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

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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.

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Data availability

All data supporting the results in this paper comply with field standards and are available at SRA/NCBI BioProject ID: PRJNA904249.

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Acknowledgements

The original findings presented in this paper were part of a PEDECIBA (Programa de Desarrollo Ciencias Básicas) PhD thesis by NG Papa. We thank the editor and reviewers for their careful consideration of our work and useful advice. We especially thank Federico PF for the critical overview of the entire manuscript writing process.

Funding

This research was supported by Iniciativa Científica Milenio (ICN2021_044), Comisión Sectorial de Investigación Científica, Universidad de la República, Universidad de la República, Uruguay (I + D2014, Project ID 147 and Iniciación a la investigación 2017 Modalidad 2, Project ID 324), Programa de Desarrollo de las Ciencias Básicas (PEDECIBA), Facultad de Ciencias, Universidad de la República and Instituto de Investigaciones Biológicas Clemente Estable, Uruguay. Comisión Académica de Posgrado Universidad de la República, Uruguay, (CAP) supported Nicolás Papa with a doctoral fellowship.

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Contributions

All authors, except LI, contributed to the study conception and design. Biological samples (embryo stages) were obtained by NP, NB, MJA and CM. RNA isolation for sequencing was performed by CV and LP. Sequencing and reference transcriptome assembly were performed by FG and ADG. Embryo transcriptome differential expression and functional analyses were performed by NP, JSS and LI. The first draft of the manuscript was written by MJA, NP and CC. All authors commented on previous versions of the manuscript as well as read and approved the final manuscript.

Corresponding authors

Correspondence to Miguel L. Allende or Maria Jose Arezo.

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All procedures performed in the study were in accordance with a protocol approved by the Animal Experimentation Committee from the Universidad de la República, CHEA (Comisión Honoraria de Experimentación Animal; protocol code 240011-002308-14).

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The authors declare no competing interests.

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Papa, N.G., Sotelo-Silveira, J., Inchausti, L. et al. Exploring the molecular basis of diapause I induction in the annual killifish Garcialebias charrua: a transcriptomic approach. Environ Biol Fish 107, 693–717 (2024). https://doi.org/10.1007/s10641-024-01562-x

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