. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=17360644. 17360644
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