Skip to main content
U.S. Department of Energy
Office of Scientific and Technical Information

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

Journal Article · · BMC Genomics
 [1];  [2];  [2];  [3]
  1. Univ. of Konstanz (Germany); DOE/OSTI
  2. DOE Joint Genome Inst. and Lawrence Berkeley National Lab. (LBNL), and Univ. of California, Berkeley, CA (United States)
  3. 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.

Research Organization:
USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); Lawrence Berkeley National Laboratory (LBNL), 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 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 journal May 2005
Phylogenetic Timing of the Fish-Specific Genome Duplication Correlates with the Diversification of Teleost Fish journal August 2004
Novel Relationships Among Ten Fish Model Species Revealed Based on a Phylogenomic Analysis Using ESTs journal May 2006
Developmental expression of the amphioxus Tbx1/10 gene illuminates the evolution of vertebrate branchial arches and sclerotome journal September 2004
Molecular and biological characterization of an isolate of the potyvirus passiflora virus Y naturally infecting soybean (Glycine max) in Brazil journal September 2022
Organization and base composition of tilapia Hox genes: implications for the evolution of Hox clusters in fish journal February 2005
Mitochondrial molecular clocks and the origin of the major Otocephalan clades (Pisces: Teleostei): A new insight journal March 2006
Novel evolutionary relationship among four fish model systems journal September 2004
Hox clusters as models for vertebrate genome evolution journal August 2005
Genome duplication and the origin of angiosperms journal November 2005
Possible Significance of Duplication in Evolution book January 1951
Potential Protection by Cyclosporin Against Glucocorticoid Effects on bone journal December 1989
Genome duplication, divergent resolution and speciation journal June 2001
Transcription regulation and animal diversity journal July 2003
Hox cluster disintegration with persistent anteroposterior order of expression in Oikopleura dioica journal September 2004
Organization of the Fugu rubripes Hox clusters: evidence for continuing evolution of vertebrate Hox complexes journal May 1997
The zebrafish hoxDb cluster has been reduced to a single microRNA journal June 2006
Homozygous HOXA1 mutations disrupt human brainstem, inner ear, cardiovascular and cognitive development journal September 2005
The amphioxus Hox cluster: deuterostome posterior flexibility and Hox14 journal September 2000
Hox gene clusters in the Indonesian coelacanth, Latimeria menadoensis journal January 2003
Ciona intestinalis Hox gene cluster: Its dispersed structure and residual colinear expression in development journal October 2004
Regulatory gene networks and the properties of the developmental process journal February 2003
Breakup of a homeobox cluster after genome duplication in teleosts journal June 2006
Highly conserved syntenic blocks at the vertebrate Hox loci and conserved regulatory elements within and outside Hox gene clusters journal April 2006
VISTA : visualizing global DNA sequence alignments of arbitrary length journal November 2000
A Detailed Linkage Map of Medaka, Oryzias latipes: Comparative Genomics and Genome Evolution journal April 2000
Fugu Genome Analysis Provides Evidence for a Whole-Genome Duplication Early During the Evolution of Ray-Finned Fishes journal June 2004
The “Fish-Specific” Hox Cluster Duplication Is Coincident with the Origin of Teleosts journal September 2005
Asymmetric Evolution in Two Fish-Specifically Duplicated Receptor Tyrosine Kinase Paralogons Involved in Teleost Coloration 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 journal December 2000
Bichir HoxA Cluster Sequence Reveals Surprising Trends in Ray-Finned Fish Genomic Evolution journal December 2003
Developmental Roles of Pufferfish Hox Clusters and Genome Evolution in Ray-Fin Fish journal December 2003
Conservation of regulatory sequences and gene expression patterns in the disintegrating Drosophila Hox gene complex journal April 2005
The Human Hox-bearing Chromosome Regions Did Arise by Block or Chromosome (or Even Genome) Duplications journal December 2002
LAGAN and Multi-LAGAN: Efficient Tools for Large-Scale Multiple Alignment of Genomic DNA journal March 2003
Altered Growth and Branching Patterns in Synpolydactyly Caused by Mutations in HOXD13 journal April 1996
Zebrafish hox Clusters and Vertebrate Genome Evolution journal November 1998
Many genes in fish have species-specific asymmetric rates of molecular evolution journal February 2006
Analysis of Hox gene expression in the chick limb bud journal May 1996
Knockdown of duplicated zebrafish hoxb1 genes reveals distinct roles in hindbrain patterning and a novel mechanism of duplicate gene retention journal May 2002
Evolutionary Plasticity of Vertebrate Hox Genes journal August 2004
From 2R to 3R: evidence for a fish-specific genome duplication (FSGD) journal January 2005
Exclusion of repetitive DNA elements from gnathostomeHox clusters 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 book January 1970
The species flocks of East African cichlid fishes: recent advances in molecular phylogenetics and population genetics journal April 2004
Teleost HoxD and HoxA genes: comparison with tetrapods and functional evolution of the HOXD complex journal January 1996
Teleostean Monophyly book January 1996
Possible Significance of Duplication in Evolution book January 1951
Genome duplication, divergent resolution and speciation journal June 2001
Speciation in nature: the threespine stickleback model systems 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 journal December 1999
Gen(om)e duplications in the evolution of early vertebrates journal December 1996
Major patterns of higher teleostean phylogenies: a new perspective based on 100 complete mitochondrial DNA sequences journal January 2003
Hox gene evolution in nematodes: novelty conserved journal December 2003
Organization and structure of hox gene loci in medaka genome and comparison with those of pufferfish and zebrafish genomes journal March 2006
Conserved co-regulation and promoter sharing of hoxb3a and hoxb4a in zebrafish journal September 2006
Surveying phylogenetic footprints in large gene clusters: applications to Hox cluster duplications journal May 2004
Mitogenomic evidence for the monophyly of elopomorph fishes (Teleostei) and the evolutionary origin of the leptocephalus larva journal July 2004
A PCR survey for posterior Hox genes in amphibians journal February 2006
More genes in vertebrates? journal January 2003
A gene complex controlling segmentation in Drosophila journal December 1978
Archetypal organization of the amphioxus Hox gene cluster journal August 1994
Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events journal March 2003
Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae journal March 2004
Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype journal October 2004
Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia journal November 2006
Mutation of HOXA13 in hand-foot-genital syndrome journal February 1997
Gene regulatory network growth by duplication journal April 2004
Major events in the genome evolution of vertebrates: Paranome age and size differ considerably between ray-finned fishes and land vertebrates journal February 2004
Modeling gene and genome duplications in eukaryotes journal March 2005
Molecular evolution of the HoxA cluster in the three major gnathostome lineages journal April 2002
A Simple, Fast, and Accurate Algorithm to Estimate Large Phylogenies by Maximum Likelihood journal October 2003
MRBAYES: Bayesian inference of phylogenetic trees journal August 2001
Divergence of Conserved Non-Coding Sequences: Rate Estimates and Relative Rate Tests journal July 2004
Subfunctionalization of Expression and Peptide Domains Following the Ancient Duplication of the Proopiomelanocortin Gene in Teleost Fishes journal August 2005
Gene Loss and Evolutionary Rates Following Whole-Genome Duplication in Teleost Fishes journal June 2006
The human HOX gene family 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 journal March 2003
Evolutionary Conservation of Regulatory Elements in Vertebrate Hox Gene Clusters journal May 2003
Whole-Genome Shotgun Assembly and Analysis of the Genome of Fugu rubripes journal July 2002
Origin of the Superflock of Cichlid Fishes from Lake Victoria, East Africa journal April 2003
Murine Developmental Control Genes journal July 1990
Out of Tanganyika: Genesis, explosive speciation, key-innovations and phylogeography of the haplochromine cichlid fishes journal January 2005
Extreme conservation of noncoding DNA near HoxD complex of vertebrates journal October 2004
The gain and loss of genes during 600 million years of vertebrate evolution journal January 2006
Knockdown of the complete Hox paralogous group 1 leads to dramatic hindbrain and neural crest defects journal June 2005
Evolution at Two Levels: On Genes and Form journal July 2005
Two Rounds of Whole Genome Duplication in the Ancestral Vertebrate journal September 2005
Genome Duplications and Accelerated Evolution of Hox Genes and Cluster Architecture in Teleost Fishes1 journal June 2001

