hox gene expression predicts tetrapod-like axial regionalization in the skate, Leucoraja erinacea

Abstract

The axial skeleton of tetrapods is organized into distinct anteroposterior regions of the vertebral column (cervical, trunk, sacral, and caudal), and transitions between these regions are determined by colinear anterior expression boundaries of Hox5/6, -9, -10, and -11 paralogy group genes within embryonic paraxial mesoderm. Fishes, conversely, exhibit little in the way of discrete axial regionalization, and this has led to scenarios of an origin of Hox-mediated axial skeletal complexity with the evolutionary transition to land in tetrapods. Here, combining geometric morphometric analysis of vertebral column morphology with cell lineage tracing of hox gene expression boundaries in developing embryos, we recover evidence of at least five distinct regions in the vertebral skeleton of a cartilaginous fish, the little skate (Leucoraja erinacea). We find that skate embryos exhibit tetrapod-like anteroposterior nesting of hox gene expression in their paraxial mesoderm, and we show that anterior expression boundaries of hox5/6, hox9, hox10, and hox11 paralogy group genes predict regional transitions in the differentiated skate axial skeleton. Our findings suggest that hox-based axial skeletal regionalization did not originate with tetrapods but rather has a much deeper evolutionary history than was previously appreciated.

Little skate genome provides insights into genetic programs essential for limb-based locomotion

“…Coding sequences in our assembled Hoxa cluster aligned well with the fully sequenced BAC clone ( Figure 1—figure supplement 5 ), highlighting the reliability of the new assembly. We observed complete loss of Hoxc cluster in the little skate genome which was also shown in the thorny skate genome ( King et al, 2011 ; Rhie et al, 2021 ; Criswell et al, 2021 ) and relatively high repeat contents nearby genomic regions in the scaffold41 (s41), which contains the largest number of the Hoxc neighbor genes ( Figure 1—figure supplement 6 ). Although a residual fragment of Hoxc cluster was reported in the shark genomes ( Hara et al, 2018 ), cloudy cat shark, bamboo shark, and whale shark genomes are not visualized here due to an absence of gene annotation files.…”

“…S5), highlighting the reliability of the new assembly. We observed complete loss of HoxC cluster in the little skate genome which was also shown in the thorny skate genome 6,13,22 and relatively high repeat contents nearby genomic regions in the scaffold41 (s41), which contains the largest number of the HoxC neighbor genes (Fig. S6).…”

Body-axis organization in tetrapods: a model-system to disentangle the developmental origins of convergent evolution in deep time

“…The axial skeletons of fishes are simply subdivided into trunk and tail regions [ 28 , 29 ], and the association of this regionalization with Hox -expression in Actinopterygii is well known [ 30 ]. Recent findings on the Hox -code expression and regionalization in the cartilaginous fish, Leucoraja erinacea [ 31 ] and in early ray-finned fish [ 32 ] predict an origin of Hox -based vertebral regionalization at the common ancestor of jawed vertebrates. Finally, vertebral lengths inform about differential post-patterning growth of somites among axial regions, which determines the relative lengths of vertebrae within regions.…”

Comparative Proteome Analysis of Four Stages of Spermatogenesis in the Small-Spotted Catshark (Scyliorhinus canicula), Using High-Resolution NanoLC-ESI-MS/MS

“…The small-spotted catshark belongs to the cartilaginous fishes (Chondrichthyes) comprising the Holocephalans (Chimaeras) and the Elasmobranchs (Sharks, rays, and skates), which occupy a unique phylogenetic position as a result of their divergence from Osteichthyes (Bony Vertebrates) estimated to have occurred around 450-million years ago (Mya) . Due to their key position near the base of phylogeny, the Chondrichthyans are of interest for the evolutionary study of various biological processes or systems such as the adaptive immune system, , various developmental processes, , or the endoskeleton evolution . Among the recent advances in the whole genome sequencing of several species, those concerning the elephant shark Callorhinchus milii are the first to have opened new vistas regarding the molecular underpinnings of various cellular processes in Chondrichthyans. − The genomes of sharks are characterized by reduced molecular evolution rates and their relatively large size, from a 974 Mb length for C.…”