Comparative phylogenomic analyses of teleost fish Hox gene clusters: lessons from the cichlid fish Astatotilapia burtoni

Hoegg, Simone; Boore, Jeffrey L.; Kuehl, Jennifer V.; Meyer, Axel

doi:10.1186/1471-2164-8-317

Comparative phylogenomic analyses of teleost fish Hox gene clusters: lessons from the cichlid fish Astatotilapia burtoni

Journal Article · Mon Sep 10 00:00:00 EDT 2007 · BMC Genomics

DOI:https://doi.org/10.1186/1471-2164-8-317· OSTI ID:1626455

Hoegg, Simone ^[1]; Boore, Jeffrey L. ^[2]; Kuehl, Jennifer V. ^[2]; Meyer, Axel ^[3]

Univ. of Konstanz (Germany); DOE/OSTI
DOE Joint Genome Inst. and Lawrence Berkeley National Lab. (LBNL), and Univ. of California, Berkeley, CA (United States)
Univ. of Konstanz (Germany)

Teleost fish have seven paralogous clusters of Hox genes stemming from two complete genome duplications early in vertebrate evolution, and an additional genome duplication during the evolution of ray-finned fish, followed by the secondary loss of one cluster. Gene duplications on the one hand, and the evolution of regulatory sequences on the other, are thought to be among the most important mechanisms for the evolution of new gene functions. Cichlid fish, the largest family of vertebrates with about 2500 species, are famous examples of speciation and morphological diversity. Since this diversity could be based on regulatory changes, we chose to study the coding as well as putative regulatory regions of their Hox clusters within a comparative genomic framework. We sequenced and characterized all seven Hox clusters of Astatotilapia burtoni, a haplochromine cichlid fish. Comparative analyses with data from other teleost fish such as zebrafish, two species of pufferfish, stickleback and medaka were performed. We traced losses of genes and microRNAs of Hox clusters, the medaka lineage seems to have lost more microRNAs than the other fish lineages. We found that each teleost genome studied so far has a unique set of Hox genes. The hoxb7a gene was lost independently several times during teleost evolution, the most recent event being within the radiation of East African cichlid fish. The conserved non-coding sequences (CNS) encompass a surprisingly large part of the clusters, especially in the HoxAa, HoxCa, and HoxDa clusters. Across all clusters, we observe a trend towards an increased content of CNS towards the anterior end. The gene content of Hox clusters in teleost fishes is more variable than expected, with each species studied so far having a different set. Although the highest loss rate of Hox genes occurred immediately after whole genome duplications, our analyses showed that gene loss continued and is still ongoing in all teleost lineages. Along with the gene content, the CNS content also varies across clusters. The excess of CNS at the anterior end of clusters could imply a stronger conservation of anterior expression patters than those towards more posterior areas of the embryo.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1626455

Journal Information:: BMC Genomics, Journal Name: BMC Genomics Journal Issue: 1 Vol. 8; ISSN 1471-2164

Publisher:: SpringerCopyright Statement

Country of Publication:: United States

Language:: English

References (95)

