Reconstruction of ancient homeobox gene linkages inferred from a new high-quality assembly of the Hong Kong oyster (Magallana hongkongensis) genome

Abstract

Background Homeobox-containing genes encode crucial transcription factors involved in animal, plant and fungal development, and changes to homeobox genes have been linked to the evolution of novel body plans and morphologies. In animals, some homeobox genes are clustered together in the genome, either as remnants from ancestral genomic arrangements, or due to coordinated gene regulation. Consequently, analyses of homeobox gene organization across animal phylogeny provide important insights into the evolution of genome organization and developmental gene control, and their interaction. However, homeobox gene organization remains to be fully elucidated in several key animal ancestors, including those of molluscs, lophotrochozoans and bilaterians. Results Here, we present a high-quality chromosome-level genome assembly of the Hong Kong oyster, Magallana hongkongensis (2n = 20), for which 93.2% of the genomic sequences are contained on 10 pseudomolecules (~ 758 Mb, scaffold N50 = 72.3 Mb). Our genome assembly was scaffolded using Hi-C reads, facilitating a larger scaffold size compared to the recently published M. hongkongensis genome of Peng et al. (Mol Ecol Resources, 2020), which was scaffolded using the Crassostrea gigas assembly. A total of 46,963 predicted gene models (45,308 protein coding genes) were incorporated in our genome, and genome completeness estimated by BUSCO was 94.6%. Homeobox gene linkages were analysed in detail relative to available data for other mollusc lineages. Conclusions The analyses performed in this study and the accompanying genome sequence provide important genetic resources for this economically and culturally valuable oyster species, and offer a platform to improve understanding of animal biology and evolution more generally. Transposable element content is comparable to that found in other mollusc species, contrary to the conclusion of another recent analysis. Also, our chromosome-level assembly allows the inference of ancient gene linkages (synteny) for the homeobox-containing genes, even though a number of the homeobox gene clusters, like the Hox/ParaHox clusters, are undergoing dispersal in molluscs such as this oyster.

The Crown Pearl: a draft genome assembly of the European freshwater pearl musselMargaritifera margaritifera(Linnaeus, 1758)

“…Given the disparate body plans in molluscan classes, the study of Hox cluster composition, organization and gene expression has practically become a standard in Mollusca genome assembly studies. 60 , 75–88 Homeobox genes are divided into four classes, of which the Antennapedia (ANTP)-class (Hox, ParaHox, NK, Mega-homeobox, SuperHox) is the best studied, particularly the Hox and ParaHox clusters. 60 , 74 , 84 The number of genes from these two clusters is relatively well conserved across Lophotrochozoa, with Hox cluster being composed of 11 genes (3 anterior, 6 central, and 2 posterior) and ParaHox cluster composed of 3 genes.…”

“… 60 The fact that the remaining genes were scattered in the different scaffolds is likely a consequence of the low contiguity of the genome assembly since the distances between Bivalvia Hox genes within a cluster can be as high as 9.9 Mb. 60 Conversely, three Hox and one ParaHox genes were found in the M. margaritifera transcriptome assembly and nine Hox and one ParaHox gene were found in M. nervosa genome assembly ( Supplementary Table S6 ). Finally, to further validate the identity of the identified Hox and ParaHox genes, a phylogenetic analysis using the homeodomains (encoded 60–63 amino acid domain) of several Mollusca species was conducted ( Fig.…”

“…For phylogenetic assessment of Hox and Parahox genes, amino acid sequences of homeodomain of the genes from M. margaritifera and M. nervosa , were aligned with other Mollusca orthologous. 59 , 60 Molecular evolutionary models and Maximum-Likelihood phylogenetic analyses were obtained using IQ-TREE v.1.6.12 . 53 , 61 …”

“…Sequences used include the Hox and ParaHox homeodomains obtained in this study as well as other Mollusca homeodomain sequences retrieved from Refs. 59 , 60 …”

Non-collinear Hox gene expression in bivalves and the evolution of morphological novelties in mollusks

“…The non-regionalized anterior-posterior distribution of these morphological traits and the conserved mode of www.nature.com/scientificreports/ staggered Hox gene expression coincides with the situation in the polychaete annelid Platynereis which, despite significant differences with the polyplacophoran body plan such as segmentation and ganglionated nerve cords, likewise shows a largely evenly distributed set of organ systems along its longitudinal axis as well as staggered 1,66 , animal schemes modified after 67 . Data from 16,18,19,35,39,57,68 www.nature.com/scientificreports/ expression of Hox genes 54 . From this common scheme, conchiferan molluscs have decoupled Hox gene expression from their original position along the anterior-posterior axis in various ways, depending on the degree of body regionalization.…”