Cited By (19)

Hox cluster duplication in the basal teleost Hiodon alosoides (Osteoglossomorpha) journal February 2009
Unravelling paralogous gene expression dynamics during three-spined stickleback embryogenesis journal March 2019
Enigmatic Orthology Relationships between Hox Clusters of the African Butterfly Fish and Other Teleosts Following Ancient Whole-Genome Duplication journal June 2014
SynBlast: Assisting the analysis of conserved synteny information journal August 2008
Sequence analyses of the distal-less homeobox gene family in East African cichlid fishes reveal signatures of positive selection journal January 2013
Genome-wide identification, characterization, and expression analysis of lineage-specific genes within zebrafish journal January 2013
Identification of prohormones and pituitary neuropeptides in the African cichlid, Astatotilapia burtoni journal August 2016
The genome of the largest bony fish, ocean sunfish (Mola mola), provides insights into its fast growth rate journal September 2016
MiR-10 Represses HoxB1a and HoxB3a in Zebrafish journal January 2008
Genetic Linkage Map and Comparative Genome Analysis for the Atlantic Killifish (Fundulus heteroclitus) journal January 2016
Evolution of homeobox genes: Evolution of homeobox genes 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) journal September 2012
Evolution of Hox Gene Clusters in Gnathostomes: Insights from a Survey of a Shark (Scyliorhinus canicula) Transcriptome journal July 2010
Heritability and adaptive significance of the number of egg-dummies in the cichlid fish Astatotilapia burtoni journal January 2011
Genomic atolls of differentiation in coral reef fishes ( Hypoplectrus spp., Serranidae ) journal October 2014
Phylogeny of salmonids (salmoniformes: Salmonidae) and its molecular dating: Analysis of mtDNA data journal June 2013
Rapid genomic DNA variation in newly hybridized carp lineages derived from Cyprinus carpio (♀) × Megalobrama amblycephala (♂) journal November 2019
Zebrafish hoxd4a Acts Upstream of meis1.1 to Direct Vasculogenesis, Angiogenesis and Hematopoiesis journal March 2013
Rapid genomic DNA variation in newly hybridized carp lineages derived from Cyprinus carpio (♀) × Megalobrama amblycephala (♂) posted_content November 2019