Unusual gene order and organization of the sea urchin hox cluster Cameron, R. Andrew; Rowen, Lee; Nesbitt, Ryan Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, Vol. 306B, Issue 1 https://doi.org/10.1002/jez.b.21070	journal	January 2006
The Shark HoxN Cluster Is Homologous to the Human HoxD Cluster Prohaska, Sonja J.; Fried, Claudia; Amemiya, Chris T. Journal of Molecular Evolution, Vol. 58, Issue 2 https://doi.org/10.1007/s00239-003-2545-z	journal	February 2004
Molecular Evolution of Duplicated Ray Finned Fish HoxA Clusters: Increased Synonymous Substitution Rate and Asymmetrical Co-divergence of Coding and Non-coding Sequences Wagner, Günter P.; Takahashi, Kazuhiko; Lynch, Vincent Journal of Molecular Evolution, Vol. 60, Issue 5 https://doi.org/10.1007/s00239-004-0252-z	journal	May 2005
Phylogenetic Timing of the Fish-Specific Genome Duplication Correlates with the Diversification of Teleost Fish Hoegg, Simone; Brinkmann, Henner; Taylor, John S. Journal of Molecular Evolution, Vol. 59, Issue 2 https://doi.org/10.1007/s00239-004-2613-z	journal	August 2004
Novel Relationships Among Ten Fish Model Species Revealed Based on a Phylogenomic Analysis Using ESTs Steinke, Dirk; Salzburger, Walter; Meyer, Axel Journal of Molecular Evolution, Vol. 62, Issue 6 https://doi.org/10.1007/s00239-005-0170-8	journal	May 2006
Developmental expression of the amphioxus Tbx1/10 gene illuminates the evolution of vertebrate branchial arches and sclerotome Mahadevan, Navin R.; Horton, Amy C.; Gibson-Brown, Jeremy J. Development Genes and Evolution, Vol. 214, Issue 11 https://doi.org/10.1007/s00427-004-0433-1	journal	September 2004
Molecular and biological characterization of an isolate of the potyvirus passiflora virus Y naturally infecting soybean (Glycine max) in Brazil Ribeiro-Junior, Marcos Roberto; Barreto da Silva, Felipe; Marubayashi, Julio Massaharu Archives of Virology, Vol. 167, Issue 12 https://doi.org/10.1007/s00705-022-05605-5	journal	September 2022
Organization and base composition of tilapia Hox genes: implications for the evolution of Hox clusters in fish Santini, Simona; Bernardi, Giorgio Gene, Vol. 346 https://doi.org/10.1016/j.gene.2004.10.027	journal	February 2005
Mitochondrial molecular clocks and the origin of the major Otocephalan clades (Pisces: Teleostei): A new insight Peng, Zuogang; He, Shunping; Wang, Jun Gene, Vol. 370 https://doi.org/10.1016/j.gene.2005.11.024	journal	March 2006
Novel evolutionary relationship among four fish model systems Chen, Wei-Jen; Ortí, Guillermo; Meyer, Axel Trends in Genetics, Vol. 20, Issue 9 https://doi.org/10.1016/j.tig.2004.07.005	journal	September 2004
Hox clusters as models for vertebrate genome evolution Hoegg, Simone; Meyer, Axel Trends in Genetics, Vol. 21, Issue 8 https://doi.org/10.1016/j.tig.2005.06.004	journal	August 2005
Genome duplication and the origin of angiosperms Debodt, S.; Maere, S.; Vandepeer, Y. Trends in Ecology & Evolution, Vol. 20, Issue 11 https://doi.org/10.1016/j.tree.2005.07.008	journal	November 2005
Possible Significance of Duplication in Evolution Stephens, S. G. Advances in Genetics https://doi.org/10.1016/s0065-2660(08)60237-0	book	January 1951
Potential Protection by Cyclosporin Against Glucocorticoid Effects on bone Kelly, P. J.; Sambrook, P. N.; Eisman, J. A. The Lancet, Vol. 334, Issue 8676 https://doi.org/10.1016/s0140-6736(89)91988-0	journal	December 1989
Genome duplication, divergent resolution and speciation Taylor, John S.; Van de Peer, Yves; Meyer, Axel Trends in Genetics, Vol. 17, Issue 6 https://doi.org/10.1016/s0168-9525(01)02318-6	journal	June 2001
