Hox Gene Clusters of Early Vertebrates: Do They Serve As Reliable Markers for Genome Evolution?

Overview

Journal Genomics Proteomics Bioinformatics

Specialty Biology

Date 2011 Aug 2

PMID 21802046

Citations 6

Authors

Shigehiro Kuraku

Affiliations

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Abstract

Hox genes, responsible for regional specification along the anteroposterior axis in embryogenesis, are found as clusters in most eumetazoan genomes sequenced to date. Invertebrates possess a single Hox gene cluster with some exceptions of secondary cluster breakages, while osteichthyans (bony vertebrates) have multiple Hox clusters. In tetrapods, four Hox clusters, derived from the so-called two-round whole genome duplications (2R-WGDs), are observed. Overall, the number of Hox gene clusters has been regarded as a reliable marker of ploidy levels in animal genomes. In fact, this scheme also fits the situations in teleost fishes that experienced an additional WGD. In this review, I focus on cyclostomes and cartilaginous fishes as lineages that would fill the gap between invertebrates and osteichthyans. A recent study highlighted a possible loss of the HoxC cluster in the galeomorph shark lineage, while other aspects of cartilaginous fish Hox clusters usually mark their conserved nature. In contrast, existing resources suggest that the cyclostomes exhibit a different mode of Hox cluster organization. For this group of species, whose genomes could have differently responded to the 2R-WGDs from jawed vertebrates, therefore the number of Hox clusters may not serve as a good indicator of their ploidy level.

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References

Sakamoto K, Onimaru K, Munakata K, Suda N, Tamura M, Ochi H . Heterochronic shift in Hox-mediated activation of sonic hedgehog leads to morphological changes during fin development. PLoS One. 2009; 4(4):e5121. PMC: 2664896. DOI: 10.1371/journal.pone.0005121. View

Oulion S, Borday-Birraux V, Debiais-Thibaud M, Mazan S, Laurenti P, Casane D . Evolution of repeated structures along the body axis of jawed vertebrates, insights from the Scyliorhinus canicula Hox code. Evol Dev. 2011; 13(3):247-59. DOI: 10.1111/j.1525-142X.2011.00477.x. View

Duboule D . Temporal colinearity and the phylotypic progression: a basis for the stability of a vertebrate Bauplan and the evolution of morphologies through heterochrony. Dev Suppl. 1994; :135-42. View

Inoue J, Miya M, Lam K, Tay B, Danks J, Bell J . Evolutionary origin and phylogeny of the modern holocephalans (Chondrichthyes: Chimaeriformes): a mitogenomic perspective. Mol Biol Evol. 2010; 27(11):2576-86. DOI: 10.1093/molbev/msq147. View

Kuraku S, Kuratani S . Time scale for cyclostome evolution inferred with a phylogenetic diagnosis of hagfish and lamprey cDNA sequences. Zoolog Sci. 2007; 23(12):1053-64. DOI: 10.2108/zsj.23.1053. View

Lynch V, Wagner G . Multiple chromosomal rearrangements structured the ancestral vertebrate Hox-bearing protochromosomes. PLoS Genet. 2009; 5(1):e1000349. PMC: 2622764. DOI: 10.1371/journal.pgen.1000349. View

Hunt P, Whiting J, Nonchev S, Sham M, Marshall H, Graham A . The branchial Hox code and its implications for gene regulation, patterning of the nervous system and head evolution. Dev Suppl. 1991; Suppl 2:63-77. View

Coolen M, Menuet A, Chassoux D, Compagnucci C, Henry S, Leveque L . The Dogfish Scyliorhinus canicula: A Reference in Jawed Vertebrates. CSH Protoc. 2011; 2008:pdb.emo111. DOI: 10.1101/pdb.emo111. View

Freitas R, Zhang G, Cohn M . Evidence that mechanisms of fin development evolved in the midline of early vertebrates. Nature. 2006; 442(7106):1033-7. DOI: 10.1038/nature04984. View

10.

Ota K, Kuraku S, Kuratani S . Hagfish embryology with reference to the evolution of the neural crest. Nature. 2007; 446(7136):672-5. DOI: 10.1038/nature05633. View

11.

Takio Y, Kuraku S, Murakami Y, Pasqualetti M, Rijli F, Narita Y . Hox gene expression patterns in Lethenteron japonicum embryos--insights into the evolution of the vertebrate Hox code. Dev Biol. 2007; 308(2):606-20. DOI: 10.1016/j.ydbio.2007.05.009. View

12.

Sharman A, Holland P . Estimation of Hox gene cluster number in lampreys. Int J Dev Biol. 1998; 42(4):617-20. View

13.

Davis M, Dahn R, Shubin N . An autopodial-like pattern of Hox expression in the fins of a basal actinopterygian fish. Nature. 2007; 447(7143):473-6. DOI: 10.1038/nature05838. View

14.

Seo H, Edvardsen R, Maeland A, Bjordal M, Jensen M, Hansen A . Hox cluster disintegration with persistent anteroposterior order of expression in Oikopleura dioica. Nature. 2004; 431(7004):67-71. DOI: 10.1038/nature02709. View

15.

Kim C, Amemiya C, Bailey W, Kawasaki K, Mezey J, Miller W . Hox cluster genomics in the horn shark, Heterodontus francisci. Proc Natl Acad Sci U S A. 2000; 97(4):1655-60. PMC: 26491. DOI: 10.1073/pnas.030539697. View

16.

Ikuta T, Saiga H . Organization of Hox genes in ascidians: present, past, and future. Dev Dyn. 2005; 233(2):382-9. DOI: 10.1002/dvdy.20374. View

17.

Stadler P, Fried C, Prohaska S, Bailey W, Misof B, Ruddle F . Evidence for independent Hox gene duplications in the hagfish lineage: a PCR-based gene inventory of Eptatretus stoutii. Mol Phylogenet Evol. 2004; 32(3):686-94. DOI: 10.1016/j.ympev.2004.03.015. View

18.

Grapin-Botton A, Melton D . Endoderm development: from patterning to organogenesis. Trends Genet. 2000; 16(3):124-30. DOI: 10.1016/s0168-9525(99)01957-5. View

19.

Kuraku S . Palaeophylogenomics of the vertebrate ancestor--impact of hidden paralogy on hagfish and lamprey gene phylogeny. Integr Comp Biol. 2011; 50(1):124-9. DOI: 10.1093/icb/icq044. View

20.

Kuraku S, Meyer A, Kuratani S . Timing of genome duplications relative to the origin of the vertebrates: did cyclostomes diverge before or after?. Mol Biol Evol. 2008; 26(1):47-59. DOI: 10.1093/molbev/msn222. View