Multiple Chromosomal Rearrangements Structured the Ancestral Vertebrate -Bearing Protochromosomes


While the proposal that large-scale genome expansions occurred early in vertebrate evolution is widely accepted, the exact mechanisms of the expansion—such as a single or multiple rounds of whole genome duplication, bloc chromosome duplications, large-scale individual gene duplications, or some combination of these—is unclear. Gene families with a single invertebrate member but four vertebrate members, such as the Hox clusters, provided early support for Ohno's hypothesis that two rounds of genome duplication (the 2R-model) occurred in the stem lineage of extant vertebrates. However, despite extensive study, the duplication history of the Hox clusters has remained unclear, calling into question its usefulness in resolving the role of large-scale gene or genome duplications in early vertebrates. Here, we present a phylogenetic analysis of the vertebrate Hox clusters and several linked genes (the Hox “paralogon”) and show that different phylogenies are obtained for Dlx and Col genes than for Hox and ErbB genes. We show that these results are robust to errors in phylogenetic inference and suggest that these competing phylogenies can be resolved if two chromosomal crossover events occurred in the ancestral vertebrate. These results resolve conflicting data on the order of Hox gene duplications and the role of genome duplication in vertebrate evolution and suggest that a period of genome reorganization occurred after genome duplications in early vertebrates.


Vyšlo v časopise: Multiple Chromosomal Rearrangements Structured the Ancestral Vertebrate -Bearing Protochromosomes. PLoS Genet 5(1): e32767. doi:10.1371/journal.pgen.1000349
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1000349

Souhrn

While the proposal that large-scale genome expansions occurred early in vertebrate evolution is widely accepted, the exact mechanisms of the expansion—such as a single or multiple rounds of whole genome duplication, bloc chromosome duplications, large-scale individual gene duplications, or some combination of these—is unclear. Gene families with a single invertebrate member but four vertebrate members, such as the Hox clusters, provided early support for Ohno's hypothesis that two rounds of genome duplication (the 2R-model) occurred in the stem lineage of extant vertebrates. However, despite extensive study, the duplication history of the Hox clusters has remained unclear, calling into question its usefulness in resolving the role of large-scale gene or genome duplications in early vertebrates. Here, we present a phylogenetic analysis of the vertebrate Hox clusters and several linked genes (the Hox “paralogon”) and show that different phylogenies are obtained for Dlx and Col genes than for Hox and ErbB genes. We show that these results are robust to errors in phylogenetic inference and suggest that these competing phylogenies can be resolved if two chromosomal crossover events occurred in the ancestral vertebrate. These results resolve conflicting data on the order of Hox gene duplications and the role of genome duplication in vertebrate evolution and suggest that a period of genome reorganization occurred after genome duplications in early vertebrates.


Zdroje

1. OhnoS

1970 Evolution by gene duplication Berlin Springer-Verlag

2. LarhammarD

LundinLG

HallbookF

2002 The human Hox-bearing chromosome regions did arise by block or chromosome (or even genome) duplications. Genome Res 12 1910 1920

3. LundinLG

1993 Evolution of the vertebrate genome as reflected in paralogous chromosomal regions in man and the house mouse. Genomics 16 1 19

4. MeyerA

SchartlM

1999 Gene and genome duplications in vertebrates: the one-to-four (-to-eight in fish) rule and the evolution of novel gene functions. Curr Opin Cell Biol 11 699 704

5. SpringJ

1997 Vertebrate evolution by interspecific hybridization—are we polyploid? FEBS Lett 400 2 8

6. WangY

GuX

2000 Evolutionary patterns of gene families generated in the early stage of vertebrates. J Mol Evol 51 88 96

7. DehalP

BooreJL

2005 Two Rounds of Whole Genome Duplication in the Ancestral Vertebrate. PLoS Bio 2 e314

8. GuX

WangY

GuJ

2002 Age distribution of human gene families shows significant roles of both large- and small-scale duplications in vertebrate evolution. Nat Genet 31 205 209

9. GuigoR

MuchnikI

SmithTF

1996 Reconstruction of ancient molecular phylogeny. Mol Phylogenet and Evol 6 189 213

10. McLysaghtA

HokampK

WolfeKH

2002 Extensive genomic duplication during early chordate evolution. Nat Genet 31 200 204

11. FriedmanR

HughesAL

2001 Pattern and timing of gene duplication in animal genomes. Genome Res 11 1842 1847

12. FriedmanR

HughesAL

2003 The temporal distribution of gene duplication events in a set of highly conserved human gene families. Mol Biol and Evol 20 154 161

13. HughesAL

FriedmanR

2003 2R or not 2R: testing hypotheses of genome duplication in early vertebrates. J Struct Funct Genomics 3 85 93

14. HughesAL

1999 Phylogenies of developmentally important proteins do not support the hypothesis of two rounds of genome duplication early in vertebrate history. J Mol Evol 48 565 576

15. HughesAL

1998 Molecular Phylogenetic tests of the hypothesis of block duplication of homologous genes on human chromosomes 6, 9, and 1. Mol Biol and Evol 15 854 870

16. HughesAL

da SilvaJ

FriedmanR

2001 Ancient genome duplications did not structure the human Hox-bearing chromosomes. Genome Res 11 771 780

17. ChowdharyBP

RaudseppT

FrönickeL

SherthanH

1998 Emerging patterns of comparative genome organization in some mammalian species as revealed by zoo-FISH. Genome Res 8 557 589

