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:

Developmental conservation among related species is a common generalization known as von Baer's third law and implies that early stages of development are the most refractory to change. The "hourglass model" is an alternative view that proposes that middle stages are the most constrained during development. To investigate this issue, we undertook a genomic approach and provide insights into how natural selection operates on genes expressed during the first 24 h of Drosophila ontogeny in the six species of the melanogaster group for which whole genome sequences are available. Having studied the rate of evolution of more than 2,000 developmental genes, our results showed differential selective pressures at different moments of embryogenesis. In many Drosophila species, early zygotic genes evolved slower than maternal genes indicating that mid-embryogenesis is the stage most refractory to evolutionary change. Interestingly, positively selected genes were found in all embryonic stages even during the period with the highest developmental constraint, emphasizing that positive selection and negative selection are not mutually exclusive as it is often mistakenly considered. Among the fastest evolving genes, we identified a network of nucleoporins (Nups) as part of the maternal transcriptome. Specifically, the acceleration of Nups was driven by positive selection only in the more recently diverged species. Because many Nups are involved in hybrid incompatibilities between species of the Drosophila melanogaster subgroup, our results link rapid evolution of early developmental genes with reproductive isolation. In summary, our study revealed that even within functional groups of genes evolving under strong negative selection many positively selected genes could be recognized. Understanding these exceptions to the broad evolutionary conservation of early expressed developmental genes can shed light into relevant processes driving the evolution of species divergence. © The Author(s) 2013. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.

Registro:

Documento: Artículo
Título:Positive selection in nucleoporins challenges constraints on early expressed genes in Drosophila development
Autor:Mensch, J.; Serra, F.; Lavagnino, N.J.; Dopazo, H.; Hasson, E.
Filiación:Departamento de Ecología, Facultad de Ciencias Exactasy Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
Laboratorio de Genómica Evolutiva, Departamento de Genómica y Bioinformática, Centro de Investigación Príncipe Felipe, Valencia, Spain
Structural Genomics Team, Genome Biology Group, Centre Nacional d'Anàlisis Genòmic (CNAG), Barcelona, Spain
Palabras clave:Dosage compensation; Embryonic genes; Hourglass model; Nups; Drosophila protein; nucleoporin; animal; article; developmental gene; Drosophila melanogaster; embryonic genes; gene; gene expression regulation; genetic selection; genetics; hourglass model; molecular evolution; Nups; prenatal development; dosage compensation; embryonic genes; hourglass model; Nups; Animals; Dosage Compensation, Genetic; Drosophila melanogaster; Drosophila Proteins; Evolution, Molecular; Genes, Developmental; Genes, Insect; Nuclear Pore Complex Proteins; Selection, Genetic
Año:2013
Volumen:5
Número:11
Página de inicio:2231
Página de fin:2241
DOI: http://dx.doi.org/10.1093/gbe/evt156
Título revista:Genome Biology and Evolution
Título revista abreviado:Genome Biolog. Evol.
ISSN:17596653
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_17596653_v5_n11_p2231_Mensch

Referencias:

