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Hox-cluster and evolution of morphogeneses

  • Conference Materials on Diversity of Ontogenesis: Morphological, Physiological, and Genetic Aspects (Moscow, November 23–24, 2009)
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Abstract

Comparative studies of genomes of lower Metazoa showed that many classes of transcription factors important for the development of bilateral animals appeared before the divergence of modern branches of the animal kingdom. The genes of the Hox-cluster appeared late, in the last common ancestor of Cnidaria and Bilateria. Structural expansion and perfection of mechanisms which integrate the Hox-cluster can be traced in the morphogenesis of modern bilateral animals. It is now evident that different strategies of using this regulator instrument led Bilateria to absolute domination in number and diversity of species among all Metazoa animals.

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References

  • Abzhanov, A. and Kaufman, T., Novel Regulation of the Homeotic Gene Scr Associated with a Crustacean Leg-to-Maxilliped Appendage Transformation, Development, 1999, vol. 126, pp. 1121–1128.

    CAS  PubMed  Google Scholar 

  • Adamska, M., Degnan, S.M., Green, K.M., et al., Wnt and TGF-Beta Expression in the Sponge Amphimedon quee islandica and the Origin of Metazoan Embryonic Patterning, PLoS ONE, 2007, vol. 2, p. 1031.

    Article  Google Scholar 

  • Alberts, B., Johnson, A., Lewis, J., et al., Molecular Biology of the Cell, New York: Garland Sci, 1392.

  • Amores, A., Suzuki, T., Yan, Y.L., et al., Developmental Roles of Pufferfish Hox Clusters and Genome Evolution in Ray-Fin Fish, Genome Res., 2004, vol. 14, pp. 1–10.

    Article  CAS  PubMed  Google Scholar 

  • Averof, M. and Patel, N., Crustacean Appendage Evolution Associated with Changes in Hox Gene Expression, Nature, 1997, vol. 388, pp. 382–386.

    Google Scholar 

  • Bayascas, J.R., Castillo, E., Muñoz-Mármol, A.M., and Saló, E., Planarian Hox Genes: Novel Patterns of Expression during Regeneration, Development, 1997, vol. 124, pp. 141–148.

    CAS  PubMed  Google Scholar 

  • Belting, H.G., Shashikant, C.S., and Ruddle, F.H., Modification of Expression and Cis-Regulation of Hoxc8 in the Evolution of Diverged Axial Morphology, Proc. Natl. Acad. Sci. USA, 1998, vol. 95, pp. 2355–2360.

    Article  CAS  PubMed  Google Scholar 

  • Burke, A.C., Nelson, C.E., Morgan, B.A., and Tabin, C., Hox Genes and the Evolution of Vertebrate Axial Morphology, Development, 1995, vol. 121, pp. 333–346.

    CAS  PubMed  Google Scholar 

  • Carroll, S.B., Weatherbee, S.D., and Langeland, J.A., Homeotic Genes and the Regulation and Evolution of Insect Wing Number, Nature, 1995, vol. 375, pp. 58–61.

    Article  CAS  PubMed  Google Scholar 

  • Davidson, E.H., Genomic Regulatory Systems, in Development and Evolution, New York: Academic, 2001.

    Google Scholar 

  • De Rosa, R., Grenier, J.K., Andreeva, T., et al., Hox Genes in Brachiodods priapulids Protostome Evolution, Nature, 1999, vol. 399, pp. 772–776.

    Article  CAS  PubMed  Google Scholar 

  • Dehal, P. and Boore, J., Two Rounds of Whole Genome Duplication in the Ancestral Vertebrate, PLoS Biol., 2005, vol. 3, pp. 1700–1708.

    Article  CAS  Google Scholar 

  • Duboule, D., The Rise and Fall of Hox Gene Clusters, Development, 2007, vol. 134, pp. 2549–2560.

    Article  CAS  PubMed  Google Scholar 

  • Edvardsen, R.B., Seo, H.S., Jensen, M.F., et al., Remodelling of the Homeobox Gene Complement in the Tunicate Oikopleura dioica, Curr. Biol., 2000, vol. 15, pp. R12–13.

    Article  Google Scholar 

  • Fröbius, A.C., Matus, D.Q., and Seaver, E.C., Genomic Organization and Expression Demonstrate Spatial and Temporal Hox Gene Colinearity in the Lophotrochozoan Capitella sp. I, PLoS ONE, 2008, vol. 3, pp. 1–17.

    Article  Google Scholar 

  • Erwin, D.H., Early Origin of the Bilaterian Developmental Toolkit, Phil. Trans. R. Soc. B, 2009, vol. 364, pp. 2253–2261.

    Article  CAS  PubMed  Google Scholar 

  • García-Bellido, A., Genetic Control of Wing Disc Development in Drosophila, Cell Patt. Ciba Foundat. Symp., 1975, vol. 29, pp. 161–182.