18. GregorySG

SekhonM

ScheinJ

ZhaoS

OsoegawaK

2002 A physical map of the mouse genome. Nature 418 743 750

19. MurphyWJ

StanyonR

O'BrienSJ

2002 Evolution of mammalian genome organization inferred from comparative gene mapping. Genome Res 2 51 58

20. WagnerGP

AmemiyaC

RuddleF

2003 Hox cluster duplications and the opportunity for evolutionary novelties. Proc Natl Acad Sci U S A 100 14603 14606

21. FurlongR

HollandPW

2002 Were vertebrates octoploid? Philos Trans R Soc Lond B Biol Sci 357 531 544

22. KappenC

RuddleFH

1993 Evolution of a regulatory gene family: HOM/HOX genes. Curr Opin Genet Dev 3 931 938

23. ZhangJ

NeiM

1996 Evolution of Antennapedia-Class Homeobox Genes. Genetics 142 295 303

24. BaileyWJ

KimJ

WagnerGP

RuddleFH

1997 Phylogenetic reconstruction of vertebrate Hox cluster duplications. Mol Biol and Evol 14 843 853

25. StockDW

2005 The Dlx gene complement of the leopard shark, Triakis semifasciata, resembles that of mammals: implications for genomic and morphological evolution of jawed vertebrates. Genetics 169 807 817

26. NeidertAH

VirupannavarV

HookerW

LangelandJA

2001 Lamprey Dlx genes and early vertebrate evolution. Proc Natl Acad Sci U S A 98 1665 1670

27. HolderM

LewisPO

2003 Phylogeny estimation: Traditional and Bayesian approaches. Nat Rev Genet 4 275 284

28. HollandBR

PennyD

HendyMD

2003 Outgroup misplacement and phylogenetic inaccuracy under a molecular clock–a simulation study. Syst Biol 52 229 239

29. BergstenJ

2005 A review of long-branch attraction. Cladistics 21 163 193

30. AnisimovaM

GascuelO

2006 Approximate likelihood-ratio test for branches: A fast, accurate, and powerful alternative. Syst Biol 55 539 552

31. GoldmanN

AndersonJP

RodrigoAG

2000 Likelihodd-based tests of topologies in phylogenetics. Syst Biol 49 652 670

32. ShimodairaH

HasegawaM

2001 CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 17 1246 1247

33. ShimodairaH

2002 An approximately unbiased test of phylogenetic tree selection. Syst Biol 51 492 508

34. KishinoH

HasegawaM

1989 Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in hominoidea. J Mol Evol 29 170 179

35. ShimodairaH

HasegawaM

1999 Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol Biol Evol 16 1114 1116

36. PopoviciC

LeveugleM

BirnbaumD

CoulierF

2001 Homeobox gene clusters and the human paralogy map. FEBS Lett 491 237 242

37. KimJ

1998 Large-scale phylogenies and measuring the performance of phylogenetic estimators. Syst Biol 47 43 69

38. FerrierDE

MinguillonC

HollandPW

Garcia-FernandezJ

2000 The amphioxus Hox cluster: deuterstome posterior flexability and Hox14. Evol Dev 2 284 293

39. van der HoevenF

SordinoP

FraudeauN

Izisua-BelmonteJC

DubouleD

1996 Telesost HoxD and HoxA genes: comparison wiht tetrapods and functional evolution of the HoxD complex. Mech Dev 54 9 21

40. EvansAL

MenaPA

McAllisterBF

2007 Positive selection near an inversion breakpoint on the neo-X chromosome in Drosophila americana. Genetics In Press

41. Marques-BonetT

NavarroA

2005 Chromosomal rearrangements are associated with higher rates of molecular evolution in mammals. Gene 353 147 154

42. LynchV

RothJ

WagnerG

2006 Adaptive evolution of Hox-gene homeodomains after cluster duplications. BMC Evol Biol 6 86

43. MartinA

2001 Is Tetralogy True? Lack of Support for the “One-to-Four Rule”. Mol Biol and Evol 18 89 93

44. CrowKD

StadlerPF

LynchVJ

AmemiyaC

WagnerGP

2006 The “Fish-Specific” Hox Cluster Duplication Is Coincident with the Origin of Teleosts. Mol Biol Evol 23 121 136

45. HuftonAL

GrothD

VingronM

LehrachH

PoustkaAJ

2008 Early vertebrate whole genome duplications were predated by a period of intense genome rearrangement. Genome Res 18 1582 1591

46. NakataniY

TakedaH

KoharaY

MorishitaS

2007 Reconstruction of the vertebrate ancestral genome reveals dynamic genome reorganization in early vertebrates. Genome Res 17 1254 1265

47. PontesO

NevesN

SilvaM

LewisMS

MadlungA

2004 Chromosomal locus rearrangements are a rapid response to formation of the alllotetraplid Aradidopsis suecica genome. Proc Natl Acad Sci U S A 101 18240 18245

48. SémonM

WolfeKH

2007 Consequences of genome duplication. Curr Opin Genet Dev 17 505 512

49. PhillipsR

RábP

2001 Chromosome evolution in the Salmonidae (Pisces): an update. Bio Reivews 76 1 25

50. McVeanGAT

MyersSR

HuntS

DeloukasP

BentleyDR

2004 The fine scale structure of recombination rate variation in the human genome. Science 304 581 584

51. KohnM

HogelJ

VogelW

MinichP

Kehrer-SawatzkiH

2006 Reconstruction of a 450-My-old ancestral vertebrate protokaryotype. Trends Genet 22 203 210

52. EdgarRC

2004 MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32 1792 1797

53. EdgarRC

2004 MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5 e113

54. KeaneT

CreeveyC

PentonyM

NaughtonT

McLnerneyJ

2006 Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified. BMC Evol Biol 6 29

55. GuindonS

GascuelO

2003 A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Sys Biol 52 696 704

56. HuelsenbeckJP

RonquistF

2001 MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17 754 755

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