  • Allen, T.D., Cronshaw, J.M., Bagley, S., Kiseleva, E., Goldberg, M.W., The nuclear pore complex: Mediator of translocation between nucleus and cytoplasm (2000) J Cell Sci., 113, pp. 1651-1659
  • Al-Shahrour, F., From genes to functional classes in the study of biological systems (2007) BMC Bioinformatics, 8, p. 114
  • Antonov, A.V., Schmidt, E.E., Dietmann, S., Krestyaninova, M., Hermjakob, H., R spider: A network-based analysis of gene lists by combining signaling and metabolic pathways from Reactome and KEGG databases (2010) Nucleic Acids Res., 38, pp. W78-W83
  • Arbeitman, M.N., Gene expression during the life cycle of Drosophila melanogaster (2002) Science, 297, pp. 2270-2275
  • Artieri, C.G., Haerty, W., Singh, R.S., Ontogeny and phylogeny: Molecular signatures of selection, constraint, and temporal pleiotropy in the development of Drosophila (2009) BMC Biol., 7, p. 42
  • Artieri, C.G., Singh, R.S., Molecular evidence for increased regulatory conservation during metamorphosis, and against deleterious cascading effects of hybrid breakdown in Drosophila (2010) BMC Biol., 8, p. 26
  • Assis, R., Zhou, Q., Bachtrog, D., Sex-biased transcriptome evolution in Drosophila (2012) Genome Biol Evol., 4, pp. 1189-1200
  • Bapteste, E., Charlebois, R.L., MacLeod, D., Brochier, C., The two tempos of nuclear pore complex evolution: Highly adapting proteins in an ancient frozen structure (2005) Genome Biol., 6, pp. R85
  • Barker, M.S., Demuth, J.P., Wade, M.J., Maternal expression relaxes constraint on innovation of the anterior determinant, bicoid (2005) PLoS Genet., 1, pp. e57
  • Benjamini, Y., Hochberg, Y., Controlling the false discovery rate: A practical and powerful approach to multiple testing (1995) J R Stat Soc B Stat Meth., 57, pp. 289-300
  • Bernstein, M., Cline, T.W., Differential effects of Sex-lethal mutations on dosage compensation early in Drosophila development (1994) Genetics, 136, pp. 1051-1061
  • Carroll, S.B., Grenier, J.K., Weatherbee, S.D., From DNA to diversity: Molecular genetics and the evolution of animal design (2001) Singapore: Blackwell Publishing.
  • Casillas, S., Negre, B., Barbadilla, A., Ruiz, A., Fast sequence evolution of Hox and Hox-derived genes in the genus Drosophila (2006) BMC Evol Biol., 6, p. 106
  • Clark, A.G., Evolution of genes and genomes on the Drosophila phylogeny (2007) Nature, 450, pp. 203-218
  • Clark, N.L., Aquadro, C.F., A novel method to detect proteins evolving at correlated rates: Identifying new functional relationships between coevolving proteins (2010) Mol Biol Evol., 27, pp. 1152-1161
  • Coyne, J.A., Orr, H.A., (2004) Speciation., , Sunderland MA: Sinauer Associates
  • Cruickshank, T., Wade, M.J., Microevolutionary support for a developmental hourglass: Gene expression patterns shape sequence variation and divergence in Drosophila (2008) Evol Dev., 10, pp. 583-590
  • Davis, J.C., Brandman, O., Petrov, D.A., Protein evolution in the context of Drosophila development (2005) J Mol Evol., 60, pp. 774-785
  • Devos, D., Simple fold composition and modular architecture of the nuclear pore complex (2006) Proc Natl Acad Sci U S A., 103, pp. 2172-2177
  • Edgar, R.C., MUSCLE: Multiple sequence alignment with high accuracy and high throughput (2004) Nucleic Acids Res., 32, pp. 1792-1797
  • Foe, V.E., Alberts, B.M., Studies of nuclear and cytoplasmic behaviour during the five mitotic cycles that precede gastrulation in Drosophila embryogenesis (1983) J Cell Sci., 61, pp. 31-70
  • Galis, F., Van Dooren, T.J., Metz, J.A., Conservation of the segmented germband stage: Robustness or pleiotropy? (2002) Trends Genet., 18, pp. 504-509
  • Garrigan, D., Genome sequencing reveals complex speciation in the Drosophila simulans clade (2012) Genome Res., 22, pp. 1499-1511
  • Grath, S., Baines, J.F., Parsch, J., Molecular evolution of sex-biased genes in the Drosophila ananassae subgroup (2009) BMC Evol Biol., 9, p. 291
  • Graveley, B.R., The developmental transcriptome of Drosophila melanogaster (2011) Nature, 471, pp. 473-479
  • Hooper, S.D., Identification of tightly regulated groups of genes during Drosophila melanogaster embryogenesis (2007) Mol Syst Biol., 3, p. 72
  • Jaeger, J., Modelling the Drosophila embryo (2009) Mol Biosyst., 5, pp. 1549-1568
  • Kalinka, A.T., Gene expression divergence recapitulates the developmental hourglass model (2010) Nature, 468, pp. 811-814
  • Köhler, A., Hurt, E., Gene regulation by nucleoporins and links to cancer (2010) Mol Cell., 38, pp. 6-15
  • Larracuente, A.M., Evolution of protein-coding genes in Drosophila (2008) Trends Genet., 24, pp. 114-123
  • Lavagnino, N., Serra, F., Arbiza, L., Dopazo, H., Hasson, E., Evolutionary genomics of genes involved in olfactory behavior in the Drosophila melanogaster species group (2012) Evol Bioinform Online., 8, pp. 89-104
  • Manu, Canalization of gene expression in the Drosophila blastoderm by gap gene cross regulation (2009) PLoS Biol., 7 (3), pp. e1000049
  • Manu, Ludwig, M.Z., Kreitman, M., Sex-specific pattern formation during early Drosophila development (2013) Genetics, 194, pp. 163-173
  • Mason, D.A., Goldfarb, D.S., The nuclear transport machinery as a regulator of Drosophila development (2009) Semin Cell Dev Biol., 20, pp. 582-589
  • Meisel, R.P., Towards a more nuanced understanding of the relationship between sex-biased gene expression and rates of protein-coding sequence evolution (2011) Mol Biol Evol., 28, pp. 1893-1900
  • Mendjan, S., Nuclear pore components are involved in the transcriptional regulation of dosage compensation in Drosophila (2006) Mol Cell., 21, pp. 811-823
  • Neumann, N., Lundin, D., Poole, A.M., Comparative genomic evidence for a complete nuclear pore complex in the last eukaryotic common ancestor (2010) PLoS One, 5 (10), pp. e13241
  • Nolte, V., Pandey, R.V., Kofler, R., Schlötterer, C., Genome-wide patterns of natural variation reveal strong selective sweeps and ongoing genomic conflict in Drosophila mauritiana (2013) Genome Res., 23, pp. 99-110
  • Orr, H.A., Does postzygotic isolation result from improper dosage compensation? (1989) Genetics, 122, pp. 891-894
  • Piasecka, B., Lichocki, P., Moretti, S., Bergmann, S., Robinson-Rechavi, M., The hourglass and the early conservation models-co-existing patterns of developmental constraints in vertebrates (2013) PLoS Genet., 9 (4), pp. e1003476
  • Presgraves, D.C., Does genetic conflict drive rapid molecular evolution of nuclear transport genes in Drosophila? (2007) Bioessays, 29, pp. 386-391
  • Presgraves, D.C., Stephan, W., Pervasive adaptive evolution among interactors of the Drosophila hybrid inviability gene, Nup96 (2007) Mol Biol Evol., 24, pp. 306-314
  • Raff, R.A., (1996) The Shape of Life: Genes, Development, and the Evolution of Animal form., , Chicago: The University of Chicago Press
  • 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 (2007) Proc Natl Acad Sci U S A., 104, pp. 15412-15417
  • Roux, J., Robinson-Rechavi, M., Developmental constraints on vertebrate genome evolution (2008) PLoS Genet., 4, pp. e1000311
  • Sawamura, K., Chromatin evolution and molecular drive in speciation (2012) Int J Evol Biol., 2012, pp. 1-9
  • Sawamura, K., Introgression of Drosophila simulans nuclear pore protein 160 in Drosophila melanogaster alone does not cause inviability but does cause female sterility (2010) Genetics, 186, pp. 669-676
  • Schroeder, M.D., Transcriptional control in the segmentation gene network of Drosophila (2004) PLoS Biol., 2 (9), pp. E271
  • Serra, F., Arbiza, L., Dopazo, J., Dopazo, H., Natural selection on functional modules, a genome-wide analysis (2011) PLoS Comput Biol., 7 (3), pp. e1001093
  • Szklarczyk, D., The STRING database in 2011: Functional interaction networks of proteins, globally integrated and scored (2011) Nucleic Acids Res., 39, pp. D561-D568
  • Tang, S., Presgraves, D.C., Evolution of the Drosophila nuclear pore complex results in multiple hybrid incompatibilities (2009) Science, 323, pp. 779-782
  • Tran, E.J., Wente, S.R., Dynamic nuclear pore complexes: Life on the edge (2006) Cell, 125, pp. 1041-1053
  • Ward, J.H., Hierarchical grouping to optimize an objective function (1963) J Am Stat Assoc., 58, pp. 236-244
  • Wilkins, A.S., (2002) The Evolution of Developmental pathways., , China: Sinauer Associates, Inc., Publishers
  • Yanai, I., Genome-wide midrange transcription profiles reveal expression level relationships in human tissue specification (2005) Bioinformatics, 21, pp. 650-659
  • Yang, Z., Adaptive molecular evolution (2003) Handbook of Statistical genetics., , Balding D, Bishop M, Cannings C, editors, New York: John Wiley
  • Yang, Z., PAML 4: Phylogenetic analysis by maximum likelihood (2007) Mol Biol Evol., 24, pp. 1586-1591
  • Zhang, J., Nielsen, R., Yang, Z., Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level (2005) Mol Biol Evol., 22, pp. 2472-2479