    Google Scholar 

  • Gilbert, S.F., Biologiya razvitiya (Developmental Biology), Moscow: Mir, 1995, vol. 3.

    Google Scholar 

  • Greer, J., Puetz, J., Thomas, K.R., and Capecchi, M.R., Maintenance of Functional Equivalence during Paralogous Hox Gene Evolution, Nature, 2000, vol. 403, pp. 661–665.

    Article  CAS  PubMed  Google Scholar 

  • Grenier, J. and Carroll, S., Functional Evolution of the Ultrabithorax Protein, Proc. Natl. Acad. Sci. USA, 2000, vol. 97, pp. 704–709.

    Article  CAS  PubMed  Google Scholar 

  • Hanes, S.D. and Brent, R., A Genetic Model for Interaction of the Homeodomain Recognition Helix with DNA, Science, 1991, vol. 251, pp. 426–430.

    Article  CAS  PubMed  Google Scholar 

  • Hinman, V.F., O’Brien, E.K., Richards, G.S., and Degnan, B.M., Expression of Anterior Hox Genes during Larval Development of the Gastropod Haliotis asinine, Evol. Devel., 2003, vol. 5, pp. 508–521.

    Article  CAS  Google Scholar 

  • Ho, M.C., Johnsen, H., Goetz, S.E., et al., Functional Evolution of Cis-Regulatory Modules at a Homeotic Gene in Drosophila, PloS Genet., 2009, vol. 5, pp. 1–16.

    Article  Google Scholar 

  • Holland, P.W.H. and Takahashi, T., The Evolution of Homeobox Genes: Implications for the Study of Brain Development, Brain Res. Bull., 2005, vol. 66, pp. 484–490.

    Article  CAS  PubMed  Google Scholar 

  • Iimura, T. and Pourquie, O., Hox Genes in Time and Space during Vertebrate Body Formation, Devel. Growth Differ., 2007, vol. 49, pp. 265–275.

    Article  CAS  Google Scholar 

  • Ikuta, T., Yoshida, N., Satoh, N., and Saiga, H., Ciona intestinalis Hox Gene Cluster: Its Dispersed Structure Residual Colinear Expression in Development, Proc. Natl. Acad. Sci. USA, 2004, vol. 101, pp. 15118–15123.

    Article  CAS  PubMed  Google Scholar 

  • Irvine, S.Q. and Martindale, M.Q., Expression Patterns of Anterior Hox Genes in the Polychaete Chaetopterus: Correlation with Morphological Boundaries, Devel. Biol., 2000, vol. 217, pp. 333–351.

    Article  CAS  Google Scholar 

  • King, N., Westbrook, M.J., Young, S.L., et al., The Genome of the Choanoflagellate Monosiga brevicollis and the Origin of Metazoans, Nature, 2008, vol. 451, pp. 783–788.

    Article  CAS  PubMed  Google Scholar 

  • Kourakis, M.J. and Martindale, M.Q., Hox Gene Duplication and Deployment in the Annelid Leech Helobdella, Evol. Devel., 2001, vol. 3, pp. 145–153.

    Article  CAS  Google Scholar 

  • Kourakis, M.J., Master, V.A., Lokhorst, D.K., et al., Conserved Anterior Boundaries of Hox Gene Expression in the Central Nervous System of the Leech Helobdella, Devel. Biol., 1997, vol. 190, pp. 284–300.

    Article  CAS  Google Scholar 

  • Kulakova, M., Bakalenko, N., Novikova, E., et al., Hox Gene Expression in Larval Development of the Polychaetes Nereis virens and Platynereis dumerilii (Annelida, Lophotrochozoa), Devel. Genes Evol., 2007, vol. 217, pp. 39–54.

    Article  CAS  Google Scholar 

  • Kulakova, M.A., Kostyuchenko, R.P., Andreeva, T.F., and Dondua, A.K., The Abdominal-B-Like Gene Expression during Larval Development of Nereis virens (Polychaeta), Mech. Devel., 2002, vol. 115, pp. 177–179.

    Article  CAS  Google Scholar 

  • Kuracu, S. and Meyer, A., The Evolution and Maintenance of Hox Gene Clusters in Vertebrates and the Teleost-Specific Genome Duplication, Int. J. Devel. Biol., 2009, vol. 53, pp. 765–773.

    Article  Google Scholar 

  • Kusserow, A., Pang, K., Sturm, C., et al., Unexpected Complexity of the Wnt Gene Family in a Sea Anemone, Nature, 2005, vol. 433, pp. 156–160.

    Article  CAS  PubMed  Google Scholar 

  • Larroux, C., Fahey, B., Liubicich, D., et al., Developmental Expression of Transcription Factor Genes in a Demosponge: Insights into the Origins of Metazoan Multicellularity, Evol. Devel., 2006, vol. 8, pp. 150–173.

