Genome duplication and the origin of the vertebrate skeleton

Current Opinion in Genetics and Development

Volumn 18, Issue 4, 2008, Pages 387-393

  Zhang, GuangJun ^a   Cohn, Martin J ^a,b  

^a University of Florida   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE; BONE DEVELOPMENT; CARTILAGE; CELL TYPE; DIPLOIDY; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; GENE DUPLICATION; HUMAN; MOLECULAR EVOLUTION; MULTIGENE FAMILY; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; REVIEW; SKELETON; TISSUE DIFFERENTIATION; TISSUE TYPES; VERTEBRATE;

ANIMALS; BONE AND BONES; BONE DEVELOPMENT; EVOLUTION, MOLECULAR; GENE DUPLICATION; GENE EXPRESSION PROFILING; GENOME; HUMANS; MODELS, BIOLOGICAL; PHYLOGENY;

VERTEBRATA;

EID: 53449101955     PISSN: 0959437X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.gde.2008.07.009     Document Type: Review

References (48)

1. Ohno S. Evolution by Gene Duplication (1970), Springer, New York
2. Putnam N.H., Butts T., Ferrier D.E., Furlong R.F., Hellsten U., Kawashima T., Robinson-Rechavi M., Shoguchi E., Terry A., Yu J.K., et al. The amphioxus genome and the evolution of the chordate karyotype. Nature 453 (2008) 1064-1071. This paper reports the draft genome sequence of a lancelet (or amphioxus), and confirms its status as the most basal living chordate. Comparison with vertebrate genomes supports two rounds of whole genome duplication between the origin of chordates and jawed vertebrates.
3. Storchova Z., and Pellman D. From polyploidy to aneuploidy, genome instability and cancer. Nat Rev Mol Cell Biol 5 (2004) 45-54
4. Gallardo M.H., Bickham J.W., Honeycutt R.L., Ojeda R.A., and Kohler N. Discovery of tetraploidy in a mammal. Nature 401 (1999) 341
5. Furlong R.F., and Holland P.W. Were vertebrates octoploid?. Philos Trans R Soc Lond B: Biol Sci 357 (2002) 531-544
6. Gibson T.J., and Spring J. Evidence in favour of ancient octaploidy in the vertebrate genome. Biochem Soc Trans 28 (2000) 259-264
7. Wolfe K.H. Yesterday's polyploids and the mystery of diploidization. Nat Rev Genet 2 (2001) 333-341
8. Eakin G.S., and Behringer R.R. Tetraploid development in the mouse. Dev Dyn 228 (2003) 751-766
9. Otto S.P. The evolutionary consequences of polyploidy. Cell 131 (2007) 452-462. The author provides an excellent review of the mechanisms of polyploidy and consequences of genome duplication through a discussion of short-term and long-term effects on the biology of polyploid organisms.
10. Force A., Lynch M., Pickett F.B., Amores A., Yan Y.L., and Postlethwait J. Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151 (1999) 1531-1545
11. Lynch M., and Conery J.S. The evolutionary fate and consequences of duplicate genes. Science 290 (2000) 1151-1155
12. Escriva H., Manzon L., Youson J., and Laudet V. Analysis of lamprey and hagfish genes reveals a complex history of gene duplications during early vertebrate evolution. Mol Biol Evol 19 (2002) 1440-1450
13. Panopoulou G., and Poustka A.J. Timing and mechanism of ancient vertebrate genome duplications - the adventure of a hypothesis. Trends Genet 21 (2005) 559-567
14. Lynch M. The Origins of Genome Architecture (2007), Sinauer Assocs., Inc., Sunderland, MA. Lynch's book is a contemporary and insightful treatment of evolution by genome duplication. This is the definitive bridge between Ohno's classic book [1] and the latest progress in genome evolution.
15. Kleinjan D.A., Bancewicz R.M., Gautier P., Dahm R., Schonthaler H.B., Damante G., Seawright A., Hever A.M., Yeyati P.L., van Heyningen V., et al. Subfunctionalization of duplicated zebrafish pax6 genes by cis-regulatory divergence. PLoS Genet 4 (2008) e29. By mapping the zebrafish eye mutant sunrise and conducting transgenesis experiments in mice and zebrafish, the authors show that cis-regulatory evolution drove the divergence of pax6a and pax6b.
