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.
Highlights
Arrested development is a form of dormancy in which metabolic activity is significantly depressed or even absent
To obtain a representative picture of the adaptive transcriptome response of embryonic F. heteroclitus, a total of 16,896 clones were Sanger-sequenced from a normalized embryo cDNA library constructed from embryos at different stages incubated in water or in air
Chuaypanang [73] found that hsc70, hsp70, hsp90a and hsp90b expression in F. heteroclitus embryos is largely constitutive with no major changes after desiccation stress compared with controls, and no significant differences among embryo ages. These findings suggest that Hsp40-related proteins, rather than Hsp70, and other small heat shock proteins (Hsps) might be involved during desiccation resistance in killifish embryos
Summary
Arrested development is a form of dormancy in which metabolic activity is significantly depressed or even absent. It is a widespread strategy employed by many organisms, from prokaryotes to mammals, in response to unfavorable thermal, nutritional or hydration conditions [1]. Embryonic dormancy is the most widespread form of arrested development and is often associated with dehydration tolerance, which allows survival during transient or prolonged environmental hypoxia and anoxia [7,8]. Three major forms of arrested development have been described for fish embryos: delayed hatching, embryonic diapause, and anoxia-induced quiescence [7]. In response to hypoxia-induced diapause, most cells become arrested in the G1/G0 phase of the cell cycle which may favour genome integrity for the recovery phase [8]
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