Emergence of distinct syntenic density regimes is associated with early metazoan genomic transitions

Abstract

Background Animal genomes are strikingly conserved in terms of local gene order (microsynteny). While some of these microsyntenies have been shown to be coregulated or to form gene regulatory blocks, the diversity of their genomic and regulatory properties across the metazoan tree of life remains largely unknown. Results Our comparative analyses of 49 animal genomes reveal that the largest gains of synteny occurred in the last common ancestor of bilaterians and cnidarians and in that of bilaterians. Depending on their node of emergence, we further show that novel syntenic blocks are characterized by distinct functional compositions (Gene Ontology terms enrichment) and gene density properties, such as high, average and low gene density regimes. This is particularly pronounced among bilaterian novel microsyntenies, most of which fall into high gene density regime associated with higher gene coexpression levels. Conversely, a majority of vertebrate novel microsyntenies display a low gene density regime associated with lower gene coexpression levels. Conclusions Our study provides first evidence for evolutionary transitions between different modes of microsyntenic block regulation that coincide with key events of metazoan evolution. Moreover, the microsyntenic profiling strategy and interactive online application (Syntenic Density Browser, available at: http://synteny.csb.univie.ac.at/) we present here can be used to explore regulatory properties of microsyntenic blocks and predict their coexpression in a wide-range of animal genomes.

Emergence of novel genomic regulatory regions associated with light-organ development in the bobtail squid

“…Hox clusters are also genomically unique in vertebrates, compared to other locally conserved gene clusters, in that they also show significantly higher gene density than the average genomic gene density in those genomes. 79 Similar changes in gene densities are observed around the {DAC} cluster. However, as we do not yet have tissue-resolved ATAC-seq or RNA-seq during embryonic development, we cannot fully test this hypothesis.…”

New Hydra genomes reveal conserved principles of hydrozoan transcriptional regulation

“…The boundaries of these conserved TADs are associated with binding sites for CTCF, a mediator of TAD formation (Harmston et al 2017; Heger et al 2012). However, cnidarians and bilaterians, whose last common ancestor predates the emergence of CTCF, still exhibit extensive microsyntenic conservation (Robert et al 2022; Heger et al 2012). This raises the possibility that the chromatin contact domains in Hydra may reflect an ancestral state of chromatin organization that predates the split of Bilateria and Cnidaria.…”

SYNPHONI: scale-free and phylogeny-aware reconstruction of synteny conservation and transformation across animal genomes

“…For benchmarking, we compared SYNPHONI to the MicroSynteny tool ( Simakov et al , 2013 ; Robert et al , 2022 ) and EvolClust ( Marcet-Houben and Gabaldón, 2019 ), two methods that also detect non-collinear multispecies blocks across numerous genomes ( Supplementary Material , Section S3). SYNPHONI provides the highest detection accuracy, as indicated by a significantly higher proportion of ‘core OGs’ (ancestrally microsyntenic OGs) per multispecies block (Wilcoxon rank-sum tests, P < 0.05, Supplementary Fig.…”