16. Yan Y.L., Willoughby J., Liu D., Crump J.G., Wilson C., Miller C.T., Singer A., Kimmel C., Westerfield M., and Postlethwait J.H. A pair of Sox: distinct and overlapping functions of zebrafish sox9 co-orthologs in craniofacial and pectoral fin development. Development 132 (2005) 1069-1083
17. Mise T., Iijima M., Inohaya K., Kudo A., and Wada H. Function of Pax1 and Pax9 in the sclerotome of medaka fish. Genesis 46 (2008) 185-192
18. Horton A.C., Mahadevan N.R., Ruvinsky I., and Gibson-Brown J.J. Phylogenetic analyses alone are insufficient to determine whether genome duplication(s) occurred during early vertebrate evolution. J Exp Zoolog B: Mol Dev Evol 299 (2003) 41-53
19. Dehal P., and Boore J.L. Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol 3 (2005) e314
20. Hughes A.L. Phylogenies of developmentally important proteins do not support the hypothesis of two rounds of genome duplication early in vertebrate history. J Mol Evol 48 (1999) 565-576
21. Hughes A.L., da Silva J., and Friedman R. Ancient genome duplications did not structure the human Hox-bearing chromosomes. Genome Res 11 (2001) 771-780
22. Martin A.P. Increasing genomic complexity by gene duplication and the origin of vertebrates. Am Nat 154 (1999) 111-128
23. Amemiya C.T., Prohaska S.J., Hill-Force A., Cook A., Wasserscheid J., Ferrier D.E., Pascual-Anaya J., Garcia-Fernandez J., Dewar K., and Stadler P.F. The amphioxus Hox cluster: characterization, comparative genomics, and evolution. J Exp Zoolog B: Mol Dev Evol 310 (2008) 465-477
24. Venkatesh B., Kirkness E.F., Loh Y.H., Halpern A.L., Lee A.P., Johnson J., Dandona N., Viswanathan L.D., Tay A., Venter J.C., et al. Survey sequencing and comparative analysis of the elephant shark (Callorhinchus milii) genome. PLoS Biol 5 (2007) e101. Using a shotgun-based survey sequencing approach, the authors report that the genome of a shark shares more synteny and sequence similarity with humans than does the zebrafish. Although sharks are more distantly related to humans, unlike teleosts they have not undergone the additional round genome duplication.
25. Crow K.D., Stadler P.F., Lynch V.J., Amemiya C., and Wagner G.P. The "fish-specific" Hox cluster duplication is coincident with the origin of teleosts. Mol Biol Evol 23 (2006) 121-136. A paper surveyed the teleost Hox clusters in bony fishes, and provides us the evidences that all the genome neoteleosts underwent extra round of WGD.
26. Vandepoele K., De Vos W., Taylor J.S., Meyer A., and Van de Peer Y. Major events in the genome evolution of vertebrates: paranome age and size differ considerably between ray-finned fishes and land vertebrates. Proc Natl Acad Sci U S A 101 (2004) 1638-1643
27. Horton R., Wilming L., Rand V., Lovering R.C., Bruford E.A., Khodiyar V.K., Lush M.J., Povey S., Talbot Jr. C.C., Wright M.W., et al. Gene map of the extended human MHC. Nat Rev Genet 5 (2004) 889-899
28. Castro L.F., Furlong R.F., and Holland P.W. An antecedent of the MHC-linked genomic region in amphioxus. Immunogenetics 55 (2004) 782-784
29. Azumi K., De Santis R., De Tomaso A., Rigoutsos I., Yoshizaki F., Pinto M.R., Marino R., Shida K., Ikeda M., Arai M., et al. Genomic analysis of immunity in a Urochordate and the emergence of the vertebrate immune system: "waiting for Godot". Immunogenetics 55 (2003) 570-581
30. McLysaght A., Hokamp K., and Wolfe K.H. Extensive genomic duplication during early chordate evolution. Nat Genet 31 (2002) 200-204
31. Gu X., Wang Y., and Gu J. Age distribution of human gene families shows significant roles of both large- and small-scale duplications in vertebrate evolution. Nat Genet 31 (2002) 205-209
