6533b827fe1ef96bd1286694

RESEARCH PRODUCT

Diversification of spatiotemporal expression and copy number variation of the echinoid hbox12/pmar1/micro1 multigene family

Giovanni SpinelliFabiana GeraciVincenzo Cavalieri

subject

0301 basic medicineEvolutionary GeneticsEmbryologyGene regulatory networklcsh:MedicineGene ExpressionMedicine (all); Biochemistry Genetics and Molecular Biology (all); Agricultural and Biological Sciences (all)Database and Informatics MethodsGene duplicationGene Regulatory NetworksCopy-number variationlcsh:ScienceSea urchinPhylogenyMultidisciplinarybiologyPhylogenetic treeMedicine (all)Genes HomeoboxGene Expression Regulation DevelopmentalAnimal ModelsGenomicsExperimental Organism SystemsMultigene FamilySequence AnalysisResearch ArticleEchinodermsDNA Copy Number VariationsBioinformaticsDNA transcriptionZoologySettore BIO/11 - Biologia MolecolareResearch and Analysis MethodsParacentrotus lividus03 medical and health sciencesSequence Motif Analysisbiology.animalGeneticsGene familyAnimalsGeneEvolutionary BiologyBiochemistry Genetics and Molecular Biology (all)lcsh:REmbryosOrganismsBiology and Life SciencesComputational Biologybiology.organism_classificationGenome AnalysisGenomic LibrariesInvertebrates030104 developmental biologyAgricultural and Biological Sciences (all)Evolutionary biologySea Urchinslcsh:QSequence AlignmentDevelopmental Biology

description

Changes occurring during evolution in the cis-regulatory landscapes of individual members of multigene families might impart diversification in their spatiotemporal expression and function. The archetypal member of the echinoid hbox12/pmar1/micro1 family is hbox12-a, a homeobox-containing gene expressed exclusively by dorsal blastomeres, where it governs the dorsal/ventral gene regulatory network during embryogenesis of the sea urchin Paracentrotus lividus. Here we describe the inventory of the hbox12/pmar1/micro1 genes in P. lividus, highlighting that gene copy number variation occurs across individual sea urchins of the same species. We show that the various hbox12/pmar1/micro1 genes group into three subfamilies according to their spatiotemporal expression, which ranges from broad transcription throughout development to transient expression in either the animal hemisphere or micromeres of the early embryo. Interestingly, the promoter regions of those genes showing comparable expression patterns are highly similar, while differing from those of the other subfamilies. Strikingly, phylogenetic analysis suggests that the hbox12/pmar1/micro1 genes are species-specific, exhibiting extensive divergence in their noncoding, but not in their coding, sequences across three distinct sea urchin species. In spite of this, two micromere-specific genes of P. lividus possess a TCF/LEF-binding motif in a similar position, and their transcription relies on Wnt/β-catenin signaling, similar to the pmar1 and micro1 genes, which in other sea urchin species are involved in micromere specification. Altogether, our findings suggest that the hbox12/pmar1/micro1 gene family evolved rather rapidly, generating paralogs whose cis-regulatory sequences diverged following multiple rounds of duplication from a common ancestor.

10.1371/journal.pone.0174404http://hdl.handle.net/10447/228416