Origin and evolution of ANTP-class homeobox genes

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Resumo

Genes of the ANTP class are known as evolutionary conserved and hierarchically high-level regulators of development. They are the most studied and the most numerous homeobox genes in animals. These genes encode homeodomain transcription factors and possess a set of unique features, such as clustering, colinearity, evolutionary conservation, and consistent involvement in various differentiation processes throughout the ontogeny of multicellular animals.

The first ANTP genes (from the NK subclass) appear in ctenophores and sponges, which is why the evolution of Metazoa from a common unicellular ancestor is often associated with the emergence of the ANTP class (Larroux et al., 2007; Moroz et al., 2014). Phylogenetic analysis of homeobox genes, conducted across a broad range of basal Metazoa taxa, has shown that ANTP genes from the Hox and ParaHox subclasses arose in the last common ancestor of Cnidaria and Bilateria. These new findings raise further questions. How does the evolution of these clusters correlate with the evolution of animals? What functions were acquired by the new genes, and which were inherited from ancestral NK genes? What changes in their regulation could have influenced the evolution of body plans in Metazoa? Is it even possible to answer these questions by studying modern multicellular organisms?

This review aims to address these and other questions regarding the evolution of ANTP gene clusters. Special attention is given to the concept of the “megacluster” — a hypothetical synteny that united all ANTP subclasses at the dawn of Metazoa evolution.

The decreasing cost of sequencing technologies offers some hope for answers, as it expands the range of model species available for study. The broader this range, the easier it becomes to identify universal and lineage-specific patterns of molecular and morphological evolution.

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Sobre autores

M. Kulakova

St. Petersburg State University

Autor responsável pela correspondência
Email: m.kulakowa@spbu.ru
Rússia, 199034, St. Petersburg, Old Peterhof, Oranienbaumskoye shosse 2

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2. Fig. 1. The structure of the homeodomain and classes of homeobox genes. (a) The DNA-binding domain of homeodomain proteins (homeodomain; HD) consists of 60 amino acid residues and is organized into three alpha-helices, one of which (3) enters the major groove of DNA and recognizes a short consensus. (b) Separate classes of homeobox genes. Many genes encode additional domains for binding to DNA (PAIRED, POU, Lim) or to partner proteins. Genes from the ANTP class interact with proteins from the TALE class via the hexapeptide motif Hex (based on Burglin, Affolter, 2016).

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3. Fig. 2. Scenario of sequential emergence of genes from the ANTP class. Cis-duplication of the ancestral factor Proto-ANTP led to the emergence and subsequent structural expansion of genes of the most ancient ANTP cluster - NK. The NK cluster was found in the sponge Amphimedon and one of its five genes (probably an ortholog of the Hox-associated gene Hex) already contains signs (signatures) of belonging to another subclass. At the next stage, ancestral genes of the ParaHox, Hox, Hox-linked (HoxL) and NK2 clusters arose sequentially or simultaneously. Animals in whose genomes there are traces of emerging new clusters have not been found, which may indicate a very rapid process of structural evolution. In modern cnidarians and bilaterians (Nephrozoa), ANTP genes are well recognized and fall into two large (SuperHox and NK) and two small (ParaHox, NK2) subclasses. Hox genes (EuHox), belonging to the SuperHox subclass, are the youngest ANTP genes. Vigorous structural evolution of Hox genes accompanied the emergence of bilaterians and their evolutionary radiation. The diagram does not indicate physical linkage of genes and does not show clade-specific paralogs from conserved families (according to Garcia-Fernàndez, 2005; Butts et al., 2008; Ferrier, 2016; Zimmermann et al., 2023).

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4. Fig. 3. ANTP gene clusters in annelids and lancelets. Four nearly identical syntenies in the genomes of protostomes and deuterostomes neither support nor reject the megacluster hypothesis. If such a cluster existed, it would have already broken up into subclusters (ParaHox, SuperHox, NK, and NK2) in the last common ancestor of Nephrozoa. Each subcluster acquired individual functions early in development. Gray arrows indicate breakpoints (after Hui et al., 2012; Ferrier, 2016).

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5. Fig. 4. Synteny of ANTP genes in cnidarians of the phyla Anthozoa and Medusozoa. A large number of translocations between clusters from different subclasses indicates their recent physical linkage at the level of a larger synteny - a megacluster or a large fragment thereof. In the Nematostella genome, ANTP clusters contain a small number of such rearrangements. In contrast, in scyphozoan jellyfish, the NK and SuperHox genes formed mixed syntenies that could have arisen during the period of the common SuperHox/NK cluster. The genes of the ParaHox cluster are isolated from the neighborhood with other ANTPs. They could not have been part of the megacluster or lost their connection with it earlier than the other ANTP subclusters (based on Nong et al., 2020; Zimmermann et al., 2023).

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