Developmental expression of homeobox genes in the ctenophore Mnemiopsis leidyi

Abstract

Homeobox genes are a large family of genes that encode helix-turn-helix transcription factors that play fundamental roles in such developmental processes including body axis formation and cell specification. They have been found in a wide variety of organisms, from fungi to plants and animals, with some classes being specific to the Metazoa. While it was once thought that organismal complexity was tied to gene complexity, sequencing of genomes from a cnidarian, poriferan, and placozoan have shown no clear correlation. However, little attention has been paid to ctenophores, another early branching taxon. Ctenophores are mostly pelagic marine animals, with complex morphological features, so understanding the gene content and expression of this nonbilaterian phylum is of key interest to evolutionary biology. Expression information from developmental genes in ctenophores is sparse. In this study, we isolated seven homeobox genes from the ctenophore Mnemiopsis leidyi and examined their expression through development. Phylogenetic analyses of these genes placed four in the ANTP class and three in the PRD class. These are the first reported full-length PRD class genes, although our analyses could not place them into specific families. We have found that most of these homeobox genes begin expression at gastrulation, and their expression patterns suggest a possible role in patterning of the tentacle apparati and pharynx.

Early evolution of metazoan transcription factors

“…Basic helix-loop-helix (bHLH), Mef2, Fox, Sox, T-box, ETS, nuclear receptor, Rel/NF-kB, bZIP, Smad, and a diversity of homeobox-containing classes, including ANTP, Prd-like, Pax, POU, LIM-HD, Six, and TALE (Table 1), evolved before the divergence of sponges and eumetazoans ( Figure 1) [7 , 21 ,29-33, 34 ,35 ,36,37,38 ,39-41]. Ctenophores also possess representatives of many of these TF families and classes [42][43][44][45]46 ]; however, a comprehensive inventory of their TFs awaits whole genome sequence data.…”

Population genetics of the invasive ctenophore Mnemiopsis leidyi in Europe reveal source–sink dynamics and secondary dispersal to the Mediterranean Sea

“…Moreover, the basal phylogenetic position of the main phyla Cnidaria and Ctenophora (Giribet et al 2007, Hejnol et al 2009) has spurred considerable scientific interest in the fields of evolutionary and developmental research (Pang & Martindale 2008a, Lange et al 2010. However, the presence of, and underlying causes for, population structure, gene flow and population turnover in jellyfish are currently not well understood, but are of growing interest (Licandro et al 2010, Stopar et al 2010, Lee et al 2013.…”

Lim homeobox genes in the Ctenophore Mnemiopsis leidyi: the evolution of neural cell type specification

“…Previous studies have described other genes in different regions of the apical organ of Mnemiopsis, including the T-box genes Tbx2/3 and Brachyury [55], the homeobox genes Prd1 and Prd3 [56], the Wnt genes MlWnt6 and MlWntX [46], as well as the zinc fingers MlGli and MlGlis [57]. Histological and electron microscopic studies of the ctenophore apical organ have suggested it is a highly innervated sensory structure [58-71]; however, gene expression studies suggest that it is much more complex than previously thought.…”