Transcription regulation and animal diversity Levine, Michael; Tjian, Robert Nature, Vol. 424, Issue 6945 https://doi.org/10.1038/nature01763	journal	July 2003
Hox cluster disintegration with persistent anteroposterior order of expression in Oikopleura dioica Seo, Hee-Chan; Edvardsen, Rolf Brudvik; Maeland, Anne Dorthea Nature, Vol. 431, Issue 7004 https://doi.org/10.1038/nature02709	journal	September 2004
Organization of the Fugu rubripes Hox clusters: evidence for continuing evolution of vertebrate Hox complexes Aparicio, Samuel; Hawker, Kelvin; Cottage, Amanda Nature Genetics, Vol. 16, Issue 1 https://doi.org/10.1038/ng0597-79	journal	May 1997
The zebrafish hoxDb cluster has been reduced to a single microRNA Woltering, Joost M.; Durston, Antony J. Nature Genetics, Vol. 38, Issue 6 https://doi.org/10.1038/ng0606-601	journal	June 2006
Homozygous HOXA1 mutations disrupt human brainstem, inner ear, cardiovascular and cognitive development Tischfield, Max A.; Bosley, Thomas M.; Salih, Mustafa A. M. Nature Genetics, Vol. 37, Issue 10 https://doi.org/10.1038/ng1636	journal	September 2005
The amphioxus Hox cluster: deuterostome posterior flexibility and Hox14 Ferrier, David E. K.; Minguillón, Carolina; Holland, Peter W. H. Evolution & Development, Vol. 2, Issue 5 https://doi.org/10.1046/j.1525-142x.2000.00070.x	journal	September 2000
Hox gene clusters in the Indonesian coelacanth, Latimeria menadoensis Koh, E. G. L.; Lam, K.; Christoffels, A. Proceedings of the National Academy of Sciences, Vol. 100, Issue 3 https://doi.org/10.1073/pnas.0237317100	journal	January 2003
Ciona intestinalis Hox gene cluster: Its dispersed structure and residual colinear expression in development Ikuta, T.; Yoshida, N.; Satoh, N. Proceedings of the National Academy of Sciences, Vol. 101, Issue 42 https://doi.org/10.1073/pnas.0401389101	journal	October 2004
Regulatory gene networks and the properties of the developmental process Davidson, E. H.; McClay, D. R.; Hood, L. Proceedings of the National Academy of Sciences, Vol. 100, Issue 4 https://doi.org/10.1073/pnas.0437746100	journal	February 2003
Breakup of a homeobox cluster after genome duplication in teleosts Mulley, J. F.; Chiu, C. -h.; Holland, P. W. H. Proceedings of the National Academy of Sciences, Vol. 103, Issue 27 https://doi.org/10.1073/pnas.0600341103	journal	June 2006
Highly conserved syntenic blocks at the vertebrate Hox loci and conserved regulatory elements within and outside Hox gene clusters Lee, A. P.; Koh, E. G. L.; Tay, A. Proceedings of the National Academy of Sciences, Vol. 103, Issue 18 https://doi.org/10.1073/pnas.0601492103	journal	April 2006
VISTA : visualizing global DNA sequence alignments of arbitrary length Mayor, C.; Brudno, M.; Schwartz, J. R. Bioinformatics, Vol. 16, Issue 11 https://doi.org/10.1093/bioinformatics/16.11.1046	journal	November 2000
A Detailed Linkage Map of Medaka, Oryzias latipes: Comparative Genomics and Genome Evolution Naruse, Kiyoshi; Fukamachi, Shoji; Mitani, Hiroshi Genetics, Vol. 154, Issue 4 https://doi.org/10.1093/genetics/154.4.1773	journal	April 2000
Fugu Genome Analysis Provides Evidence for a Whole-Genome Duplication Early During the Evolution of Ray-Finned Fishes Christoffels, Alan; Koh, Esther G. L.; Chia, Jer-ming Molecular Biology and Evolution, Vol. 21, Issue 6 https://doi.org/10.1093/molbev/msh114	journal	June 2004
