Clustered brachiopod Hox genes are not expressed collinearly and are associated with lophotrochozoan novelties

Abstract

Hox genes are often clustered in animal genomes and exhibit spatial and/or temporal collinearity. It is generally believed that temporal collinearity is the major force preserving Hox clusters. However, studies combining genomic and gene expression analyses of Hox genes are scarce, particularly within Spiralia and Lophotrochozoa (e.g. mollusks, segmented worms, and flatworms). Here, we use two brachiopod species -Terebratalia transversa and Novocrania anomala-that respectively belong to the two major brachiopod lineages to characterize their Hox complement, the presence of a Hox cluster, and the temporal and spatial expression of their Hox genes.We demonstrate that the Hox complement consists of ten Hox genes in T. transversa (lab, pb, Hox3, dfd, scr, lox5, antp, lox4, post2 and post1) and nine in N. anomala (missing post1). Additionally, T. transversa has an ordered, split Hox cluster. Expression analyses reveal that Hox genes are neither temporally nor spatially collinear, and only the genes pb (in T. transversa), Hox3 and dfd (in both brachiopods) show staggered expression in the mesoderm. Remarkably, lab, scr, antp and post1 are associated with the development of the chaetae and shell-forming epithelium, as also observed in annelid chaetae and mollusk shell fields. This, together with the expression of Arx homeobox, supports the deep conservation of the molecular basis for chaetae formation and shell patterning in Lophotrochozoa. Our findings challenge the current evolutionary scenario that (temporal) collinearity is the major mechanism preserving Hox clusters, and suggest that Hox genes were involved in the evolution of lophotrochozoan novelties.

Orthrozanclus elongata n. sp. and the significance of sclerite-covered taxa for early trochozoan evolution

“…Sclerites – a likely inheritance from the ancestral lophotrochozoan 17,18,29,30 – have been assembled into scleritomes on multiple occasions: the scleritomes of the scaly-footed gastropods 31 and chrysopetalid annelids 32,33 , for example, represent independent innovations that are demonstrably unique to the respective clades 31 . Indeed, multiple groups incorporate both shell-like valves and mineralized plates into dorsal imbricating skeletons – witness machaeridians, Pelagiella and certain tommotiids, who have affinities with annelids, gastropods and brachiopods, respectively 34–37 .…”

Nemertean and phoronid genomes reveal lophotrochozoan evolution and the origin of bilaterian heads

“…We failed to find Scr and Antp in Phoronis. Given that Scr and Antp are expressed in the shell-forming epithelium in brachiopods 32 , possible gene loss of Scr and Antp in the phoronid lineage may contribute to their shell-less morphology. This may also imply that common lophophorate ancestors had either unmineralized (agglutinated) or mineralized shells that were lost secondarily in crown phoronids 33,34 .…”

Phylogenomic Synteny Network Analysis of MADS-Box Transcription Factor Genes Reveals Lineage-Specific Transpositions, Ancient Tandem Duplications, and Deep Positional Conservation

“…For example, the origin of morphological novelty has been linked to the duplication of key regulatory transcription factors in the case of the Hox genes in animals, but also the MADS-box genes in plants ( Alvarez-Buylla et al, 2000b;Airoldi and Davies, 2012;Soshnikova et al, 2013). However, gene clusters are frequently dispersed or "broken up" in certain lineages, like the Hox cluster in the genomes of octopus (Lemons and McGinnis, 2006;Duboule, 2007;Albertin et al, 2015) and brachiopods (Schiemann et al, 2017), and this dispersion contributes to divergent gene expression and morphological novelties.…”