Abstract
Homeobox genes are key toolkit genes that regulate the development of metazoans and changes in their regulation and copy number have contributed to the evolution of phenotypic diversity. We recently identified a whole genome duplication (WGD) event that occurred in an ancestor of spiders and scorpions (Arachnopulmonata), and that many homeobox genes, including two Hox clusters, appear to have been retained in arachnopulmonates. To better understand the consequences of this ancient WGD and the evolution of arachnid homeobox genes, we have characterized and compared the homeobox repertoires in a range of arachnids. We found that many families and clusters of these genes are duplicated in all studied arachnopulmonates (Parasteatoda tepidariorum, Pholcus phalangioides, Centruroides sculpturatus, and Mesobuthus martensii) compared with nonarachnopulmonate arachnids (Phalangium opilio, Neobisium carcinoides, Hesperochernes sp., and Ixodes scapularis). To assess divergence in the roles of homeobox ohnologs, we analyzed the expression of P. tepidariorum homeobox genes during embryogenesis and found pervasive changes in the level and timing of their expression. Furthermore, we compared the spatial expression of a subset of P. tepidariorum ohnologs with their single copy orthologs in P. opilio embryos. We found evidence for likely subfunctionlization and neofunctionalization of these genes in the spider. Overall our results show a high level of retention of homeobox genes in spiders and scorpions post-WGD, which is likely to have made a major contribution to their developmental evolution and diversification through pervasive subfunctionlization and neofunctionalization, and paralleling the outcomes of WGD in vertebrates.
Highlights
Developmental programs precisely orchestrate proliferation and differentiation to build multicellular organisms
Many of the key regulatory factors and pathways utilized in development are conserved between species like the Wnt and Delta/ Notch signaling pathways and transcription factors (TF) such as those encoded by the homeobox genes (Reviewed by Carroll et al 2005; Rokas 2008)
Our work shows that whole genome duplication (WGD) greatly expanded the repertoire of homeobox genes in arachnopulmonates and that this contributed to diversification in their developmental gene regulatory networks and may have contributed to evolutionary innovations in these animals as has been postulated in other animal lineages (Van de Peer et al 2009; Huminiecki and Conant 2012)
Summary
Developmental programs precisely orchestrate proliferation and differentiation to build multicellular organisms. The homeobox genes encode a large superclass of TFs (Garcia-Fernandez 2005; Hoegg and Meyer 2005; PascualAnaya et al 2012; Holland 2015; Ferrier 2016). They are characterized by encoding a homeodomain, which is usually 60 amino acids in length and folds to form a structure with three a-helices and an N-terminal domain (Ortiz-Lombardia et al 2017).
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