Evolutionary genomics and adaptive evolution of the hedgehog gene family (Shh, Ihh and Dhh) in vertebrates

PLoS ONE

Volumn 9, Issue 12, 2014, Pages

  Pereira, Joana ^a,i   Johnson, Warren E ^b   O'Brien, Stephen J ^c,d   Jarvis, Erich D ^e   Zhang, Guojie ^f   Gilbert, M Thomas P ^g   Vasconcelos, Vitor ^a,h   Antunes, Agostinho ^a,h  

^a UNIVERSITY OF PORTO   (Portugal)

^b SMITHSONIAN CONSERVATION BIOLOGY INSTITUTE   (United States)

^c ST PETERSBURG STATE UNIVERSITY   (Russian Federation)

^d NOVA SOUTHEASTERN UNIVERSITY   (United States)

^e DUKE UNIVERSITY MEDICAL CENTER   (United States)

^f BGI SHENZHEN   (China)

^g UNIVERSITY OF COPENHAGEN   (Denmark)

^h UNIVERSITY OF PORTO   (Portugal)

ⁱ EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

SONIC HEDGEHOG PROTEIN;

ARTICLE; BINDING SITE; BIRD; CONTROLLED STUDY; ENZYME ACTIVE SITE; EVOLUTIONARY ADAPTATION; EVOLUTIONARY RATE; GENE DUPLICATION; GENE SEQUENCE; GENETIC LINKAGE; GENOMICS; INVERTEBRATE; MOLECULAR EVOLUTION; MULTIGENE FAMILY; NONHUMAN; ORTHOLOGY; PARALOGY; REPTILE; SEQUENCE HOMOLOGY; SYNTENY; VERTEBRATE; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; PHYLOGENY; POULTRY; PROCEDURES; PROTEIN TERTIARY STRUCTURE;

AVES; ERINACEIDAE; INVERTEBRATA; REPTILIA; VERTEBRATA;

ANIMALS; BINDING SITES; EVOLUTION, MOLECULAR; GENE DUPLICATION; GENOMICS; HEDGEHOG PROTEINS; MODELS, MOLECULAR; MULTIGENE FAMILY; PHYLOGENY; POULTRY; PROTEIN STRUCTURE, TERTIARY; REPTILES; VERTEBRATES;

EID: 84920130334     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0074132     Document Type: Article

References (114)

