Abstract
The loss in some taxa of conserved developmental control genes that are present in the vast majority of animal lineages is an understudied phenomenon. It is likely that in those lineages in which loss has occurred it may be a strong signal of the mode, tempo and direction of developmental evolution and thus identify ways of generating morphological novelties. Intuitively we might expect these novelties to be particularly those associated with morphological simplifications. One striking example of this has occurred within the nematodes. It appears that over half the ancestral bilaterian Hox cluster has been lost from the model organism Caenorhabditis elegans and its closest related species. Studying the Hox gene complement of nematodes across the phylum has shown that many, if not all these losses occurred within the phylum. Other nematode clades only distantly related to C. elegans have additional Hox genes orthologous to those present in the ancestral bilaterian but absent from the model nematode. In some of these cases rapid sequence evolution of the homeodomain itself obscures orthology assignment until comparison is made with sequences from multiple nematode clades with slower evolving Hox genes. Across the phylum the homeodomains of the Hox genes that are present are evolving very rapidly. In one particular case the genomic arrangement of two homeodomains suggests a mechanism for gene loss. Studying the function in nematodes of the Hox genes absent from C. elegans awaits further research and the establishment of new nematode models. However, what we do know about Hox gene functions suggests that the genetic circuits within which Hox genes act have changed significantly within C. elegans and its close relatives.
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References
Akam M. Hox genes: from master genes to micromanagers. Curr Biol 1998; 8(19):R676.
McGinnis W, Levine MS, Hafen E et al. A conserved DNA sequence in homoeotic genes of the Drosophila Antennapedia and bithorax complexes. Nature 1984; 308(5958):428.
Gehring WJ, Hiromi Y. Homeotic genes and the homeobox. Annu Rev Genet 1986; 20:147.
Aboobaker A, Blaxter M. Hox gene evolution in nematodes: novelty conserved. Curr Opin Genet Dev 2003; 13(6):593.
Burglin TR, Ruvkun G. The Caenorhabditis elegans homeobox gene cluster. Curr Opin Genet Dev 1993; 3(4):615.
Bürglin TR, Ruvkun G, Coulson A et al. Nematode homeobox cluster. Nature 1991; 351(6329):703.
The C. elegans Genome Sequencing Consortium, Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 1998; 282(5396):2012.
Aboobaker AA, Blaxter ML. Hox gene loss during dynamic evolution of the nematode cluster. Curr Biol 2003; 13(1):37.
Sommer RJ, Eizinger A, Lee KZ et al. The Pristionchus HOX gene Ppa-lin-39 inhibits programmed cell death to specify the vulva equivalence group and is not required during vulval induction. Development 1998; 125(19):3865.
Jungblut B, Sommer RJ. The Pristionchus pacificus mab-5 gene is involved in the regulation of ventral epidermal cell fates. Curr Biol 1998; 8(13):775.
Grandien K, Sommer RJ. Functional comparison of the nematode Hox gene lin-39 in C. elegans and P. pacificus reveals evolutionary conservation of protein function despite divergence of primary sequences. Genes Dev 2001; 15(16):2161.
Gutierrez A, Knoch L, Witte H et al. Functional specificity of the nematode Hox gene mab-5. Development 2003; 130(5):983.
Streit A, Kohler R, Marty T et al. Conserved regulation of the Caenorhabditis elegans labial/Hox1 gene ceh-13. Dev Biol 2002; 242(2):96.
Van Auken K, Weaver D, Robertson B et al. Roles of the Homothorax/Meis/Prep homolog UNC-62 and the Exd/Pbx homologs CEH-20 and CEH-40 in C. elegans embryogenesis. Development 2002; 129(22):5255.
Sidow A, Thomas WK. A molecular evolutionary framework for eukaryotic model organisms. Current Biology 1994; 4:596.
Salser SJ, Kenyon C, Patterning C. elegans: homeotic cluster genes, cell fates and cell migrations. Trends in Genetics 1994; 10:159.