The “Fish-Specific” Hox Cluster Duplication Is Coincident with the Origin of Teleosts Crow, Karen D.; Stadler, Peter F.; Lynch, Vincent J. Molecular Biology and Evolution, Vol. 23, Issue 1 https://doi.org/10.1093/molbev/msj020	journal	September 2005
Asymmetric Evolution in Two Fish-Specifically Duplicated Receptor Tyrosine Kinase Paralogons Involved in Teleost Coloration Braasch, Ingo; Salzburger, Walter; Meyer, Axel Molecular Biology and Evolution, Vol. 23, Issue 6 https://doi.org/10.1093/molbev/msk003	journal	March 2006
Comparative genomics provides evidence for an ancient genome duplication event in fish Taylor, John S.; Van de Peer, Yves; Braasch, Ingo Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, Vol. 356, Issue 1414 https://doi.org/10.1098/rstb.2001.0975	journal	October 2001
Zebrafish Comparative Genomics and the Origins of Vertebrate Chromosomes Postlethwait, J. H. Genome Research, Vol. 10, Issue 12 https://doi.org/10.1101/gr.164800	journal	December 2000
Bichir HoxA Cluster Sequence Reveals Surprising Trends in Ray-Finned Fish Genomic Evolution Chiu, C. -h. Genome Research, Vol. 14, Issue 1 https://doi.org/10.1101/gr.1712904	journal	December 2003
Developmental Roles of Pufferfish Hox Clusters and Genome Evolution in Ray-Fin Fish Amores, A. Genome Research, Vol. 14, Issue 1 https://doi.org/10.1101/gr.1717804	journal	December 2003
Conservation of regulatory sequences and gene expression patterns in the disintegrating Drosophila Hox gene complex Negre, B. Genome Research, Vol. 15, Issue 5 https://doi.org/10.1101/gr.3468605	journal	April 2005
The Human Hox-bearing Chromosome Regions Did Arise by Block or Chromosome (or Even Genome) Duplications Larhammar, D. Genome Research, Vol. 12, Issue 12 https://doi.org/10.1101/gr.445702	journal	December 2002
LAGAN and Multi-LAGAN: Efficient Tools for Large-Scale Multiple Alignment of Genomic DNA Brudno, M. Genome Research, Vol. 13, Issue 4 https://doi.org/10.1101/gr.926603	journal	March 2003
Altered Growth and Branching Patterns in Synpolydactyly Caused by Mutations in HOXD13 Muragaki, Yasuteru; Mundlos, Stefan; Upton, Joseph Science, Vol. 272, Issue 5261 https://doi.org/10.1126/science.272.5261.548	journal	April 1996
Zebrafish hox Clusters and Vertebrate Genome Evolution Amores, A. Science, Vol. 282, Issue 5394 https://doi.org/10.1126/science.282.5394.1711	journal	November 1998
Many genes in fish have species-specific asymmetric rates of molecular evolution Steinke, Dirk; Salzburger, Walter; Braasch, Ingo BMC Genomics, Vol. 7, Issue 1 https://doi.org/10.1186/1471-2164-7-20	journal	February 2006
Analysis of Hox gene expression in the chick limb bud Nelson, C. E.; Morgan, B. A.; Burke, A. C. Development, Vol. 122, Issue 5 https://doi.org/10.1242/dev.122.5.1449	journal	May 1996
Knockdown of duplicated zebrafish hoxb1 genes reveals distinct roles in hindbrain patterning and a novel mechanism of duplicate gene retention McClintock, James M.; Kheirbek, Mazen A.; Prince, Victoria E. Development, Vol. 129, Issue 10 https://doi.org/10.1242/dev.129.10.2339	journal	May 2002
Evolutionary Plasticity of Vertebrate Hox Genes Powers, Thomas; Amemiya, Chris Current Genomics, Vol. 5, Issue 6 https://doi.org/10.2174/1389202043349048	journal	August 2004
From 2R to 3R: evidence for a fish-specific genome duplication (FSGD) Meyer, Axel; Van de Peer, Yves BioEssays, Vol. 27, Issue 9 https://doi.org/10.1002/bies.20293	journal	January 2005
Exclusion of repetitive DNA elements from gnathostomeHox clusters Fried, Claudia; Prohaska, Sonja J.; Stadler, Peter F. Journal of Experimental Zoology, Vol. 302B, Issue 2 https://doi.org/10.1002/jez.b.20007	journal	January 2004