1. Nichols SA, Dirks W, Pearse JS, King N (2006) Early evolution of animal cell signaling and adhesion genes. Proc Natl Acad Sci U S A 103: 12451-12456.
2. Ingham PW, Nakano Y, Seger C (2011) Mechanisms and functions of Hedgehog signalling across the metazoa. Nat Rev Genet 12: 393-406.
3. Ingham PW, McMahon AP (2001) Hedgehog signaling in animal development: paradigms and principles. Genes Dev 15: 3059-3087.
4. Lee JJ, Ekker SC, von Kessler DP, Porter JA, Sun BI, et al. (1994) Autoproteolysis in hedgehog protein biogenesis. Science 266: 1528-1537.
5. Beachy PA, Cooper MK, Young KE, von Kessler DP, Park WJ, et al. (1997) Multiple roles of cholesterol in hedgehog protein biogenesis and signaling. Cold Spring Harb Symp Quant Biol 62: 191-204.
6. Chen MH, Li YJ, Kawakami T, Xu SM, Chuang PT (2004) Palmitoylation is required for the production of a soluble multimeric Hedgehog protein complex and long-range signaling in vertebrates. Genes Dev 18: 641-659.
7. Chen X, Tukachinsky H, Huang CH, Jao C, Chu YR, et al. (2011) Processing and turnover of the Hedgehog protein in the endoplasmic reticulum. J Cell Biol 192: 825-838.
8. Eugster C, Panakova D, Mahmoud A, Eaton S (2007) Lipoprotein-heparan sulfate interactions in the Hh pathway. Dev Cell 13: 57-71.
9. Burglin TR (2008) The Hedgehog protein family. Genome Biol 9: 241.
10. Kumar S, Balczarek K, Lai Z (1996) Evolution of the hedgehog gene family. Genetics 142: 965-1037.
11. Chen X, Tukachinsky H, Huang C-H, Jao C, Chu Y-R, et al. (2011) Processing and turnover of the Hedgehog protein in the endoplasmic reticulum. The Journal of cell biology 192: 825-863.
12. Koonin EV (1995) A protein splice-junction motif in hedgehog family proteins. Trends Biochem Sci 20: 141-142.
13. Chamoun Z, Mann R, Nellen D, von Kessler D, Bellotto M, et al. (2001) Skinny hedgehog, an acyltransferase required for palmitoylation and activity of the hedgehog signal. Science (New York, NY) 293: 2080-2084.
14. Zheng X, Mann RK, Sever N, Beachy PA (2010) Genetic and biochemical definition of the Hedgehog receptor. Genes Dev 24: 57-71.
15. Murone M, Rosenthal A, de Sauvage FJ (1999) Hedgehog signal transduction: from flies to vertebrates. Exp Cell Res 253: 25-33.
16. Taipale J, Beachy P (2001) The Hedgehog and Wnt signalling pathways in cancer. Nature 411: 349-403.
17. Odent S, Atti-Bitach T, Blayau M, Mathieu M, Aug J, et al. (1999) Expression of the Sonic hedgehog (SHH) gene during early human development and phenotypic expression of new mutations causing holoprosencephaly. Hum Mol Genet 8: 1683-1689.
18. Nanni L, Ming JE, Bocian M, Steinhaus K, Bianchi DW, et al. (1999) The mutational spectrum of the sonic hedgehog gene in holoprosencephaly: SHH mutations cause a significant proportion of autosomal dominant holoprosencephaly. Hum Mol Genet 8: 2479-2488.
19. Mortier GR, Kramer PP, Giedion A, Beemer FA (2003) Acrocapitofemoral dysplasia: an autosomal recessive skeletal dysplasia with cone shaped epiphyses in the hands and hips. J Med Genet 40: 201-207.
20. Umehara F, Tate G, Itoh K, Yamaguchi N, Douchi T, et al. (2000) A novel mutation of desert hedgehog in a patient with 46, XY partial gonadal dysgenesis accompanied by minifascicular neuropathy. American journal of human genetics 67: 1302-1307.
21. Rubin L, de Sauvage F (2006) Targeting the Hedgehog pathway in cancer. Nature reviews Drug discovery 5: 1026-1059.
22. Burglin TR (2008) Evolution of hedgehog and hedgehog-related genes, their origin from Hog proteins in ancestral eukaryotes and discovery of a novel Hint motif. BMC Genomics 9: 127.
23. Hao L, Johnsen R, Lauter G, Baillie D, Burglin TR (2006) Comprehensive analysis of gene expression patterns of hedgehog-related genes. BMC Genomics 7: 280.
24. Hammerschmidt M, Brook A, McMahon AP (1997) The world according to hedgehog. Trends Genet 13: 14-21.
25. Varjosalo M, Taipale J (2008) Hedgehog: functions and mechanisms.
26. Nagase T, Nagase M, Machida M, Yamagishi M (2007) Hedgehog signaling: a biophysical or biomechanical modulator in embryonic development? Ann N Y Acad Sci 1101: 412-438.
27. Yao HH, Whoriskey W, Capel B (2002) Desert Hedgehog/Patched 1 signaling specifies fetal Leydig cell fate in testis organogenesis. Genes Dev 16: 1433-1440.