Wilson R, Ainscough R, Anderson K et al. 2.2 Mb of contiguous nucleotide sequence from chromosome III of C. elegans. Nature 1994; 368:32.
Mushegian AR, Garey JR, Martin J et al. Large-scale taxonomic profiling of eukaryotic model organisms: a comparison of orthologous proteins encoded by the human, fly, nematode and yeast genomes. Genome Res 1998; 8(6):590.
Aguinaldo AM, Turbeville JM, Linford LS et al. Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 1997; 387(6632):489.
Halanych KM, Bacheller JD, Aguinaldo AM et al. Evidence from 18S ribosomal DNA that the lophophorates are protostome animals. Science 1995; 267(5204):1641.
Zheng J, Rogozin IB, Koonin EV et al. Support for the Coelomata clade of animals from a rigorous analysis of the pattern of intron conservation. Mol Biol Evol 2007; 24(11):2583.
Philip GK, Creevey CJ, McInerney JO. The opisthokonta and the ecdysozoa may not be clades: stronger support for the grouping of plant and animal than for animal and fungi and stronger support for the coelomata than ecdysozoa. Mol Biol Evol 2005; 22(5):1175.
Adoutte A, Balavoine G, Lartillot N et al. The new animal phylogeny: reliability and implications. Proc Natl Acad Sci USA 2000; 97(9):4453.
Dunn CW, Hejnol A, Matus DQ et al. Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 2008; 452(7188):745.
Ruvkun G, Hobert O. The taxonomy of developmental control in Caenorhabditis elegans. Science 1998; 282(5396):2033.
de Rosa R, Grenier JK, Andreeva T et al. Hox genes in brachiopods and priapulids and protostome evolution. Nature 1999; 399(6738):772.
Blaxter ML, De Ley P, Garey JR et al. A molecular evolutionary framework for the phylum Nematoda. Nature 1998; 392(6671):71.
Meldal BH, Debenham NJ, De Ley P et al. An improved molecular phylogeny of the Nematoda with special emphasis on marine taxa. Mol Phylogenet Evol 2007; 42(3):622.
Ikuta T, Yoshida N, Satoh N et al. Ciona intestinalis Hox gene cluster: Its dispersed structure and residual colinear expression in development. Proc Natl Acad Sci USA 2004; 101(42):15118.
Seo HC, Edvardsen RB, Maeland AD et al. Hox cluster disintegration with persistent anteroposterior order of expression in Oikopleura dioica. Nature 2004; 431(7004):67.
Edvardsen RB, Seo HC, Jensen MF et al. Remodelling of the homeobox gene complement in the tunicate Oikopleura dioica. Curr Biol 2005; 15(1):R12.
Delattre M, Felix MA. Polymorphism and evolution of vulval precursor cell lineages within two nematode genera, Caenorhabditis and Oscheius. Curr Biol 2001; 11(9):631.
Kiontke K, Barrière A, Kolotuev I et al. Trends, stasis and drift in the evolution of nematode vulva development. Curr Biol 2007; 17(22):1925.
Teng Y, Girard L, Ferreira HB et al. Dissection of cis-regulatory elements in the C. elegans Hox gene egl-5 promoter. Dev Biol 2004; 276(2):476.
Stoyanov CN, Fleischmann M, Suzuki Y et al. Expression of the C. elegans labial orthologue ceh-13 during male tail morphogenesis. Dev Biol 2003; 259(1):137.
Shemer G, Podbilewicz B. LIN-39/Hox triggers cell division and represses EFF-1/fusogen-dependent vulval cell fusion. Genes Dev 2002; 16(24):3136.
Maloof JN, Kenyon C. The Hox gene lin-39 is required during C. elegans vulval induction to select the outcome of Ras signaling. Development 1998; 125(2):181.
Kenyon CJ, Austin J, Costa M et al. The dance of the Hox genes: patterning the anteroposterior body axis of Caenorhabditis elegans. Cold Spring Harb Symp Quant Biol 1997; 62:293.
