Artículo

Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

In this paper, we provide a historical account of the contribution of a single line of research to our current understanding of the structure of cis-regulatory regions and the genetic basis for morphological evolution. We revisit the experiments that shed light on the evolution of larval cuticular patterns within the genus Drosophila and the evolution and structure of the shavenbaby gene. We describe the experiments that led to the discovery that multiple genetic changes in the cis-regulatory region of shavenbaby caused the loss of dorsal cuticular hairs (quaternary trichomes) in first instar larvae of Drosophila sechellia. We also discuss the experiments that showed that the convergent loss of quaternary trichomes in D. sechellia and Drosophila ezoana was generated by parallel genetic changes in orthologous enhancers of shavenbaby. We discuss the observation that multiple shavenbaby enhancers drive overlapping patterns of expression in the embryo and that these apparently redundant enhancers ensure robust shavenbaby expression and trichome morphogenesis under stressful conditions. All together, these data, collected over 13 years, provide a fundamental case study in the fields of gene regulation and morphological evolution, and highlight the importance of prolonged, detailed studies of single genes.

Registro:

Documento: Artículo
Título:The structure and evolution of cisregulatory regions: The shavenbaby story
Autor:Stern, D.L.; Franke, N.
Filiación:Janelia Farm Research Campus, Howard Hughes Medical Institute, 19700 Helix Drive, Ashburn, VA 20147-2408, United States
Departamento de Ecología, Genética y Evolución, IEGEBA-CONICET, Universidad de Buenos Aires, Ciudad Universitaria, Pabellón 2, C1428EHA Buenos Aires, Argentina
Palabras clave:Cis-regulatory evolution; Cis-regulatory structure; Evolution of enhancer function; Morphological change; Shavenbaby gene; cuticle; evolutionary biology; genetic analysis; hair; molecular analysis; morphogenesis; morphology; DNA binding protein; Drosophila protein; ovo protein, Drosophila; transcription factor; animal; cis-regulatory evolution; cis-regulatory structure; Drosophila; evolution of enhancer function; gene expression regulation; genetics; growth, development and aging; metabolism; molecular evolution; morphogenesis; morphological change; prenatal development; regulatory sequence; review; shavenbaby gene; species difference; trichome; cis-regulatory evolution; cis-regulatory structure; evolution of enhancer function; morphological change; shavenbaby gene; Animals; DNA-Binding Proteins; Drosophila; Drosophila Proteins; Evolution, Molecular; Gene Expression Regulation, Developmental; Morphogenesis; Regulatory Sequences, Nucleic Acid; Species Specificity; Transcription Factors; Trichomes
Año:2013
Volumen:368
Número:1632
DOI: http://dx.doi.org/10.1098/rstb.2013.0028
Título revista:Philosophical Transactions of the Royal Society B: Biological Sciences
Título revista abreviado:Philos. Trans. R. Soc. B Biol. Sci.
ISSN:09628436
CODEN:PTRBA
CAS:DNA-Binding Proteins; Drosophila Proteins; Transcription Factors; ovo protein, Drosophila
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_09628436_v368_n1632_p_Stern

Referencias:

  • Averof, M., Akam, M., Hox genes and the diversification of insect and crustacean body plans (1995) Nature, 376, pp. 420-423. , doi:10.1038/376420a0
  • Cohn, M.J., Tickle, C., Developmental basis of limblessness and axial patterning in snakes (1999) Nature, 399, pp. 474-479. , doi:10.1038/20944
  • Warren, R.W., Nagy, L., Selegue, J., Gates, J., Carroll, S., Evolution of homeotic gene regulation and function in flies and butterflies (1994) Nature, 372, pp. 458-461. , doi:10.1038/372458a0
  • Averof, M., Patel, N.H., Crustacean appendage evolution associated with changes in Hox gene expression (1997) Nature, 388, pp. 682-686. , doi:10.1038/41786
  • Stern, D.L., A role of Ultrabithorax in morphological differences between Drosophila species (1998) Nature, 396, pp. 463-466. , doi:10.1038/24863
  • Dickinson, W.J., Tang, Y., Schuske, K., Akam, M., Conservation of molecular prepatterns during the evolution of cuticle morphology in Drosophila larvae (1993) Evolution, 47, pp. 1396-1406. , doi:10.2307/2410155
  • Bokor, P., Dinardo, S., The roles of hedgehog, wingless and lines in patterning the dorsal epidermis in Drosophila (1996) Development, 122, pp. 1083-1092
  • Sucena, E., Stern, D.L., Divergence of larval morphology between Drosophila sechellia and its sibling species caused by cis-regulatory evolution of ovo/shaven-baby (2000) Proc. Natl Acad. Sci. USA, 97, pp. 4530-4534. , doi:10.1073/pnas.97.9.4530
  • Wieschaus, E., Nusslein-Volhard, C., Jurgens, G., Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster (1984) Roux's Arch. Dev. Biol, 193, pp. 296-307. , doi:10.1007/BF00848158
  • Mevel-Ninio, M., Terracol, R., Salles, C., Vincent, A., Payre, F., Ovo, a Drosophila gene required for ovarian development, is specifically expressed in the germline and shares most of its coding sequences with shavenbaby, a gene involved in embryo patterning (1995) Mech. Dev, 49, pp. 83-95. , doi:10.1016/0925-4773(94)00305-7
  • Delon, I., Chanut-Delalande, H., Payre, F., The ovo/ shavenbaby transcription factor specifies actin remodelling during epidermal differentiation in Drosophila (2003) Mech. Dev, 120, pp. 747-758. , doi:10.1016/S0925-4773(03)00081-9
  • Payre, F., Vincent, A., Carreno, S., Ovo/svb integrates wingless and DER pathways to control epidermis differentiation (1999) Nature, 400, pp. 271-275. , doi:10.1038/22330
  • Kondo, T., Plaza, S., Zanet, J., Benrabah, E., Valenti, P., Hashimoto, Y., Kobayashi, S., Kageyama, Y., Small peptides switch the transcriptional activity of shavenbaby during Drosophila embryogenesis (2010) Science, 329, pp. 336-339. , doi:10.1126/science.1188158
  • Pueyo, J.I., Couso, J.P., Tarsal-less peptides control notch signalling through the shavenbaby transcription factor (2011) Dev. Biol, 355, pp. 183-193. , doi:10.1016/j.ydbio.2011.03.033
  • Payre, F., Genetic control of epidermis differentiation in Drosophila (2004) Int. J. Dev. Biol, 48, pp. 207-215. , doi:10.1387/ijdb.15272387
  • Chanut-Delalande, H., Fernandes, I., Roch, F., Payre, F., Plaza, S., Shavenbaby couples patterning to epidermal cell shape control (2006) PLoS Biol, 4, pp. e290. , doi:10.1371/journal.pbio.0040290
  • Fernandes, I., Chanut-Delalande, H., Ferrer, P., Latapie, Y., Waltzer, L., Affolter, M., Payre, F., Plaza, S., Zona pellucida domain proteins remodel the apical compartment for localized cell shape changes (2010) Dev. Cell, 18, pp. 64-76. , doi:10.1016/j.devcel.2009.11.009
  • Stern, D.L., Orgogozo, V., Is genetic evolution predictable? (2009) Science, 323, pp. 746-751. , doi:10.1126/ science.1158997