28. Zardoya R, Abouheif E, Meyer A (1996) Evolution and orthology of hedgehog genes. Trends Genet 12: 496-497.
29. Avaron F, Hoffman L, Guay D, Akimenko MA (2006) Characterization of two new zebrafish members of the hedgehog family: atypical expression of a zebrafish indian hedgehog gene in skeletal elements of both endochondral and dermal origins. Dev Dyn 235: 478-489.
30. Hadzhiev Y, Lang M, Ertzer R, Meyer A, Strahle U, et al. (2007) Functional diversification of sonic hedgehog paralog enhancers identified by phylogenomic reconstruction. Genome Biol 8: R106.
31. Bingham S, Nasevicius A, Ekker SC, Chandrasekhar A (2001) Sonic hedgehog and tiggy-winkle hedgehog cooperatively induce zebrafish branchiomotor neurons. Genesis 30: 170-174.
32. Meyer A, Van de Peer Y (2005) From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). Bioessays 27: 937-945.
33. Ekker SC, McGrew LL, Lai CJ, Lee JJ, von Kessler DP, et al. (1995) Distinct expression and shared activities of members of the hedgehog gene family of Xenopus laevis. Development 121: 2337-2347.
34. Kano S, Xiao JH, Osorio J, Ekker M, Hadzhiev Y, et al. (2010) Two lamprey Hedgehog genes share non-coding regulatory sequences and expression patterns with gnathostome Hedgehogs. PLoS One 5: e13332.
35. Takatori N, Satou Y, Satoh N (2002) Expression of hedgehog genes in Ciona intestinalis embryos. Mech Dev 116: 235-238.
36. Gunbin K, Afonnikov D, Kolchanov N (2007) The evolution of the Hh-signaling pathway genes: a computer-assisted study. In silico biology 7: 333-387.
37. Muffato M, Louis A, Poisnel CE, Crollius HR (2010) Genomicus: a database and a browser to study gene synteny in modern and ancestral genomes. Bioinformatics 26: 1119-1121.
38. Flicek P, Amode MR, Barrell D, Beal K, Brent S, et al. (2012) Ensembl 2012. Nucleic Acids Research 40: D84-D90.
39. Dutcher SK (2001) The tubulin fraternity: alpha to eta. Curr Opin Cell Biol 13: 49-54.
40. McKean PG, Vaughan S, Gull K (2001) The extended tubulin superfamily. J Cell Sci 114: 2723-2733.
41. Sun X-J, Xu P-F, Zhou T, Hu M, Fu C-T, et al. (2008) Genome-Wide Survey and Developmental Expression Mapping of Zebrafish SET Domain-Containing Genes. PLoS One 3: e1499.
42. Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW (2011) GenBank. Nucleic Acids Research 39: D32-D37.
43. Djabali M, Selleri L, Parry P, Bower M, Young B, et al. (1992) A trithorax-like gene is interrupted by chromosome 11q23 translocations in acute leukaemias. Nature genetics 2: 113-121.
44. Krivtsov A, Armstrong S (2007) MLL translocations, histone modifications and leukaemia stem-cell development. Nature reviews Cancer 7: 823-856.
45. Misawa H, Yamaguchi M (2000) The gene of Ca2+-binding protein regucalcin is highly conserved in vertebrate species. Int J Mol Med 6: 191-196.
46. Yang Z (2007) PAML 4: Phylogenetic Analysis by Maximum Likelihood. Molecular Biology and Evolution 24: 1586-1591.
47. Yang Z (1998) Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Molecular Biology and Evolution 15: 568-641.
48. Yang Z (2002) Inference of selection from multiple species alignments. Current opinion in genetics & development 12: 688-782.
49. Kosakovsky Pond S, Frost S (2005) Not so different after all: a comparison of methods for detecting amino acid sites under selection. Molecular Biology and Evolution 22: 1208-1230.
50. Pond S, Frost S (2005) Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics (Oxford, England) 21: 2531-2534.
51. Delport W, Poon A, Frost S, Kosakovsky Pond S (2010) Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology. Bioinformatics (Oxford, England) 26: 2455-2462.
52. McClellan D, McCracken K (2001) Estimating the influence of selection on the variable amino acid sites of the cytochrome B protein functional domains. Molecular Biology and Evolution 18: 917-942.
53. McClellan D, Palfreyman E, Smith M, Moss J, Christensen R, et al. (2005) Physicochemical evolution and molecular adaptation of the cetacean and artiodactyl cytochrome b proteins. Molecular Biology and Evolution 22: 437-492.
54. da Fonseca R, Johnson W, O'Brien S, Ramos M, Antunes A (2008) The adaptive evolution of the mammalian mitochondrial genome. BMC Genomics 9: 119.
55. da Fonseca R, Antunes A, Melo A, Ramos M (2007) Structural divergence and adaptive evolution in mammalian cytochromes P450 2C. Gene 387: 58-124.