Salser SJ, Kenyon C. A C. elegans Hox gene switches on, off, on and off again to regulate proliferation, differentiation and morphogenesis. Development 1996; 122(5):1651.
Harris J, Honigberg L, Robinson N et al. Neuronal cell migration in C. elegans: regulation of Hox gene expression and cell position. Development 1996; 122(10):3117.
Cowing D, kenyon C. Correct Hox gene expression established independently of position in Caenorhabditis elegans. Nature 1996; 382:353.
Ferreira HB, Zhang Y, Zhao C et al. Patterning of Caenorhabditis elegans posterior structures by the Abdominal-B homolog, egl-5. Dev Biol 1999; 207(1):215.
Brunschwig K, Wittmann C, Schnabel R et al. Anterior organization of the Caenorhabditis elegans embryo by the labial-like Hox gene ceh-13. Development 1999; 126(7):1537.
Wittmann C, Bossinger O, Goldstein B et al. The expression of the C. elegans labial-like Hox gene ceh-13 during early embryogenesis relies on cell fate and on anteroposterior cell polarity. Development 1997; 124(21):4193.
Van Auken K, Weaver DC, Edgar LG et al. Caenorhabditis elegans embryonic axial patterning requires two recently discovered posterior-group Hox genes. Proc Natl Acad Sci USA 2000; 97(9):4499.
Eisenmann DM, Maloof JN, Simske JS et al. The beta-catenin homolog BAR-1 and LET-60 Ras coordinately regulate the Hox gene lin-39 during Caenorhabditis elegans vulval development. Development 1998; 125(18):3667.
Takács-Vellai K, Vellai T, Chen EB et al. Transcriptional control of Notch signaling by a HOX and a PBX/ EXD protein during vulval development in C. elegans. Dev Biol 2007; 302(2):661.
Arata Y, Kouike H, Zhang Y et al. Wnt signaling and a Hox protein cooperatively regulate psa-3/Meis to determine daughter cell fate after asymmetric cell division in C. elegans. Dev Cell 2006; 11(1):105.
Yang L, Sym M, Kenyon C. The roles of two C. elegans HOX cofactor orthologs in cell migration and vulva development. Development 2005; 132(6):1413.
Liu J, Fire A. Overlapping roles of two Hox genes and the exd ortholog ceh-20 in diversification of the C. elegans postembryonic mesoderm. Development 2000; 127(23):5179.
Maloof JN, Whangbo J, Harris JM et al. A Wnt signaling pathway controls hox gene expression and neuroblast migration in C. elegans. Development 1999; 126(1):37.
Guerry F, Marti CO, Zhang Y et al. The Mi-2 nucleosome-remodeling protein LET-418 is targeted via LIN-1/ ETS to the promoter of lin-39/Hox during vulval development in C. elegans. Dev Biol 2007; 306(2):469.
Zhang H, Smolen GA, Palmer R et al. SUMO modification is required for in vivo Hox gene regulation by the Caenorhabditis elegans Polycomb group protein SOP-2. Nat Genet 2004; 36(5):507.
Zhang H, Azevedo RB, Lints R et al. Global Regulation of Hox Gene Expression in C. elegans by a SAM Domain Protein. Dev Cell 2003; 4(6):903.
Ross JM, Zarkower D. Polycomb Group Regulation of Hox Gene Expression in C. elegans. Dev Cell 2003; 4(6):891.
Haerty W, Artieri C, Khezri N et al. Comparative analysis of function and interaction of transcription factors in nematodes: extensive conservation of orthology coupled to rapid sequence evolution. BMC Genomics 2008; 9:399.
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Aboobaker, A., Blaxter, M. (2010). The Nematode Story: Hox Gene Loss and Rapid Evolution. In: Deutsch, J.S. (eds) Hox Genes. Advances in Experimental Medicine and Biology, vol 689. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-6673-5_7
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