Regulatory Genes in Ancestral Chordates

Abstract

The phylum ‘Chordate’ includes amphioxus, tunicate and vertebrate. The three groups evolved from a common ancestor. The evolution of chordates is a fascinating subject for biologists, who have long pondered which changes in the genome and genes were critical to the evolution, with no real resolution to this issue. Recent genome projects in the chordates have revealed a repertoire of so‐called regulatory genes, and comparison of these essential genes for development has provided insights into chordate evolution. The ancestral chordate is estimated to have had approximately 80% of the genes in the extant chordate genomes. Some regulatory genes are specific to specific lineages, which may have led to the separation of amphioxus, tunicates and vertebrates.

Key concepts

  • Small subsets of genes encoding transcription factors and signal transductions play roles as conductors during development. These genes are called regulatory genes. Genetic changes in regulatory genes served as major driving forces for the evolution of chordates. The regulatory genes present in the ancestral chordate can be deduced by comparing the extant chordate genomes. This information is crucial to understand the evolution of chordates.

Keywords: amphioxus; tunicate; vertebrate; Ciona intestinalis; evolution

Figure 1.

(a) An adult amphioxus Branchiostoma belcheri. (b) A swimming larva of an ascidian Ciona intestinalis. Ascidian larvae have a notochord in the tail. The anterior part of the central nervous system is developed to form a brain vesicle. The brain vesicle contains two pigmented organs, the otolith and ocellus. (c) An adult Ciona intestinalis. After metamorphosis, ascidians lose their tails and start a sessile lifestyle. (d) A schematic phylogenetic tree of deuterostomes showing the relationships between amphioxus, tunicates and vertebrates.

Figure 2.

Wnt clusters. Wnt clusters found in the human, amphioxus and Drosophila genomes are shown in green, pink and blue, respectively. A box represents a Wnt gene, and the position of the box with respect to the horizontal bar indicates the direction of the transcription. The located chromosome or scaffold numbers are described on the right. DrosophilaDWnt4 is orthologous to Wnt9/14/15, and wg an orthologue of Wnt1.

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References

Adams MD, Celniker SE, Holt RA et al. (2000) The genome sequence of Drosophila melanogaster. Science 287: 2185–2195.

Aparicio S, Chapman J, Stupka E et al. (2002) Whole‐genome shotgun assembly and analysis of the genome of Fugu rubripes. Science 297: 1301–1310.

Bourlat SJ, Juliusdottir T, Lowe CJ et al. (2006) Deuterostome phylogeny reveals monophyletic chordates and the new phylum Xenoturbellida. Nature 444: 85–88.

Cameron CB, Garey JR and Swalla BJ (2000) Evolution of the chordate body plan: New insight from phylogenetic analyses of deuterostome phyla. Proceedings of the National Academy of Sciences of the USA 97: 4469–4474.

Cloney RA (1982) Ascidian larvae and the events of metamorphosis. American Zoologist 22: 817–826.

Conklin EG (1905) Organ forming substances in the eggs of ascidians. Biological Bulletin 8: 205–230.

Dehal P, Satou Y, Campbell RK et al. (2002) The draft genome of Ciona intestinalis: insight into chordate and vertebrate origins. Science 298: 2157–2167.

Delsuc F, Brinkmann H, Chourrout D and Philippe H (2006) Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439: 965–968.

Flood PR, Guthrie DM and Banks JR (1969) Paramyosin muscle in the notochord of amphioxus. Nature 222: 87–88.

Holland LZ, Albalat R, Azumi K et al. (2008) The amphioxus genome illuminates vertebrate origins and cephalochordate biology. Genome Research 18: 1100–1111.

Holland PW, Garcia‐Fernàndez J, Williams NA and Sidow A (1994) Gene duplications and the origins of vertebrate development. Development Supplement 1994: 125–133.

Holt RA, Subramanian GM, Halpern A et al. (2002) The genome sequence of the malaria mosquito Anopheles gambiae. Science 298: 129–149.