Evolution of microRNAs located withinHox gene clusters Tanzer, Andrea; Amemiya, Chris T.; Kim, Chang-Bae Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, Vol. 304B, Issue 1 https://doi.org/10.1002/jez.b.21021	journal	January 2005
A BAC library of the East African haplochromine cichlid fishAstatotilapia burtoni Lang, Michael; Miyake, Tsutomu; Braasch, Ingo Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, Vol. 306B, Issue 1 https://doi.org/10.1002/jez.b.21068	journal	January 2006
Evolution by Gene Duplication Ohno, Susumu Springer Berlin, Heidelberg https://doi.org/10.1007/978-3-642-86659-3	book	January 1970
The species flocks of East African cichlid fishes: recent advances in molecular phylogenetics and population genetics Salzburger, Walter; Meyer, Axel Naturwissenschaften, Vol. 91, Issue 6 https://doi.org/10.1007/s00114-004-0528-6	journal	April 2004
Teleost HoxD and HoxA genes: comparison with tetrapods and functional evolution of the HOXD complex van der Hoeven, Frank; Sordino, Paolo; Fraudeau, Nadine Mechanisms of Development, Vol. 54, Issue 1 https://doi.org/10.1016/0925-4773(95)00455-6	journal	January 1996
Teleostean Monophyly De Pinna, Mãrio C. C. Interrelationships of Fishes https://doi.org/10.1016/B978-012670950-6/50008-4	book	January 1996
Possible Significance of Duplication in Evolution Stephens, S. G. Advances in Genetics https://doi.org/10.1016/S0065-2660(08)60237-0	book	January 1951
Genome duplication, divergent resolution and speciation Taylor, John S.; Van de Peer, Yves; Meyer, Axel Trends in Genetics, Vol. 17, Issue 6 https://doi.org/10.1016/S0168-9525(01)02318-6	journal	June 2001
Speciation in nature: the threespine stickleback model systems McKinnon, Jeffrey S.; Rundle, Howard D. Trends in Ecology & Evolution, Vol. 17, Issue 10 https://doi.org/10.1016/S0169-5347(02)02579-X	journal	October 2002
Gene and genome duplications in vertebrates: the one-to-four (-to-eight in fish) rule and the evolution of novel gene functions Meyer, A.; Schartl, M. Current Opinion in Cell Biology, Vol. 11, Issue 6 https://doi.org/10.1016/S0955-0674(99)00039-3	journal	December 1999
Gen(om)e duplications in the evolution of early vertebrates Sidow, Arend Current Opinion in Genetics & Development, Vol. 6, Issue 6 https://doi.org/10.1016/S0959-437X(96)80026-8	journal	December 1996
Major patterns of higher teleostean phylogenies: a new perspective based on 100 complete mitochondrial DNA sequences Miya, Masaki; Takeshima, Hirohiko; Endo, Hiromitsu Molecular Phylogenetics and Evolution, Vol. 26, Issue 1 https://doi.org/10.1016/S1055-7903(02)00332-9	journal	January 2003
Hox gene evolution in nematodes: novelty conserved Aboobaker, Aziz; Blaxter, Mark Current Opinion in Genetics & Development, Vol. 13, Issue 6 https://doi.org/10.1016/j.gde.2003.10.009	journal	December 2003
Organization and structure of hox gene loci in medaka genome and comparison with those of pufferfish and zebrafish genomes Kurosawa, Gene; Takamatsu, Naofumi; Takahashi, Masayoshi Gene, Vol. 370 https://doi.org/10.1016/j.gene.2005.11.015	journal	March 2006
Conserved co-regulation and promoter sharing of hoxb3a and hoxb4a in zebrafish Hadrys, Thorsten; Punnamoottil, Beena; Pieper, Mareike Developmental Biology, Vol. 297, Issue 1 https://doi.org/10.1016/j.ydbio.2006.04.446	journal	September 2006
Surveying phylogenetic footprints in large gene clusters: applications to Hox cluster duplications Prohaska, Sonja J.; Fried, Claudia; Flamm, Christoph Molecular Phylogenetics and Evolution, Vol. 31, Issue 2 https://doi.org/10.1016/j.ympev.2003.08.009	journal	May 2004
