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The genesis and evolution of homeobox gene clusters

Nature Reviews Genetics volume 6, pages 881–892 (2005)Cite this article

Key Points

  • Hox, ParaHox and NK genes are related ANTP-class homeobox genes that are organized into chromosomal clusters in several metazoan lineages. Both Hox and ParaHox clusters are thought to have arisen by duplication and divergence from an ancient ProtoHox cluster that was present in an ancestral animal.

  • Phylogenetic and chromosomal reconstructions indicate that the Hox and ParaHox clusters, as well as other ANTP homeobox classes (Evx, Meox, Gbx, Mnx and En) originated after successive gene duplications and chromosomal breakages from a founder ProtoHox-like gene.

  • A large array of ANTP-class homeobox genes — the homeobox megacluster that includes the Hox, ParaHox and NK clusters — existed early in metazoan evolution. It contained up to 25 homeobox genes, and probably originated before the divergence of cnidarians and bilaterians.

  • An NK cluster of seven homeobox genes existed before the divergence of protostomes and deuterosomes. The organization of the cluster has been maintained largely intact in fruitflies and mosquitoes, but has been split into three in chordates.

  • Hox, ParaHox and NK cluster genes are preferentially expressed in ectodermal, endodermal and mesodermal derivatives, respectively. I speculate that the origin of the three gene clusters was related to the origin, patterning and diversification of the three bilaterian germ layers.

  • The above thesis implies that cnidarians are primitively bilaterian triploblasts; that these gene clusters have been evolving independently in the distinct clades; and that their present-day functions are a composite of ancestral and derived functions.

  • The selective constraint that has favoured the maintenance of homeobox gene clustering is probably the need for close gene linkage; this would enable sequential chromatin decondensation and thereby allow the temporal deployment of gene expression.

  • The linkage constraint is maintained for the Hox and ParaHox clusters in animals that have a slow mode of development, and for the NK cluster in insects. In the lineages for which the constraint has disappeared, the clusters tend to disintegrate by phylogenetic inertia.

Abstract

Once called the 'Rosetta stone' of developmental biology, the homeobox continues to fascinate both evolutionary and developmental biologists. The birth of the homeotic, or Hox, gene cluster, and its subsequent evolution, has been crucial in mediating the major transitions in metazoan body plan. Comparative genomics studies indicate that the more recently discovered ParaHox and NK clusters were linked to the Hox cluster early in evolution, and that together they constituted a 'megacluster' of homeobox genes that conspicuously contributed to body-plan evolution.

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Figure 1: Genesis and evolution of Hox and ParaHox clusters.
Figure 2: The NK cluster.
Figure 3: The homeobox megacluster.

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Acknowledgements

I am very grateful to P. Holland, J. Baguñà, C. Minguillón and the members of the Barcelona Evo-Devo group for passionate discussions. I especially thank G. Luke for allowing me to use and cite his Ph.D. Thesis, and R. Rycroft for checking the English. The author's research is funded by the Ministerio de Educación y Ciencia, Spain, by the Departament d'Universitats, Recerca i Societat de la Informació de la Generalitat de Catalunya (Distinció per la Promoció de la Recerca Universitaria), and by the European Community's 'Neurogenome' Human Potential Programme.

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  1. Departament de Genètica, Facultat de Biologia, Universitat de Barcelona, Avinguda Diagonal 645, Barcelona, 08028, España

    Jordi Garcia-Fernàndez

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DATABASES

Entrez Gene

ATNP

bap

Cdx

En

Evx

Gbx

Gsh

Ipf1

Meox

slou

tin

UBX

vnd

FURTHER INFORMATION

Expert Protein Analysis System (ExPASy)

FlyBase

GenBank

Human Genome Organization

Jordi Garcia's web page

Glossary

BILATERIANS

Members of the animal kingdom that have bilateral symmetry — the property of having two similar sides, with definite upper and lower surfaces, and anterior and posterior ends. They include acoelomorphs, protostomes and deuterostomes.

CNIDARIANS

Radially symmetrical animals that have sac-like bodies with only one opening. They include jellyfish, corals, hydra and anemones.

METAZOAN

A multicellular animal.

MACRO EVOLUTIONARY EVENTS

Evolutionary processess that occur above the species level; for example, the origin of phyla and changes in body-plan organization.

THROUGH-GUT

A gut that has two openings: a mouth and an anus.

TRIPLOBLASTIC

An animal that has three primary germ layers: the ectoderm, endoderm and mesoderm. Triploblasts include acoelomorphs, protostomes and deuterostomes.

CHORDATES

The members of a phylum of animals (the Chordata) that is characterized by the possession of a notochord. It includes urochordates (such as the ascidians), cephalochordates (amphioxus) and vertebrates.

PROTOSTOMES

One of the main groups of bilaterally symmetrical animals. The name derives from 'proto' (first) and 'stome' (mouth), because the first opening of the embryo (the blastopore) becomes the definitive mouth.

DEUTEROSTOMES

The second of the two main groups of bilaterally symmetrical animals. The name derives from 'deutero' (second) and 'stome' (mouth), which refers to the origin of the definitive mouth as an opening that is independent from the blastopore of the embryo.

AMPHIOXUS

The invertebrate that is most closely related to vertebrates.

FLUORESCENCE IN SITU HYBRIDIZATION

A technique in which a fluorescently labelled DNA probe is used to detect a particular chromosome or gene with the help of fluorescence microscopy.

DIPLOBLASTIC

An animal that has only two primary germ layers: the ectoderm and the endoderm. Diploblasts include the cnidarians, the ctenophores and — according to some authors — the placozoans and the poriferans.

CAMBRIAN EXPLOSION

The sudden appearance, about 520 million years ago, in the fossil record of many major groups (phyla) of bilaterian animals.

HEMICHORDATES

A phylum of deuterostome marine worms that comprise the enteropneust and pterobranchs.

PLANULA BLASTOPORE

The opening of the planuloid larva. A planula is the swimming larva of cnidarians. Its ciliated epidermis covers either a solid or a hollowed-out mass of endoderm cells. The blastopore will develop into the oral opening of the polyp.

NEOTENOUS

The term neoteny describes the retention of juvenile characteristics in the adult of an animal species.

PLACOZOANS

Simple balloon-like marine animals with a body cavity that is filled with pressurized fluid. They lack most organs and tissues, including a nervous system, They are either the simplest metazoans, or simplified forms of more complex animals. Only a single species (Trichoplax adhaerens) comprises the phylum Placozoa.

CHOANOCYTES

Flagellated cells that line the body cavity of a sponge and that are characterized by a collar of cytoplasm surrounding the flagellum. They are also called collar cells.

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Garcia-Fernàndez, J. The genesis and evolution of homeobox gene clusters. Nat Rev Genet 6, 881–892 (2005). https://doi.org/10.1038/nrg1723

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