Exploring the molecular basis of diapause I induction in the annual killifish Garcialebias charrua: a transcriptomic approach

Abstract

One of the most unique examples of adaptation to extreme environments is exemplified by diapauses (I, II and III) in annual killifish embryos. We aimed to understand the molecular mechanisms involved in the regulation of these arrests. In this context, we first comprehensively analysed the expression of genes using a transcriptomic approach to distinguish between two developmental trajectories: diapause induction and non-diapause induction. We focused on the process of diapause I induction by comparing the mRNA profiles at the maternal stage with those of diapause I-induced embryos, non-diapause I-induced embryos and embryos that had exited diapause I. Our analysis revealed approximately seven hundred transcripts that were differentially and exclusively expressed upon the induction of diapause I. The Gene Ontology (GO) categories of the gene-specific transcriptional regulator group, RNA metabolism, cytoskeletal protein and scaffold/adaptor proteins exhibited the highest representation among differentially expressed genes (DEGs) and coexpression analysis. Remarkably, the identification of different homeodomain transcription factors, cell cycle regulators and RNA processing/regulators as DEGs suggests that these regulators play important roles in Garcialebias charrua diapause I induction. Consistent with the results of the DEG analysis, the results of the Clust coexpression analysis revealed 5 and 3 patterns of diapause I-induced gene upregulation and downregulation, corresponding to 3939 and 1250 genes, respectively. Comparative expression analysis of genes and signalling pathways reported to contribute to diapauses in other species revealed that insulin/IGF, vitamin D, Wnt, polycomb and heat shock proteins are also involved in diapause I induction in annual killifish.