The Antennapedia-type homeobox genes have evolved from three precursors separated early in metazoan evolution.

Abstract

The developmental control genes containing an Antennapedia-type homeobox are clustered in insects andvertebrates. The evolution of these genes was studied by the construction ofevolutionary trees and by statistical geometry in sequence space. The comparative analysis of the homeobox sequences reveals the subdivision of the Antennapedia-type homeobox genes into three classes early in metazoan evolution. This observation suggests an important function of these genes even in the most primitive metazoans. Subsequent duplication events generated a cluster of at least five homeobox genes in the last common ancestor of insects and vertebrates. These genes later independently gave rise to the 13 groups of paralogous genes in vertebrates and to the 11 Antennapedia-type genes in the Drosophila complexes.The homeobox consists ofa 183-base-pair sequence encoding a trihelical DNA binding motif. This domain has been found in several genes in a wide variety ofeukaryotic organisms (for reviews see refs. 1 and 2). The protein products of some of the homeobox genes act as ubiquitous transcription factors, whereas most are involved in the control of embryonic development. In the fruit fly Drosophila as well as in the house mouse, the segment identity along the anteriorposterior axis of the embryo is specified by homeotic selector genes belonging to the Antennapedia-type of homeobox genes (reviewed in ref.3). Both in insects (HOM genes) and in vertebrates (Hox genes) these genes are located in clusters. The beetle Tribolium (4, 5) has its homeotic genes arranged in one complex (HOM-C), whereas Drosophila has them split into two complexes [Bithorax complex (BX-C) and Antennapedia complex (ANT-C)]. In mammals, the four clusters (Hox-1 to Hox-4) can be aligned according to sequence similarities of their genes, thus defining 13 groups of paralogous genes. Kappen et al. (6) have therefore suggested that cluster duplication events underlie the evolution of the vertebrate Hox genes. A closer examination of the homeobox gene clusters in insects and vertebrates revealed remarkable resemblances (7,8). The Drosophila HOM genes are arranged in a similar order on the chromosome as their vertebrate counterparts. Moreover, in both organisms, these genes exhibit a correlation between their expression boundaries and their position in the cluster: generally the further downstream (3') a gene is in its cluster, the more anterior its expression boundary is in the embryo (for reviews see refs. 9 and 10). A common ancestral cluster for insects and vertebrates therefore appears to be highly probable (7,8,11). Reports of a related homeobox gene cluster in the nematode Caenorhabditis (12) and ofAntennapedia-type homeobox genes in cnidarians (13, 14) support this hypothesis.To gain insight into the evolution of developmental control mechanisms, as well as the phylogenetic relationships between the metazoans, several studies of the evolution of the Antennapedia-type homeobox genes were done by comparative sequence analyses (1,6,11,(15)(16)(17). While...

HOX genes in the sepiolid squid Euprymna scolopes : Implications for the evolution of complex body plans

“…We have identified one anterior group gene, one ortholog of paralog group 3 (PG3), five central group genes, and two posterior group genes. Our data support the idea of a single putative Hox cluster in E. scolopes encoding a minimum of nine Hox paralogs, and support earlier hypotheses about the ancient origin of the Hox gene cluster (14,28). The presence of the diverged posterior group genes provides additional support for the Lophotrochozoan assemblage (29).…”

The duplication of the Hox gene clusters in teleost fishes*1

“…Hox genes code for transcription factors homologous to the genes of the Drosophila homeotic gene clusters [36,58]. They are involved in the development of vertebrate body plan characters [59] and are one of the best-studied gene families, see e.g.…”

Exclusion of repetitive DNA elements from gnathostome Hox clusters

“…They specify the identity of cells and tissues along the anterior-posterior body axis by means of a spatial-temporaly coordinated expression pattern. The homology of the vertebrate Hox genes with the genes in the Drosophila homeotic gene clusters was demonstrated already a decade ago (Akam, 1989;Schubert et al, 1993). In many species they are organized in tightly linked clusters although in some cases the clusters have been broken up, see Table 1.…”