Mitogenomic evidence for the monophyly of elopomorph fishes (Teleostei) and the evolutionary origin of the leptocephalus larva Inoue, Jun G.; Miya, Masaki; Tsukamoto, Katsumi Molecular Phylogenetics and Evolution, Vol. 32, Issue 1 https://doi.org/10.1016/j.ympev.2003.11.009	journal	July 2004
A PCR survey for posterior Hox genes in amphibians Mannaert, An; Roelants, Kim; Bossuyt, Franky Molecular Phylogenetics and Evolution, Vol. 38, Issue 2 https://doi.org/10.1016/j.ympev.2005.08.012	journal	February 2006
More genes in vertebrates? Holland, Peter W. H. Journal of Structural and Functional Genomics, Vol. 3, Issue 1/4, p. 75-84 https://doi.org/10.1023/A:1022656931587	journal	January 2003
A gene complex controlling segmentation in Drosophila Lewis, E. B. Nature, Vol. 276, Issue 5688 https://doi.org/10.1038/276565a0	journal	December 1978
Archetypal organization of the amphioxus Hox gene cluster Garcia-Fernàndez, Jordi; Holland, Peter W. H. Nature, Vol. 370, Issue 6490 https://doi.org/10.1038/370563a0	journal	August 1994
Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events Bowers, John E.; Chapman, Brad A.; Rong, Junkang Nature, Vol. 422, Issue 6930 https://doi.org/10.1038/nature01521	journal	March 2003
Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae Kellis, Manolis; Birren, Bruce W.; Lander, Eric S. Nature, Vol. 428, Issue 6983 https://doi.org/10.1038/nature02424	journal	March 2004
Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype Jaillon, Olivier; Aury, Jean-Marc; Brunet, Frédéric Nature, Vol. 431, Issue 7011 https://doi.org/10.1038/nature03025	journal	October 2004
Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia Aury, Jean-Marc; Jaillon, Olivier; Duret, Laurent Nature, Vol. 444, Issue 7116 https://doi.org/10.1038/nature05230	journal	November 2006
Mutation of HOXA13 in hand-foot-genital syndrome Mortlock, Douglas P.; Innis, Jeffrey W. Nature Genetics, Vol. 15, Issue 2 https://doi.org/10.1038/ng0297-179	journal	February 1997
Gene regulatory network growth by duplication Teichmann, Sarah A.; Babu, M. Madan Nature Genetics, Vol. 36, Issue 5 https://doi.org/10.1038/ng1340	journal	April 2004
Major events in the genome evolution of vertebrates: Paranome age and size differ considerably between ray-finned fishes and land vertebrates Vandepoele, K.; De Vos, W.; Taylor, J. S. Proceedings of the National Academy of Sciences, Vol. 101, Issue 6 https://doi.org/10.1073/pnas.0307968100	journal	February 2004
Modeling gene and genome duplications in eukaryotes Maere, S.; De Bodt, S.; Raes, J. Proceedings of the National Academy of Sciences, Vol. 102, Issue 15 https://doi.org/10.1073/pnas.0501102102	journal	March 2005
Molecular evolution of the HoxA cluster in the three major gnathostome lineages Chiu, C. -h.; Amemiya, C.; Dewar, K. Proceedings of the National Academy of Sciences, Vol. 99, Issue 8 https://doi.org/10.1073/pnas.052709899	journal	April 2002
A Simple, Fast, and Accurate Algorithm to Estimate Large Phylogenies by Maximum Likelihood Guindon, Stéphane; Gascuel, Olivier Systematic Biology, Vol. 52, Issue 5 https://doi.org/10.1080/10635150390235520	journal	October 2003
MRBAYES: Bayesian inference of phylogenetic trees Huelsenbeck, J. P.; Ronquist, F. Bioinformatics, Vol. 17, Issue 8 https://doi.org/10.1093/bioinformatics/17.8.754	journal	August 2001