Ikuta T, Yoshida N, Satoh N and Saiga H (2004) Ciona intestinalis Hox gene cluster: its dispersed structure and residual colinear expression in development. Proceedings of the National Academy of Sciences of the USA 101: 15118–15123.

Imai KS, Levine M, Satoh N and Satou Y (2006) Regulatory blueprint for a chordate embryo. Science 312: 1183–1187.

Imai KS, Satoh N and Satou Y (2003) A Twist‐like bHLH gene is a downstream facor of an endogenous FGF and determines mesenchymal fate in the ascidian embryos. Development 130: 4461–4472.

Kawakami K (2005) Transposon tools and methods in zebrafish. Developmental Dynamics 234: 244–254.

Koller BH and Smithies O (1989) Inactivating the β2‐microglobulin locus in mouse embryonic stem cells by homologous recombination. Proceedings of the National Academy of Sciences of the USA 86: 8932–8935.

Meng X, Noyes MB, Zhu LJ, Lawson ND and Wolfe SA (2008) Targeted gene inactivation in zebrafish using engineered zinc‐finger nucleases. Nature Biotechnology 26: 695–701.

Nishida H (1992) Regionality of egg cytoplasm that promotes muscle differentiation in embryo of the ascidian, Halocynthia roretzi. Development 116: 521–529.

Nishida H and Sawada K (2001) macho‐1 encodes a localized mRNA in ascidian eggs that specifies muscle fate during embryogenesis. Nature 409: 679–680.

Prodon F, Yamada L, Shirae‐Kurabayashi M, Nakamura Y and Sasakura Y (2007) Postplasmic/PEM RNAs: a class of localized maternal mRNAs with multiple roles in cell polarity and development in ascidian embryos. Developmental Dynamics 236: 1698–1715.

Putnam NH, Butts T, Ferrier DEK et al. (2008) The amphioxus genome and the evolution of the chordate karyotype. Nature 453: 1064–1071.

Sasakura Y, Nakashima K, Awazu S et al. (2005) Transposon‐mediated insertional mutagenesis revealed the functions of animal cellulose synthase in the ascidian Ciona intestinalis. Proceedings of the National Academy of Sciences of the USA 102: 15134–15139.

Sasakura Y, Ogasawara M and Makabe KW (2000) Two pathways of maternal RNA localization at the posterior‐vegetal cytoplasm in early ascidian embryos. Developmental Biology 220: 365–378.

Satou Y, Imai K, Levine M et al. (2003a) A genomewide survey of developmentally relevant genes in Ciona intestinalis. I. Genes for bHLH transcription factors. Development Genes and Evolution 213: 213–221.

Satou Y, Imai KS and Satoh N (2002) Fgf genes in the basal chordate Ciona intestinalis. Development Genes and Evolution 212: 432–438.

Satou Y, Sasakura Y, Yamada L et al. (2003b) A genomewide survey of developmentally relevant genes in Ciona intestinalis. V. Genes for receptor tyrosine kinase pathway and Notch signaling pathway. Development Genes and Evolution 213: 254–263.

Satou Y, Wada S, Sasakura Y and Satoh N (2008) Regulatory genes in the protochordate genome. Development Genes and Evolution 218: 715–721.

Schubert M, Yu J, Holland ND et al. (2005) Retinoic acid signaling acts via Hox1 to establish the posterior limit of the pharynx in the chordate amphioxus. Development 132: 61–73.

Shimeld SM (2008) C2H2 zinc finger genes of the Gli, Zic, KLF, SP, Wilm's tumour, Huckebein, Snail, Ovo, Spalt, Odd, Blimp‐1, Fez, and related gene families from Branchiostoma floridae. Development Genes and Evolution 218: 639–649.

Suzuki MM and Satoh N (2000) Genes expressed in the amphioxus notochord revealed by EST analysis. Developmental Biology 224: 168–177.

Takatori N, Butts T, Candiani S et al. (2008) Comprehensive survey and classification of homeobox genes in the genome of amphioxus, Branchiostoma floridae. Development Genes and Evolution 218: 579–590.

