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

Abstract

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 severalmore » 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.« less

Authors:
 [1];  [2];  [2];  [1]
+ Show Author Affiliations
  1. Univ. of Konstanz (Germany)
  2. DOE Joint Genome Inst. and Lawrence Berkeley National Lab. (LBNL), and Univ. of California, Berkeley, CA (United States)
Publication Date:
Research Org.:
USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); University of California, Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
OSTI Identifier:
1626455
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
BMC Genomics
Additional Journal Information:
Journal Volume: 8; Journal Issue: 1; Journal ID: ISSN 1471-2164
Publisher:
Springer
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Biotechnology & Applied Microbiology; Genetics & Heredity; Takifugu Rubripes; Haplochromine Cichlid; HoxDa Cluster; Paralogous Cluster; Posterior Gene

Citation Formats

Hoegg, Simone, Boore, Jeffrey L., Kuehl, Jennifer V., and Meyer, Axel. Comparative phylogenomic analyses of teleost fish Hox gene clusters: lessons from the cichlid fish Astatotilapia burtoni. United States: N. p., 2007. Web. doi:10.1186/1471-2164-8-317.
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Hoegg, Simone, Boore, Jeffrey L., Kuehl, Jennifer V., & Meyer, Axel. Comparative phylogenomic analyses of teleost fish Hox gene clusters: lessons from the cichlid fish Astatotilapia burtoni. United States. https://doi.org/10.1186/1471-2164-8-317
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Hoegg, Simone, Boore, Jeffrey L., Kuehl, Jennifer V., and Meyer, Axel. Mon . "Comparative phylogenomic analyses of teleost fish Hox gene clusters: lessons from the cichlid fish Astatotilapia burtoni". United States. https://doi.org/10.1186/1471-2164-8-317. https://www.osti.gov/servlets/purl/1626455.
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@article{osti_1626455,
title = {Comparative phylogenomic analyses of teleost fish Hox gene clusters: lessons from the cichlid fish Astatotilapia burtoni},
author = {Hoegg, Simone and Boore, Jeffrey L. and Kuehl, Jennifer V. and Meyer, Axel},
abstractNote = {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.},
doi = {10.1186/1471-2164-8-317},
journal = {BMC Genomics},
number = 1,
volume = 8,
place = {United States},
year = {Mon Sep 10 00:00:00 EDT 2007},
month = {Mon Sep 10 00:00:00 EDT 2007}
}
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Regulatory gene networks and the properties of the developmental process
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Breakup of a homeobox cluster after genome duplication in teleosts
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Highly conserved syntenic blocks at the vertebrate Hox loci and conserved regulatory elements within and outside Hox gene clusters
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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

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The “Fish-Specific” Hox Cluster Duplication Is Coincident with the Origin of Teleosts
journal, September 2005

  • Crow, Karen D.; Stadler, Peter F.; Lynch, Vincent J.
  • Molecular Biology and Evolution, Vol. 23, Issue 1
  • DOI: 10.1093/molbev/msj020

Asymmetric Evolution in Two Fish-Specifically Duplicated Receptor Tyrosine Kinase Paralogons Involved in Teleost Coloration
journal, March 2006

  • Braasch, Ingo; Salzburger, Walter; Meyer, Axel
  • Molecular Biology and Evolution, Vol. 23, Issue 6
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Comparative genomics provides evidence for an ancient genome duplication event in fish
journal, October 2001

  • Taylor, John S.; Van de Peer, Yves; Braasch, Ingo
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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

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

  • McClintock, James M.; Kheirbek, Mazen A.; Prince, Victoria E.
  • Development, Vol. 129, Issue 10
  • DOI: 10.1242/dev.129.10.2339

Evolutionary Plasticity of Vertebrate Hox Genes
journal, August 2004

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    Works referencing / citing this record:

    The genome of the largest bony fish, ocean sunfish (Mola mola), provides insights into its fast growth rate
    journal, September 2016

    Enigmatic Orthology Relationships between Hox Clusters of the African Butterfly Fish and Other Teleosts Following Ancient Whole-Genome Duplication
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    • Martin, Kyle J.; Holland, Peter W. H.
    • Molecular Biology and Evolution, Vol. 31, Issue 10
    • DOI: 10.1093/molbev/msu202

    Evolution of Hox Gene Clusters in Gnathostomes: Insights from a Survey of a Shark (Scyliorhinus canicula) Transcriptome
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    • Oulion, S.; Debiais-Thibaud, M.; d'Aubenton-Carafa, Y.
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    • DOI: 10.1093/molbev/msq172

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    • Proceedings of the Royal Society B: Biological Sciences, Vol. 278, Issue 1716
    • DOI: 10.1098/rspb.2010.2483

    Evolution of homeobox genes: Evolution of homeobox genes
    journal, September 2012

    • Holland, Peter W. H.
    • Wiley Interdisciplinary Reviews: Developmental Biology, Vol. 2, Issue 1
    • DOI: 10.1002/wdev.78

    Phylogeny of salmonids (salmoniformes: Salmonidae) and its molecular dating: Analysis of mtDNA data
    journal, June 2013

    • Shedko, S. V.; Miroshnichenko, I. L.; Nemkova, G. A.
    • Russian Journal of Genetics, Vol. 49, Issue 6
    • DOI: 10.1134/s1022795413060112

    Zebrafish hoxd4a Acts Upstream of meis1.1 to Direct Vasculogenesis, Angiogenesis and Hematopoiesis
    journal, March 2013

    Hox cluster duplication in the basal teleost Hiodon alosoides (Osteoglossomorpha)
    journal, February 2009

    • Chambers, Karen E.; McDaniell, Ryan; Raincrow, Jeremy D.
    • Theory in Biosciences, Vol. 128, Issue 2
    • DOI: 10.1007/s12064-009-0056-1

    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

    • Martin, Kyle J.; Holland, Peter W. H.
    • Molecular Biology and Evolution, Vol. 31, Issue 10
    • DOI: 10.1093/molbev/msu202

    SynBlast: Assisting the analysis of conserved synteny information
    journal, August 2008

    • Lehmann, Jörg; Stadler, Peter F.; Prohaska, Sonja J.
    • BMC Bioinformatics, Vol. 9, Issue 1
    • DOI: 10.1186/1471-2105-9-351

    Sequence analyses of the distal-less homeobox gene family in East African cichlid fishes reveal signatures of positive selection
    journal, January 2013

    • Diepeveen, Eveline T.; Kim, Fabienne D.; Salzburger, Walter
    • BMC Evolutionary Biology, Vol. 13, Issue 1
    • DOI: 10.1186/1471-2148-13-153

    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 (<i>Fundulus heteroclitus</i>)
    journal, January 2016

    • Waits, Eric R.; Martinson, John; Rinner, Brian
    • Open Journal of Genetics, Vol. 06, Issue 01
    • DOI: 10.4236/ojgen.2016.61004
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