Divergence of Conserved Non-Coding Sequences: Rate Estimates and Relative Rate Tests Wagner, G. P. Molecular Biology and Evolution, Vol. 21, Issue 11 https://doi.org/10.1093/molbev/msh221	journal	July 2004
Subfunctionalization of Expression and Peptide Domains Following the Ancient Duplication of the Proopiomelanocortin Gene in Teleost Fishes de Souza, F. S. J. Molecular Biology and Evolution, Vol. 22, Issue 12 https://doi.org/10.1093/molbev/msi236	journal	August 2005
Gene Loss and Evolutionary Rates Following Whole-Genome Duplication in Teleost Fishes Brunet, Frédéric G.; Crollius, Hugues Roest; Paris, Mathilde Molecular Biology and Evolution, Vol. 23, Issue 9 https://doi.org/10.1093/molbev/msl049	journal	June 2006
The human HOX gene family Acampora, Dario; D'Esposito, Maurizio; Faiella, Antonio Nucleic Acids Research, Vol. 17, Issue 24 https://doi.org/10.1093/nar/17.24.10385	journal	January 1989
Were vertebrates octoploid? Furlong, Rebecca F.; Holland, Peter W. H. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, Vol. 357, Issue 1420 https://doi.org/10.1098/rstb.2001.1035	journal	April 2002
Genome Duplication, a Trait Shared by 22,000 Species of Ray-Finned Fish Taylor, J. S. Genome Research, Vol. 13, Issue 3 https://doi.org/10.1101/gr.640303	journal	March 2003
Evolutionary Conservation of Regulatory Elements in Vertebrate Hox Gene Clusters Santini, S. Genome Research, Vol. 13, Issue 6 https://doi.org/10.1101/gr.700503	journal	May 2003
Whole-Genome Shotgun Assembly and Analysis of the Genome of Fugu rubripes Aparicio, S. Science, Vol. 297, Issue 5585 https://doi.org/10.1126/science.1072104	journal	July 2002
Origin of the Superflock of Cichlid Fishes from Lake Victoria, East Africa Verheyen, Erik; Salzburger, Walter; Snoeks, Jos Science, Vol. 300, Issue 5617 https://doi.org/10.1126/science.1080699	journal	April 2003
Murine Developmental Control Genes Kessel, Michael; Gruss, Peter Science, Vol. 249, Issue 4967 https://doi.org/10.1126/science.1974085	journal	July 1990
Out of Tanganyika: Genesis, explosive speciation, key-innovations and phylogeography of the haplochromine cichlid fishes Salzburger, Walter; Mack, Tanja; Verheyen, Erik BMC Evolutionary Biology, Vol. 5, Issue 1 https://doi.org/10.1186/1471-2148-5-17	journal	January 2005
Extreme conservation of noncoding DNA near HoxD complex of vertebrates Sabarinadh, Chilaka; Subramanian, Subbaya; Tripathi, Anshuman BMC Genomics, Vol. 5, Issue 1 https://doi.org/10.1186/1471-2164-5-75	journal	October 2004
The gain and loss of genes during 600 million years of vertebrate evolution Blomme, Tine; Vandepoele, Klaas; De Bodt, Stefanie Genome Biology, Vol. 7, Issue 5, p. R43 https://doi.org/10.1186/gb-2006-7-5-r43	journal	January 2006
Knockdown of the complete Hox paralogous group 1 leads to dramatic hindbrain and neural crest defects McNulty, Claire L.; Peres, João N.; Bardine, Nabila Development, Vol. 132, Issue 12 https://doi.org/10.1242/dev.01872	journal	June 2005
Evolution at Two Levels: On Genes and Form Carroll, Sean B. PLoS Biology, Vol. 3, Issue 7 https://doi.org/10.1371/journal.pbio.0030245	journal	July 2005
Two Rounds of Whole Genome Duplication in the Ancestral Vertebrate Dehal, Paramvir; Boore, Jeffrey L. PLoS Biology, Vol. 3, Issue 10 https://doi.org/10.1371/journal.pbio.0030314	journal	September 2005
Genome Duplications and Accelerated Evolution of Hox Genes and Cluster Architecture in Teleost Fishes1 Málaga-Trillo, Edward; Meyer, Axel American Zoologist, Vol. 41, Issue 3 https://doi.org/10.1668/0003-1569(2001)041[0676:GDAAEO]2.0.CO;2	journal	June 2001