    Article  CAS  Google Scholar 

  • Larroux, C., Fahey, B., and Degnan, S.M., The NK Homeobox Gene Cluster Predates the Origin of Hox Genes, Curr. Biol., 2007, vol. 17, pp. 706–710.

    Article  CAS  PubMed  Google Scholar 

  • Lee, P.N., Callaerts, P., De Couet, H.G., and Martindale, M.Q., Cephalopod Hox Genes and the Origin of Morphological Novelties, Nature, 2003, vol. 424, pp. 1061–1065.

    Article  CAS  PubMed  Google Scholar 

  • Liubicich, D.M., Serano, J.M., Pavlopoulos, A., et al., Knockdown of Parhyale Ultrabithorax Recapitulates Evolutionary Changes in Crustacean Appendage Morphology, Proc. Natl. Acad. Sci. USA, 2009, vol. 106, pp. 13892–13896.

    Article  CAS  PubMed  Google Scholar 

  • Malicki, J., Schughart, K., and McGinnis, W., Mouse Hox-2.2 Specifies Thoracic Segmental Identity in Drosophila Embryos and Larvae, Cell, 1990, vol. 63, pp. 961–967.

    Article  CAS  PubMed  Google Scholar 

  • Martindale, M.Q., Pang, K., and Finnerty, J.R., Investigating the Origins of Triploblasty: “Mesodermal” Gene Expression in a Diploblastic Animal, the Sea Anemone Nematostella vectensis (Phylum, Cnidaria, Class, Anthozoa), Development, 2004, vol. 131, pp. 2463–2474.

    Article  CAS  PubMed  Google Scholar 

  • Nardelli-Haefliger, D. and Shankland, M., Lox2, a Putative Leech Segment Identity Gene, is Expressed in the Same Segmental Domain in Different Stem Cell Lineages, Development, 1992, vol. 116, pp. 697–710.

    CAS  PubMed  Google Scholar 

  • Negre, B. and Ruiz, A., HOM-C Evolution in Drosophila: Is There a Need for Hox Gene Clustering, Trends Genet., 2007, vol. 23, pp. 55–59.

    Article  CAS  PubMed  Google Scholar 

  • Nogi, T. and Watanabe, K., Position-Specific and Non-Colinear Expression of the Planarian Posterior (Abdominal-B-Like) Gene, Devel. Growth. Differ., 2001, vol. 43, pp. 117–184.

    Article  Google Scholar 

  • Orii, H., Kato, K., Umesono, Y., et al., The Planarian Hom/Hox Homeobox Genes (Plox) Expressed along the Anteroposterior Axis, Devel. Biol., 1999, vol. 210, pp. 456–468.

    Article  CAS  Google Scholar 

  • Papageorgiou, S., Hox Gene Expression, New York: Springer, 2007.

    Google Scholar 

  • Pavlopoulos, A., Kontarakis, Z., Liubicich, D.M., et al., Probing the Evolution of Appendage Specialization by Hox Gene Misexpression in an Emerging Model Crustacean, Proc. Natl. Acad. Sci. USA, 2009, vol. 106, pp. 13897–13902.

    Article  CAS  PubMed  Google Scholar 

  • Phelan, M.L., Rambaldi, I., and Featherstone, M.S., Cooperative Interactions between HOX and PBX Proteins Mediated by a Conserved Peptide Motif, Mol. Cell. Biol., 1995, vol. 15, pp. 3989–3997.

    CAS  PubMed  Google Scholar 

  • Quiquand, M., Yanze, N., Schmich, J., et al., More Constraint on ParaHox Than Hox Gene Families in Early Metazoan Evolution, Devel. Biol., 2009, vol. 328, pp. 173–187.

    Article  CAS  Google Scholar 

  • Rauskolb, C. and Wieschaus, E., Coordinate Regulation of Downstream Genes Byextradenticle and the Homeotic Selector Proteins, EMBO J., 1994, vol. 13, pp. 3561–3569.

    CAS  PubMed  Google Scholar 

  • Röder, L., Vola, C., and Kerridge, S., The Role of the Teashirt Gene in Trunk Segmental Identity in Drosophila, Development, 1992, vol. 115, pp. 1017–1033.

    PubMed  Google Scholar 

  • Robertson, L.K., Bowling, D.B., Mahaffey, J.P., et al., An Interactive Network of Zinc-Finger Proteins Contributes to Regionalization of the Drosophila Embryo and Establishes the Domains of HOM-C Protein Function, Development, 2004, vol. 131, pp. 2781–2789.

    Article  CAS  PubMed  Google Scholar 

  • Seo, H.C., Edvardsen, R.B., and Maeland, A.D., Hox Cluster Disintegration with Persistent Anteroposterior Order of Expression in Oikopleura dioica, Nature, 2004, vol. 431, pp. 67–71.