32. Bailey W.J., Kim J., Wagner G.P., and Ruddle F.H. Phylogenetic reconstruction of vertebrate Hox cluster duplications. Mol Biol Evol 14 (1997) 843-853
33. Abbasi A.A., and Grzeschik K.H. An insight into the phylogenetic history of HOX linked gene families in vertebrates. BMC Evol Biol 7 (2007) 239
34. Runnegar B. Collagen gene construction and evolution. J Mol Evol 22 (1985) 141-149
35. Morvan-Dubois G., Le Guellec D., Garrone R., Zylberberg L., and Bonnaud L. Phylogenetic analysis of vertebrate fibrillar collagen locates the position of zebrafish alpha3(I) and suggests an evolutionary link between collagen alpha chains and hox clusters. J Mol Evol 57 (2003) 501-514
36. ••] report that jawless fishes have Col2α1 genes and Collagen II-based cartilage, pushing the origin of the collagenous skeleton back to the common ancestor of all living vertebrates. Additionally, lancelets have a single ancestral fibrillar collagen gene expressed in the notochord. This study shows that expansion of the fibrillar collagen gene family coincided with origin of the vertebrate skeleton.
37. •].
38. Force A., Amores A., and Postlethwait J.H. Hox cluster organization in the jawless vertebrate Petromyzon marinus. J Exp Zool 294 (2002) 30-46
39. Irvine S.Q., Carr J.L., Bailey W.J., Kawasaki K., Shimizu N., Amemiya C.T., and Ruddle F.H. Genomic analysis of Hox clusters in the sea lamprey Petromyzon marinus. J Exp Zool 294 (2002) 47-62
40. Stadler P.F., Fried C., Prohaska S.J., Bailey W.J., Misof B.Y., Ruddle F.H., and Wagner G.P. Evidence for independent Hox gene duplications in the hagfish lineage: a PCR-based gene inventory of Eptatretus stoutii. Mol Phylogenet Evol 32 (2004) 686-694
41. Fried C., Prohaska S.J., and Stadler P.F. Independent Hox-cluster duplications in lampreys. J Exp Zoolog B: Mol Dev Evol 299 (2003) 18-25
42. Furlong R.F., Younger R., Kasahara M., Reinhardt R., Thorndyke M., and Holland P.W. A degenerate ParaHox gene cluster in a degenerate vertebrate. Mol Biol Evol 24 (2007) 2681-2686. To test the 2R hypothesis, the authors characterize the ParaHox cluster in hagfishes, and suggest that the first genome duplication in vertebrates postdated the divergence of hagfishes from the lineage leading to jawed vertebrates.
43. Shimeld S.M., and Holland P.W. Vertebrate innovations. Proc Natl Acad Sci U S A 97 (2000) 4449-4452
44. Cole A.G., and Hall B.K. Cartilage is a metazoan tissue; integrating data from nonvertebrate sources. Acta Zool (Stockholm) 85 (2004) 69-80
45. Stemple D.L. Structure and function of the notochord: an essential organ for chordate development. Development 132 (2005) 2503-2512
46. Wada H., Okuyama M., Satoh N., and Zhang S. Molecular evolution of fibrillar collagen in chordates, with implications for the evolution of vertebrate skeletons and chordate phylogeny. Evol Dev 8 (2006) 370-377. This paper showed the two chordates, asidians and lancelets, fibrillar collagen gene expression patterns and discussed the origin of veretbrate skeletons.
47. Meulemans D., and Bronner-Fraser M. Insights from amphioxus into the evolution of vertebrate cartilage. PLoS ONE 2 (2007) e787
48. Rychel A.L., and Swalla B.J. Development and evolution of chordate cartilage. J Exp Zoolog B: Mol Dev Evol 308 (2007) 325-335. The authors show that SoxE and fibrillar collagen genes are expressed in pharyngeal endoderm of lancelets and hemichordates, adjacent to the acellular cartilage. They raise the possibility that the secretion of acellular matrix by pharyngeal endoderm was the primitive mode of chondrogenesis for deuterostomes, and the gene network was later co-opted by neural crest cells.