56. Woolley S, Johnson J, Smith M, Crandall K, McClellan D (2003) TreeSAAP: selection on amino acid properties using phylogenetic trees. Bioinformatics (Oxford, England) 19: 671-673.
57. Gu X (1999) Statistical methods for testing functional divergence after gene duplication. Molecular Biology and Evolution 16: 1664-1738.
58. Gu X (2001) Maximum-likelihood approach for gene family evolution under functional divergence. Molecular Biology and Evolution 18: 453-517.
59. Gu X (2006) A simple statistical method for estimating type-II (cluster-specific) functional divergence of protein sequences. Molecular Biology and Evolution 23: 1937-1982.
60. Gu X, Vander Velden K (2002) DIVERGE: phylogeny-based analysis for functional-structural divergence of a protein family. Bioinformatics (Oxford, England) 18: 500-501.
61. Beachy P, Hymowitz S, Lazarus R, Leahy D, Siebold C (2010) Interactions between Hedgehog proteins and their binding partners come into view. Genes & development 24: 2001-2013.
62. Irimia M, Royo JL, Burguera D, Maeso I, Gómez-Skarmeta JL, et al. (2012) Comparative genomics of the Hedgehog loci in chordates and the origins of Shh regulatory novelties. Sci Rep 2.
63. Kuraku S, Meyer A, Kuratani S (2009) Timing of genome duplications relative to the origin of the vertebrates: did cyclostomes diverge before or after? Molecular Biology and Evolution 26: 47-106.
64. Burt DW (2002) Origin and evolution of avian microchromosomes. Cytogenet Genome Res 96: 97-112.
65. Ladjali-Mohammedi K, Bitgood JJ, Tixier-Boichard M, Ponce De Leon FA (1999) International system for standardized avian karyotypes (ISSAK): standardized banded karyotypes of the domestic fowl (Gallus domesticus). Cytogenet Cell Genet 86: 271-276.
66. International Chicken Genome Sequencing Consortium (2004) Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432: 695-716.
67. Masabanda JS, Burt DW, O'Brien PC, Vignal A, Fillon V, et al. (2004) Molecular cytogenetic definition of the chicken genome: the first complete avian karyotype. Genetics 166: 1367-1373.
68. Morisson M, Denis M, Milan D, Klopp C, Leroux S, et al. (2007) The chicken RH map: current state of progress and microchromosome mapping. Cytogenet Genome Res 117: 14-21.
69. Trukhina AV, Smirnov AF (2010) Microsatellites from the linkage groups E26C13 and E50C23 are located on the Gallus gallus domesticus microchromosomes 20 and 21. Genetika 46: 509-516.
70. Davis J, Brandman O, Petrov D (2005) Protein evolution in the context of Drosophila development. Journal of molecular evolution 60: 774-859.
71. Roux J, Robinson-Rechavi M (2008) Developmental constraints on vertebrate genome evolution. PLoS Genet 4: e1000311.
72. McLellan J, Zheng X, Hauk G, Ghirlando R, Beachy P, et al. (2008) The mode of Hedgehog binding to Ihog homologues is not conserved across different phyla. Nature 455: 979-1062.
73. Swanson WJ, Vacquier VD (2002) The rapid evolution of reproductive proteins. Nat Rev Genet 3: 137-144.
74. Sobrinho I, de Brito R (2010) Evidence for positive selection in the gene fruitless in Anastrepha fruit flies. BMC evolutionary biology 10: 293.
75. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, et al. (2009) BLAST+: architecture and applications. BMC Bioinformatics 10: 421.
76. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797.
77. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Molecular Biology and Evolution 28: 2731-2739.
78. Gouy M, Guindon S, Gascuel O (2010) SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27: 221-224.
79. Dessimoz C, Gil M (2010) Phylogenetic assessment of alignments reveals neglected tree signal in gaps. Genome biology 11.
80. Posada D (2008) jModelTest: Phylogenetic Model Averaging. Molecular Biology and Evolution 25: 1253-1256.
81. Xia X, Xie Z (2001) DAMBE: Software Package for Data Analysis in Molecular Biology and Evolution. Journal of Heredity 92: 371-373.
82. Xia X, Xie Z, Salemi M, Chen L, Wang Y (2003) An index of substitution saturation and its application. Molecular phylogenetics and evolution 26: 1-8.
83. Guindon S, Delsuc F, Dufayard J-F, Gascuel O (2009) Estimating maximum likelihood phylogenies with PhyML. Methods in molecular biology (Clifton, NJ) 537: 113-150.
84. Huelsenbeck J, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics (Oxford, England) 17: 754-759.