Cited By (19)

Hox cluster duplication in the basal teleost Hiodon alosoides (Osteoglossomorpha) Chambers, Karen E.; McDaniell, Ryan; Raincrow, Jeremy D. Theory in Biosciences, Vol. 128, Issue 2 https://doi.org/10.1007/s12064-009-0056-1	journal	February 2009
Unravelling paralogous gene expression dynamics during three-spined stickleback embryogenesis Kaitetzidou, Elisavet; Katsiadaki, Ioanna; Lagnel, Jacques Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-40127-2	journal	March 2019
Enigmatic Orthology Relationships between Hox Clusters of the African Butterfly Fish and Other Teleosts Following Ancient Whole-Genome Duplication Martin, Kyle J.; Holland, Peter W. H. Molecular Biology and Evolution, Vol. 31, Issue 10 https://doi.org/10.1093/molbev/msu202	journal	June 2014
SynBlast: Assisting the analysis of conserved synteny information Lehmann, Jörg; Stadler, Peter F.; Prohaska, Sonja J. BMC Bioinformatics, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2105-9-351	journal	August 2008
Sequence analyses of the distal-less homeobox gene family in East African cichlid fishes reveal signatures of positive selection Diepeveen, Eveline T.; Kim, Fabienne D.; Salzburger, Walter BMC Evolutionary Biology, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2148-13-153	journal	January 2013
Genome-wide identification, characterization, and expression analysis of lineage-specific genes within zebrafish Yang, Liandong; Zou, Ming; Fu, Beide BMC Genomics, Vol. 14, Issue 1 https://doi.org/10.1186/1471-2164-14-65	journal	January 2013
Identification of prohormones and pituitary neuropeptides in the African cichlid, Astatotilapia burtoni Hu, Caroline K.; Southey, Bruce R.; Romanova, Elena V. BMC Genomics, Vol. 17, Issue 1 https://doi.org/10.1186/s12864-016-2914-9	journal	August 2016
The genome of the largest bony fish, ocean sunfish (Mola mola), provides insights into its fast growth rate Pan, Hailin; Yu, Hao; Ravi, Vydianathan GigaScience, Vol. 5, Issue 1 https://doi.org/10.1186/s13742-016-0144-3	journal	September 2016
MiR-10 Represses HoxB1a and HoxB3a in Zebrafish Woltering, Joost M.; Durston, Antony J. PLoS ONE, Vol. 3, Issue 1 https://doi.org/10.1371/journal.pone.0001396	journal	January 2008
Genetic Linkage Map and Comparative Genome Analysis for the Atlantic Killifish (Fundulus heteroclitus) Waits, Eric R.; Martinson, John; Rinner, Brian Open Journal of Genetics, Vol. 06, Issue 01 https://doi.org/10.4236/ojgen.2016.61004	journal	January 2016
Evolution of homeobox genes: Evolution of homeobox genes Holland, Peter W. H. Wiley Interdisciplinary Reviews: Developmental Biology, Vol. 2, Issue 1 https://doi.org/10.1002/wdev.78	journal	September 2012
Ancyrocephalidae (Monogenea) of Lake Tanganyika: III: Cichlidogyrus infecting the world’s biggest cichlid and the non-endemic tribes Haplochromini, Oreochromini and Tylochromini (Teleostei, Cichlidae) Muterezi Bukinga, Fidel; Vanhove, Maarten P. M.; Van Steenberge, Maarten Parasitology Research, Vol. 111, Issue 5 https://doi.org/10.1007/s00436-012-3052-1	journal	September 2012
Evolution of Hox Gene Clusters in Gnathostomes: Insights from a Survey of a Shark (Scyliorhinus canicula) Transcriptome Oulion, S.; Debiais-Thibaud, M.; d'Aubenton-Carafa, Y. Molecular Biology and Evolution, Vol. 27, Issue 12 https://doi.org/10.1093/molbev/msq172	journal	July 2010
Heritability and adaptive significance of the number of egg-dummies in the cichlid fish Astatotilapia burtoni Lehtonen, Topi K.; Meyer, Axel Proceedings of the Royal Society B: Biological Sciences, Vol. 278, Issue 1716 https://doi.org/10.1098/rspb.2010.2483	journal	January 2011
Genomic atolls of differentiation in coral reef fishes ( Hypoplectrus spp., Serranidae ) Puebla, O.; Bermingham, E.; McMillan, W. O. Molecular Ecology, Vol. 23, Issue 21 https://doi.org/10.1111/mec.12926	journal	October 2014
Phylogeny of salmonids (salmoniformes: Salmonidae) and its molecular dating: Analysis of mtDNA data Shedko, S. V.; Miroshnichenko, I. L.; Nemkova, G. A. Russian Journal of Genetics, Vol. 49, Issue 6 https://doi.org/10.1134/s1022795413060112	journal	June 2013
Rapid genomic DNA variation in newly hybridized carp lineages derived from Cyprinus carpio (♀) × Megalobrama amblycephala (♂) Luo, Kaikun; Wang, Shi; Fu, Yeqing BMC Genetics, Vol. 20, Issue 1 https://doi.org/10.1186/s12863-019-0784-2	journal	November 2019
Zebrafish hoxd4a Acts Upstream of meis1.1 to Direct Vasculogenesis, Angiogenesis and Hematopoiesis Amali, Aseervatham Anusha; Sie, Lawrence; Winkler, Christoph PLoS ONE, Vol. 8, Issue 3 https://doi.org/10.1371/journal.pone.0058857	journal	March 2013
Rapid genomic DNA variation in newly hybridized carp lineages derived from Cyprinus carpio (♀) × Megalobrama amblycephala (♂) Luo, Kaikun; Wang, Shi; Fu, Yeqing https://doi.org/10.21203/rs.2.16098/v1	posted_content	November 2019

Similar Records

An Independent Genome Duplication Inferred from Hox Paralogs in the American Paddlefish—A Representative Basal Ray-Finned Fish and Important Comparative Reference

Journal Article · Sat Dec 31 19:00:00 EST 2011 · Genome Biology and Evolution · OSTI ID:1625329

Evolutionary conservation of regulatory elements in vertebrate HOX gene clusters

Journal Article · Tue Dec 30 23:00:00 EST 2003 · Genome Research · OSTI ID:833695

Consequences of Lineage-Specific Gene Loss on Functional Evolution of Surviving Paralogs: ALDH1A and Retinoic Acid Signaling in Vertebrate Genomes

Journal Article · Thu May 28 20:00:00 EDT 2009 · PLoS Genetics · OSTI ID:1627275

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Biotechnology & Applied Microbiology
Genetics & Heredity
Haplochromine Cichlid
HoxDa Cluster
Paralogous Cluster
Posterior Gene
Takifugu Rubripes

Comparative phylogenomic analyses of teleost fish Hox gene clusters: lessons from the cichlid fish Astatotilapia burtoni

Citation Formats

References (95)

Cited By (19)

Similar Records

Related Subjects