    Article  CAS  PubMed  Google Scholar 

  • Shen, W., Rozenfeld, S., Lawrence, H.J., and Largman, C., The Abd-B-Like Hox Homeodomain Proteins can be Subdivided by the Ability to Form Complexes with Pbx1a on a Novel DNA Target, J. Biol. Chem., 1997, vol. 272, pp. 8198–8206.

    Article  CAS  PubMed  Google Scholar 

  • Shippy, T.D., Ronshaugen, M., and Cande, J., Analysis of the Tribolium Homeotic Complex: Insights into Mechanisms Constraining Insect Hox Clusters, Devel. Genes Evol., 2008, vol. 218, pp. 127–139.

    Article  Google Scholar 

  • Slack, J., The Zootype the Phylotypic Stage, Nature, 1993, vol. 361, pp. 490–492.

    Article  CAS  PubMed  Google Scholar 

  • Spitz, F., Gonzalez, F., and Duboule, D., A Global Control Region Defines a Chromosomal Regulatory Landscape Containing the HoxD Cluster, Cell, 2003, vol. 113, pp. 405–417.

    Article  CAS  PubMed  Google Scholar 

  • Srivastava, M., Begovic, E., Chapman, J., et al., The Trichoplax Genome and the Nature of Placozoans, Nature, 2008, vol. 454, pp. 955–960.

    Article  CAS  PubMed  Google Scholar 

  • Stauber, M., Jäckle, H., and Schmidt-Ott, U., The Anterior Determinant Bicoid of Drosophila Is a Derived Hox Class 3 Gene, Devel. Biol., 1999, vol. 96, pp. 3786–3789.

    CAS  Google Scholar 

  • Stern, D., The Hox Gene Ultrabithorax Modulates the Shape and Size of the Third Leg of Drosophila by Influencing Diverse Mechanisms, Devel. Biol., 2003, vol. 256, pp. 355–366.

    Article  CAS  Google Scholar 

  • Tarchini, B. and Duboule, D., Control of Hoxd Genes’ Collinearity during Early Limb Development, Devel. Cell, 2006, vol. 10, pp. 93–103.

    Article  CAS  Google Scholar 

  • Tomoyasu, Y., Arakane, Y., Kramer, K.J., and Denell, R.E., Repeated Co-Options of Exoskeleton Formation during Wing-to-Elytron Evolution in Beetles, Curr. Biol., 2009, vol. 19, pp. 2057–2065.

    Article  CAS  PubMed  Google Scholar 

  • Tschopp, P., Tarchini, B., Spitz, F., et al., Uncoupling Time and Space in the Collinear Regulation of Hox Genes, PLoS Genet., 2009, vol. 5, pp. 1–12.

    Article  Google Scholar 

  • Tvrdik, P. and Capecchi, M., Reversal of Hox1 Gene Subfunctionalization in the Mouse, Devel. Cell, 2006, vol. 11, pp. 239–250.

    Article  CAS  Google Scholar 

  • Wada, S., Tokuoka, M., Shoguchi, E., et al., A Genomewide Survey of Developmentally Relevant Genes in Ciona intestinalis. II. Genes for Homeobox Transcription Factors, Devel. Genes Evol., 2003, vol. 213, pp. 222–234.

    Article  CAS  Google Scholar 

  • Weatherbee, S.D., Nijhout, H.F., and Grunert, L.W., Ultrabithorax Function in Butterfly Wings and the Evolution of Insect Wing Patterns, Curr. Biol., 1999, vol. 9, pp. 109–115.

    Article  CAS  PubMed  Google Scholar 

  • Weisblat, D. and Huang, F., An Overview of Glossiphoniid Leech Development, Can. J. Zool., 2000, vol. 79, pp. 218–232.

    Article  Google Scholar 

  • Wolpert, L., Beddington, R., Brockes, J., et al., Developmental Biology Comes of Age: Principles of Development, Oxford: Univ. Press, 1998.

    Google Scholar 

  • Zhao, J.J., Lazzarini, R.A., and Pick, L., The Mouse Hox-1.3 Gene is Functionally Equivalent to the Drosophila Sex Combs Reduced Gene, Genes Devel., 1993, vol. 7, pp. 343–354.

    Article  CAS  PubMed  Google Scholar 

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Correspondence to N. M. Korchagina.

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Original Russian Text © N.M. Korchagina, N.I. Bakalenko, M.A. Kulakova, 2010, published in Ontogenez, 2010, Vol. 41, No. 5, pp. 353–363.

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Korchagina, N.M., Bakalenko, N.I. & Kulakova, M.A. Hox-cluster and evolution of morphogeneses. Russ J Dev Biol 41, 302–311 (2010). https://doi.org/10.1134/S106236041005005X

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