Takatori N and Saiga H (2008) Evolution of CUT class homeobox genes: insights from the genome of the amphioxus, Branchiostoma floridae. International Journal of Developmental Biology 52: 969–977.

Venter JC, Adams MD, Myers EW et al. (2001) The sequence of the human genome. Science 291: 1304–1351.

Wada H, Saiga H, Satoh N and Holland PWH (1998) Tripartite organization of the ancestral chordate brain and the antiquity of placodes: insights from ascidian Pax‐2/5/8, Hox and Otx genes. Development 125: 1113–1122.

Wada H and Satoh N (1994) Details of the evolutionary history from invertebrates to vertebrates, as deduced from the sequences of 18S rDNA. Proceedings of the National Academy of Sciences of the USA 91: 1801–1804.

Wada S, Tokuoka M, Shoguchi E et al. (2003) A genomewide survey of developmentally relevant genes in Ciona intestinalis. II. Genes for homeobox transcription factors. Development Genes and Evolution 213: 222–234.

Yagi K, Satou Y, Mazet F et al. (2003) A genomewide survey of developmentally relevant genes in Ciona intestinalis. III. Genes for Fox, ETS, nuclear receptors and NFκB. Development Genes and Evolution 213: 235–244.

Yamada L (2006) Embryonic expression profiles and conserved localization mechanisms of pem/postplasmic mRNAs of two species of ascidian, Ciona intestinalis and Ciona savignyi. Developmental Biology 296: 524–536.

Yamada L, Kobayashi K, Degnan B, Satoh N and Satou Y (2003) A genomewide survey of developmentally relevant genes in Ciona intestinalis. IV. Genes for HMG transcriptional regulators, bZip and GATA/Gli/Zic/Snail. Development Genes and Evolution 213: 245–253.

Yoshida S, Marikawa Y and Satoh N (1996) Posterior end mark, a novel maternal gene encoding a localized factor in the ascidian embryo. Development 122: 2005–2012.

Yu J, Mazet F, Chen Y et al. (2008) The Fox genes of Branchiostoma floridae. Development Genes and Evolution 218: 629–638.

Further Reading

Carroll SB, Grenier JK and Weatherbee SD (2001) From DNA to diversity. Molecular genetics and the evolution of animal design. Oxford: Blackwell publishing.

Gibson‐Brown JJ and Hartenstein V (2008) The amphioxus genome sequence illuminates the evolutionary origin of vertebrates. Development Genes and Evolution 218: 575–578.

Gilbert SF (2006) Developmental Biology, 8th edn. Sunderland, MA: Sinauer Associates.

Imai KS, Hino K, Yagi K, Satoh N and Satou Y (2004) Gene expression profiles of transcription factors and signaling molecules in the ascidian embryo: towards a comprehensive understanding of gene networks. Development 131: 4047–4058.

Satoh N (1994) Developmental Biology of ascidians. New York: Cambridge University Press.

Satoh N (2003) The ascidian tadpole larva: comparative molecular development and genomics. Nature Reviews. Genetics 4: 285–295.

Satoh N, Kawashima T, Shoguchi E and Satou Y (2006) Urochordate genomes. In: Volff JN (ed.) Vertebrate Genomes, vol. 2, pp. 198–212. Basel: Karger.

Schubert M, Escriva H, Xavier‐Neto J and Laudet V (2006) Amphioxus and tunicates as evolutionary model systems. Trends in Ecology and Evolution 21: 269–277.

Seo HC, Edvardsen RB, Maeland AD et al. (2004) Hox cluster disintegration with persistent anteroposterior order of expression in Oikopleura dioica. Nature 431: 67–71.

Seo HC, Kube M, Edvardsen RB et al. (2001) Miniature genome in the marine chordate Oikopleura dioica. Science 294: 2506.

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How to Cite close
Sasakura, Yasunori(Sep 2009) Regulatory Genes in Ancestral Chordates. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0021774]