Citas:

---------- APA ----------
Mensch, J., Serra, F., Lavagnino, N.J., Dopazo, H. & Hasson, E. (2013) . Positive selection in nucleoporins challenges constraints on early expressed genes in Drosophila development. Genome Biology and Evolution, 5(11), 2231-2241.
http://dx.doi.org/10.1093/gbe/evt156
---------- CHICAGO ----------
Mensch, J., Serra, F., Lavagnino, N.J., Dopazo, H., Hasson, E. "Positive selection in nucleoporins challenges constraints on early expressed genes in Drosophila development" . Genome Biology and Evolution 5, no. 11 (2013) : 2231-2241.
http://dx.doi.org/10.1093/gbe/evt156
---------- MLA ----------
Mensch, J., Serra, F., Lavagnino, N.J., Dopazo, H., Hasson, E. "Positive selection in nucleoporins challenges constraints on early expressed genes in Drosophila development" . Genome Biology and Evolution, vol. 5, no. 11, 2013, pp. 2231-2241.
http://dx.doi.org/10.1093/gbe/evt156
---------- VANCOUVER ----------
Mensch, J., Serra, F., Lavagnino, N.J., Dopazo, H., Hasson, E. Positive selection in nucleoporins challenges constraints on early expressed genes in Drosophila development. Genome Biolog. Evol. 2013;5(11):2231-2241.
http://dx.doi.org/10.1093/gbe/evt156