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Waking the sleeping dragon: gene expression profiling reveals adaptive strategies of the hibernating reptile Pogona vitticeps.

ABSTRACT: BACKGROUND:Hibernation is a physiological state exploited by many animals exposed to prolonged adverse environmental conditions associated with winter. Large changes in metabolism and cellular function occur, with many stress response pathways modulated to tolerate physiological challenges that might otherwise be lethal. Many studies have sought to elucidate the molecular mechanisms of mammalian hibernation, but detailed analyses are lacking in reptiles. Here we examine gene expression in the Australian central bearded dragon (Pogona vitticeps) using mRNA-seq and label-free quantitative mass spectrometry in matched brain, heart and skeletal muscle samples from animals at late hibernation, 2 days post-arousal and 2 months post-arousal. RESULTS:We identified differentially expressed genes in all tissues between hibernation and post-arousal time points; with 4264 differentially expressed genes in brain, 5340 differentially expressed genes in heart, and 5587 differentially expressed genes in skeletal muscle. Furthermore, we identified 2482 differentially expressed genes across all tissues. Proteomic analysis identified 743 proteins (58 differentially expressed) in brain, 535 (57 differentially expressed) in heart, and 337 (36 differentially expressed) in skeletal muscle. Tissue-specific analyses revealed enrichment of protective mechanisms in all tissues, including neuroprotective pathways in brain, cardiac hypertrophic processes in heart, and atrophy protective pathways in skeletal muscle. In all tissues stress response pathways were induced during hibernation, as well as evidence for gene expression regulation at transcription, translation and post-translation. CONCLUSIONS:These results reveal critical stress response pathways and protective mechanisms that allow for maintenance of both tissue-specific function, and survival during hibernation in the central bearded dragon. Furthermore, we provide evidence for multiple levels of gene expression regulation during hibernation, particularly enrichment of miRNA-mediated translational repression machinery; a process that would allow for rapid and energy efficient reactivation of translation from mature mRNA molecules at arousal. This study is the first molecular investigation of its kind in a hibernating reptile, and identifies strategies not yet observed in other hibernators to cope stress associated with this remarkable state of metabolic depression.

SUBMITTER: Capraro A

PROVIDER: S-EPMC6555745 | biostudies-literature | 2019 Jun

REPOSITORIES: biostudies-literature

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Waking the sleeping dragon: gene expression profiling reveals adaptive strategies of the hibernating reptile Pogona vitticeps.

Capraro Alexander A O'Meally Denis D Waters Shafagh A SA Patel Hardip R HR Georges Arthur A Waters Paul D PD

BMC genomics 20190606 1

<h4>Background</h4>Hibernation is a physiological state exploited by many animals exposed to prolonged adverse environmental conditions associated with winter. Large changes in metabolism and cellular function occur, with many stress response pathways modulated to tolerate physiological challenges that might otherwise be lethal. Many studies have sought to elucidate the molecular mechanisms of mammalian hibernation, but detailed analyses are lacking in reptiles. Here we examine gene expression i ...[more]

PMID: 31170930

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Project description:Imaging techniques have proved to be crucial for diagnosis in reptile species. The topography of the internal organs of bearded dragons has been described in recent studies as meeting the small animal practitioners´ demand for knowledge concerning their anatomy. However, the nomenclature in the respective literature is not uniform, which could lead to misunderstandings concerning the respective and/or affected parts of the alimentary canal. Therefore, the aim of this study was to provide clear information on anatomy and histology of the alimentary canal of bearded dragons including supplying blood vessels. For the dissection of the alimentary canal, 11 Inland Bearded Dragons (Pogona vitticeps) were used (five males, six females), which had been euthanised for clinical reasons other than those concerning the digestive tract or had died spontaneously. The supplying arteries were demonstrated by injecting red latex into the aorta, while the intestinal veins were filled with blue latex via the portal vein. Microscopic examination was carried out on specimens of seven additional bearded dragons using routine histologic procedures. Macroscopically, the sections of the alimentary canal from oral to aboral were distinguished into oesophagus, stomach, small intestine, colic ampulla, colic isthmus, rectum and cloaca. Differentiation of the duodenum, jejunum and ileum was only possible when considering the bile duct, the vasculature and the histology of the organ wall. Arteries supplying the oesophagus and the final straight part of the large intestine originated from the aorta in a segmental manner. Between these, three unpaired arteries arose from the aorta. Their branches supplied stomach and intestine excluding its last part. Based on the findings of the present study, a nomenclature for the different parts of the alimentary canal and the supplying blood vessels of bearded dragons is suggested which is well understandable for veterinary practitioners and is based on zoological knowledge of reptiles.

Project description:BackgroundThe development of male- or female-specific phenotypes in squamates is typically controlled by either temperature-dependent sex determination (TSD) or chromosome-based genetic sex determination (GSD). However, while sex determination is a major switch in individual phenotypic development, it is unknownhow evolutionary transitions between GSD and TSD might impact on the evolution of squamate phenotypes, particularly the fast-evolving and diverse genitalia. Here, we take the unique opportunity of studying the impact of both sex determination mechanisms on the embryological development of the central bearded dragon (Pogona vitticeps). This is possible because of the transitional sex determination system of this species, in which genetically male individuals reverse sex at high incubation temperatures. This can trigger the evolutionary transition of GSD to TSD in a single generation, making P. vitticeps an ideal model organism for comparing the effects of both sex determination processes in the same species.ResultsWe conducted four incubation experiments on 265 P. vitticeps eggs, covering two temperature regimes ("normal" at 28 °C and "sex reversing" at 36 °C) and the two maternal sexual genotypes (concordant ZW females or sex-reversed ZZ females). From this, we provide the first detailed staging system for the species, with a focus on genital and limb development. This was augmented by a new sex chromosome identification methodology for P. vitticeps that is non-destructive to the embryo. We found a strong correlation between embryo age and embryo stage. Aside from faster growth in 36 °C treatments, body and external genital development was entirely unperturbed by temperature, sex reversal or maternal sexual genotype. Unexpectedly, all females developed hemipenes (the genital phenotype of adult male P. vitticeps), which regress close to hatching.ConclusionsThe tight correlation between embryo age and embryo stage allows the precise targeting of specific developmental periods in the emerging field of molecular research on P. vitticeps. The stability of genital development in all treatments suggests that the two sex-determining mechanisms have little impact on genital evolution, despite their known role in triggering genital development. Hemipenis retention in developing female P. vitticeps, together with frequent occurrences of hemipenis-like structures during development in other squamate species, raises the possibility of a bias towards hemipenis formation in the ancestral developmental programme for squamate genitalia.

Dataset Information

Waking the sleeping dragon: gene expression profiling reveals adaptive strategies of the hibernating reptile Pogona vitticeps.

Publications

Waking the sleeping dragon: gene expression profiling reveals adaptive strategies of the hibernating reptile Pogona vitticeps.

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