  • Dai, X., Schonbaum, C., Degenstein, L., Bai, W., Mahowald, A., Fuchs, E., The ovo gene required for cuticle formation and oogenesis in flies is involved in hair formation and spermatogenesis in mice (1998) Genes Dev, 12, pp. 3452-3463. , doi:10.1101/gad.12.21.3452
  • Delon, I., (2003) Etude De La Morphogénèse Au Cours Du Développement Et De L'évolution: Caractérisation Fonctionnelle Du Gène Ovo/shavenbaby Chez La Drosophile, , These de doctorat de la Université de Toulouse, France
  • Frankel, N., Erezyilmaz, D.F., McGregor, A.P., Wang, S., Payre, F., Stern, D.L., Morphological evolution caused by many subtle-effect substitutions in regulatory DNA (2011) Nature, 474, pp. 598-603. , doi:10.1038/nature10200
  • Frankel, N., Davis, G.K., Vargas, D., Wang, S., Payre, F., Stern, D.L., Phenotypic robustness conferred by apparently redundant transcriptional enhancers (2010) Nature, 466, pp. 490-493. , doi:10.1038/nature09158
  • Parks, A.L., Systematic generation of highresolution deletion coverage of the Drosophila melanogaster genome (2004) Nat. Genet, 36, pp. 288-292. , doi:10.1038/ng1312
  • Waddington, C.H., Canalization of development and the inheritance of acquired characters (1942) Nature, 150, pp. 563-565. , doi:10.1038/150563a0
  • Perry, M.W., Boettiger, A.N., Bothma, J.P., Levine, M., Shadow enhancers foster robustness of Drosophila gastrulation (2010) Curr. Biol, 20, pp. 1562-1567. , doi:10.1016/j.cub.2010.07.043
  • Frankel, N., Multiple layers of complexity in cisregulatory regions of developmental genes (2012) Dev. Dyn, 241, pp. 1857-1866. , doi:10.1002/dvdy.23871
  • McGregor, A.P., Orgogozo, V., Delon, I., Zanet, J., Srinivasan, D.G., Payre, F., Stern, D.L., Morphological evolution through multiple cisregulatory mutations at a single gene (2007) Nature, 448, pp. 587-590. , doi:10.1038/nature05988
  • Orr, H.A., Testing natural selection vs. genetic drift in phenotypic evolution using quantitative trait locus data (1998) Genetics, 149, pp. 2099-2104
  • Sucena, E., Delon, I., Jones, I., Payre, F., Stern, D.L., Regulatory evolution of shavenbaby/ovo underlies multiple cases of morphological parallelism (2003) Nature, 424, pp. 935-938. , doi:10.1038/nature01768
  • Frankel, N., Wang, S., Stern, D.L., Conserved regulatory architecture underlies parallel genetic changes and convergent phenotypic evolution (2012) Proc. Natl Acad. Sci. USA, 109, pp. 20975-20979. , doi:10.1073/pnas.1207715109
  • Cande, J., Goltsev, Y., Levine, M.S., Conservation of enhancer location in divergent insects (2009) Proc. Natl Acad. Sci. USA, 106, pp. 14414-14419. , doi:10.1073/pnas.0905754106
  • Hare, E.E., Peterson, B.K., Iyer, V.N., Meier, R., Eisen, M.B., Sepsid even-skipped enhancers are functionally conserved in Drosophila despite lack of sequence conservation (2008) PLoS Genet, 4, pp. e1000106. , doi:10.1371/journal.pgen.1000106
  • Lang, M., Hadzhiev, Y., Siegel, N., Amemiya, C.T., Parada, C., Strahle, U., Becker, M.-B., Meyer, A., Conservation of shh cis-regulatory architecture of the coelacanth is consistent with its ancestral phylogenetic position (2010) EvoDevo, 1, p. 11. , doi:10.1186/2041-9139-1-11
  • Kuhn, D.T.S.M., Ventimiglia, J., Sprey, T.E., Cuticle morphology changes with each larval molt in D. melanogaster (1992) Drosophila Inf. Ser, 71, pp. 218-222
  • Rockman, M.V., The QTN program and the alleles that matter for evolution: All that's gold does not glitter (2012) Evolution, 66, pp. 1-17. , doi:10.1111/j.1558-5646.2011.01486.x
  • Flint, J., Mackay, T.F., Genetic architecture of quantitative traits in mice, flies, and humans (2009) Genome Res, 19, pp. 723-733. , doi:10.1101/gr.086660.108
  • Graze, R.M., Barmina, O., Tufts, D., Naderi, E., Harmon, K.L., Persianinova, M., Nuzhdin, S.V., New candidate genes for sex-comb divergence between Drosophila mauritiana and Drosophila simulans (2007) Genetics, 176, pp. 2561-2576. , doi:10.1534/genetics.106.067686
