A Rapid Transcriptome Response Is Associated with Desiccation Resistance in Aerially-Exposed Killifish Embryos

Abstract

Delayed hatching is a form of dormancy evolved in some amphibian and fish embryos to cope with environmental conditions transiently hostile to the survival of hatchlings or larvae. While diapause and cryptobiosis have been extensively studied in several animals, very little is known concerning the molecular mechanisms involved in the sensing and response of fish embryos to environmental cues. Embryos of the euryhaline killifish Fundulus heteroclitus advance dvelopment when exposed to air but hatching is suspended until flooding with seawater. Here, we investigated how transcriptome regulation underpins this adaptive response by examining changes in gene expression profiles of aerially incubated killifish embryos at ∼100% relative humidity, compared to embryos continuously flooded in water. The results confirm that mid-gastrula embryos are able to stimulate development in response to aerial incubation, which is accompanied by the differential expression of at least 806 distinct genes during a 24 h period. Most of these genes (∼70%) appear to be differentially expressed within 3 h of aerial exposure, suggesting a broad and rapid transcriptomic response. This response seems to include an early sensing phase, which overlaps with a tissue remodeling and activation of embryonic development phase involving many regulatory and metabolic pathways. Interestingly, we found fast (0.5–1 h) transcriptional differences in representatives of classical “stress” proteins, such as some molecular chaperones, members of signalling pathways typically involved in the transduction of sensor signals to stress response genes, and oxidative stress-related proteins, similar to that described in other animals undergoing dormancy, diapause or desiccation. To our knowledge, these data represent the first transcriptional profiling of molecular processes associated with desiccation resistance during delayed hatching in non-mammalian vertebrates. The exceptional transcriptomic plasticity observed in killifish embryos provides an important insight as to how the embryos are able to rapidly adapt to non-lethal desiccation conditions.

Transcriptomics of diapause in an isogenic self-fertilizing vertebrate

“…Nevertheless, several diapause studies using an earlier technology (cDNA microarrays) can provide some useful perspectives. By using microarrays, 15,686 expression sequence tags (ESTs) were obtained from a time-course analysis of the Mummichog fish ( Fundulus heteroclitus ), including embryos with delayed hatching due to desiccation [ 28 ]. The individual F. heteroclitus genes identified were different than those reported in the current study.…”

Global transcriptome analysis identifies regulated transcripts and pathways activated during oogenesis and early embryogenesis in atlantic cod

“…A few reports have followed the fish transcriptome throughout embryogenesis using microarrays, in zebrafish (Mathavan et al, 2005), gilthead sea bream (Sparus auratus L.) (Sarropoulou et al, 2005), and mummichog (Fundulus heteroclitus) (Bozinovic et al, 2011). Environmentalbased changes in the mummichog embryonic transcriptome have been described (Tingaud-Sequeira et al, 2013). The first large-scale analyses of the Atlantic cod transcriptome during embryogenesis were recently performed by Drivenes et al (2012), Kleppe et al (2012), and Lanes et al (2012), respectively using microarray (7,000 genes), cDNA sequencing (257 genes), and qPCR (25 genes).…”

Amphibious fishes: evolution and phenotypic plasticity

“…Terrestrial incubation in K. marmoratus embryos also decreased the energetic costs of development relative to those of embryos reared in water, as shown by lower O 2 uptake and opercular movements and larger yolk reserves (Wells et al, 2015). Fundulus heteroclitus embryos in air downregulated aquaporin proteins, a process that may be a protective mechanism to avoid desiccation (Tingaud-Sequeira et al, 2009), and they differentially expressed 806 genes relative to control embryos in water (Tingaud-Sequeira et al, 2013). Thus, plasticity is demonstrated by embryos of many species in response to the rearing environment.…”