85. Ronquist F, Huelsenbeck J (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics (Oxford, England) 19: 1572-1576.
86. Castresana J (2000) Selection of Conserved Blocks from Multiple Alignments for Their Use in Phylogenetic Analysis. Molecular Biology and Evolution 17: 540-552.
87. Talavera G, Castresana J (2007) Improvement of Phylogenies after Removing Divergent and Ambiguously Aligned Blocks from Protein Sequence Alignments. Systematic Biology 56: 564-577.
88. Yang Z, Nielsen R, Goldman N, Pedersen A (2000) Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155: 431-480.
89. Yang Z, Wong W, Nielsen R (2005) Bayes empirical bayes inference of amino acid sites under positive selection. Molecular Biology and Evolution 22: 1107-1125.
90. Porter M, Cronin T, McClellan D, Crandall K (2007) Molecular characterization of crustacean visual pigments and the evolution of pancrustacean opsins. Molecular Biology and Evolution 24: 253-321.
91. Wang Y, Gu X (2001) Functional divergence in the caspase gene family and altered functional constraints: statistical analysis and prediction. Genetics 158: 1311-1331.
92. Jeffreys H, editor (1998) Theory of Probability. 3rd ed.
93. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, et al. (2000) The Protein Data Bank. Nucleic Acids Research 28: 235-242.
94. Roy A, Xu D, Poisson J, Zhang Y (2011) A protocol for computer-based protein structure and function prediction. J Vis Exp: e3259.
95. Zhang Y (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 9: 40.
96. Battey JN, Kopp J, Bordoli L, Read RJ, Clarke ND, et al. (2007) Automated server predictions in CASP7. Proteins 69 Suppl 8: 68-82.
97. Zhang Y (2007) Template-based modeling and free modeling by I-TASSER in CASP7. Proteins 69 Suppl 8: 108-117.
98. Zhang Y (2009) I-TASSER: fully automated protein structure prediction in CASP8. Proteins 77 Suppl 9: 100-113.
99. Cozzetto D, Kryshtafovych A, Fidelis K, Moult J, Rost B, et al. (2009) Evaluation of template-based models in CASP8 with standard measures. Proteins 77 Suppl 9: 18-28.
100. Wu S, Szilagyi A, Zhang Y (2011) Improving protein structure prediction using multiple sequence-based contact predictions. Structure 19: 1182-1191.
101. Kinch L, Yong Shi S, Cong Q, Cheng H, Liao Y, et al. (2011) CASP9 assessment of free modeling target predictions. Proteins 79 Suppl 10: 59-73.
102. Roy A, Kucukural A, Zhang Y (2010) I-TASSER: a unified platform for automated protein structure and function prediction. Nature protocols 5: 725-763.
103. Zhang Y, Skolnick J (2004) Scoring function for automated assessment of protein structure template quality. Proteins 57: 702-710.
104. The PyMOL Molecular Graphics System, Version 1.2r3pre, Schrödinger, LLC.
105. Alföldi J, Di Palma F, Grabherr M, Williams C, Kong L, et al. (2011) The genome of the green anole lizard and a comparative analysis with birds and mammals. Nature 477: 587-678.
106. Zhan X, Pan S, Wang J, Dixon A, He J, et al. (2013) Peregrine and saker falcon genome sequences provide insights into evolution of a predatory lifestyle. Nat Genet.
107. St John J, Braun E, Isberg S, Miles L, Chong A, et al. (2012) Sequencing three crocodilian genomes to illuminate the evolution of archosaurs and amniotes. Genome Biology 13: 415.
108. Hillier LDW, Miller W, Birney E, Warren W, Hardison RC, et al. (2004) Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432: 695-1411.
109. Darling ACE, Mau B, Blattner FR, Perna NT (2004) Mauve: Multiple Alignment of Conserved Genomic Sequence With Rearrangements. Genome Research 14: 1394-1403.
110. Darling AE, Mau B, Perna NT (2010) progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 5: e11147.
111. Fujita PA, Rhead B, Zweig AS, Hinrichs AS, Karolchik D, et al. (2010) The UCSC Genome Browser database: update 2011. Nucleic Acids Research.
112. Okonechnikov K, Golosova O, Fursov M, the UGENE team (2012) Unipro UGENE: a unified bioinformatics toolkit. Bioinformatics.
113. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, et al. (2009) Circos: an information aesthetic for comparative genomics. Genome Research 19: 1639-1684.
114. Magrane M, Consortium U (2011) UniProt Knowledgebase: a hub of integrated protein data. Database: the journal of biological databases and curation 2011.