  • Bradshaw, H.D., Otto, K.G., Frewen, B.E., McKay, J.K., Schemske, D.W., Quantitative trait loci affecting differences in floral morphology between two species of monkeyflower (Mimulus) (1998) Genetics, 149, pp. 367-382
  • Reed, R.D., Optix drives the repeated convergent evolution of butterfly wing pattern mimicry (2011) Science, 333, pp. 1137-1141. , doi:10.1126/science.1208227
  • Stam, L.F., Laurie, C.C., Molecular dissection of a major gene effect on a quantitative trait: The level of alcohol dehydrogenase expression in Drosophila melanogaster (1996) Genetics, 144, pp. 1559-1564
  • Bickel, R.D., Kopp, A., Nuzhdin, S.V., Composite effects of polymorphisms near multiple regulatory elements create a major-effect QTL (2011) PLoS Genet, 7, pp. e1001275. , doi:10.1371/journal.pgen.1001275
  • Loehlin, D.W., Werren, J.H., Evolution of shape by multiple regulatory changes to a growth gene (2012) Science, 335, pp. 943-947. , doi:10.1126/science.1215193
  • Studer, A.J., Doebley, J.F., Do large effect QTL fractionate? A case study at the maize domestication QTL teosinte branched1 (2011) Genetics, 188, pp. 673-681. , doi:10.1534/genetics.111.126508
  • Linnen, C.R., Poh, Y.P., Peterson, B.K., Barrett, R.D., Larson, J.G., Jensen, J.D., Hoekstra, H.E., Adaptive evolution of multiple traits through multiple mutations at a single gene (2013) Science, 339, pp. 1312-1316. , doi:10.1126/science.1233213
  • Marinic, M., Aktas, T., Ruf, S., Spitz, F., An integrated holo-enhancer unit defines tissue and gene specificity of the fgf8 regulatory landscape (2013) Dev. Cell, 24, pp. 530-542. , doi:10.1016/j.devcel.2013.01.025
  • Montavon, T., Soshnikova, N., Mascrez, B., Joye, E., Thevenet, L., Splinter, E., de Laat, W., Duboule, D., A regulatory archipelago controls Hox genes transcription in digits (2011) Cell, 147, pp. 1132-1145. , doi:10.1016/j.cell.2011.10.023
  • Hollenback, S.M., Lyman, S., Cheng, J., Recombineering-based procedure for creating BAC transgene constructs for animals and cell lines (2011) Curr. Protoc. Mol. Biol, 95, pp. 23.14.1-23.14.28. , doi:10.1002/0471142727.mb2314s95
  • Wesolowska, N., Rong, Y.S., Long-range targeted manipulation of the Drosophila genome by sitespecific integration and recombinational resolution (2013) Genetics, 193, pp. 411-419. , doi:10.1534/genetics.112.145631
  • Robert, V.J., Katic, I., Bessereau, J.L., Mos1 transposition as a tool to engineer the Caenorhabditis elegans genome by homologous recombination (2009) Methods, 49, pp. 263-269. , doi:10.1016/j.ymeth.2009.02.013

Citas:

---------- APA ----------
Stern, D.L. & Franke, N. (2013) . The structure and evolution of cisregulatory regions: The shavenbaby story. Philosophical Transactions of the Royal Society B: Biological Sciences, 368(1632).
http://dx.doi.org/10.1098/rstb.2013.0028
---------- CHICAGO ----------
Stern, D.L., Franke, N. "The structure and evolution of cisregulatory regions: The shavenbaby story" . Philosophical Transactions of the Royal Society B: Biological Sciences 368, no. 1632 (2013).
http://dx.doi.org/10.1098/rstb.2013.0028
---------- MLA ----------
Stern, D.L., Franke, N. "The structure and evolution of cisregulatory regions: The shavenbaby story" . Philosophical Transactions of the Royal Society B: Biological Sciences, vol. 368, no. 1632, 2013.
http://dx.doi.org/10.1098/rstb.2013.0028
---------- VANCOUVER ----------
Stern, D.L., Franke, N. The structure and evolution of cisregulatory regions: The shavenbaby story. Philos. Trans. R. Soc. B Biol. Sci. 2013;368(1632).
http://dx.doi.org/10.1098/rstb.2013.0028