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Decoding transcriptional regulation in response to visible light in vertebrates

ABSTRACT: Sunlight influences various physiological processes, including circadian clock regulation and DNA repair via D-box enhancer elements. However, the broader transcriptional effects of visible light remain unclear. To investigate this, we compared light-mediated gene expression in zebrafish (Danio rerio) and the blind Somalian cavefish (Phreatichthys andruzzii), a species that evolved in perpetual darkness and lacks light-dependent circadian and DNA repair responses. We performed RNA sequencing of zebrafish and cavefish embryonic cell lines exposed to blue light (468 nm, for up to 6 hours), followed by gene ontology analysis and functional validation via bioinformatic, in vitro, and in vivo approaches. We revealed a light-dependent activation of a set of mitochondrial and heme metabolism genes via D-box enhancer elements. This transcriptional response was absent in cavefish cells. Further analysis revealed that while all zebrafish and cavefish PAR-bZip factors can activate the D-box, cavefish homologs exhibit diminished activity, suggesting an evolutionary reduction in light responsiveness. The D-box emerges as a key regulator of light-driven transcription in zebrafish, extending its role beyond circadian and DNA repair pathways to metabolic and mitochondrial processes. These findings provide insights into the evolution of light-sensing transcriptional mechanisms and lay the groundwork for future studies on their physiological implications.

ORGANISM(S): Danio rerio Garra andruzzii

PROVIDER: GSE290582 | GEO | 2025/12/03

REPOSITORIES: GEO

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Project description:Dysregulation of sleep has widespread health consequences and represents an enormous health burden. Short-sleeping individuals are predisposed to the effects of neurodegeneration, suggesting a critical role for sleep in the maintenance of neuronal health. While the effects of sleep on cellular function are not completely understood, growing evidence has identified an association between sleep loss and DNA damage, raising the possibility that sleep facilitates efficient DNA repair. The Mexican tetra fish,Astyanax mexicanusprovides a model to investigate the evolutionary basis for changes in sleep and the consequences of sleep loss. Multiple cave-adapted populations of these fish have evolved to sleep for substantially less time compared to surface populations of the same species without identifiable impacts on healthspan or longevity. To investigate whether the evolved sleep loss is associated with DNA damage and cellular stress, we compared the DNA Damage Response (DDR) and oxidative stress levels betweenA. mexicanuspopulations. We measured markers of chronic sleep loss and discovered elevated levels of the DNA damage marker γH2AX in the brain, and increased oxidative stress in the gut of cavefish, consistent with chronic sleep deprivation. Notably, we found that acute UV-induced DNA damage elicited an increase in sleep in surface fish but not in cavefish. On a transcriptional level, only the surface fish activated the photoreactivation repair pathway following UV damage. These findings suggest a reduction of the DDR in cavefish compared to surface fish that coincides with elevated DNA damage in cavefish. To examine DDR pathways at a cellular level, we created an embryonic fibroblast cell line from the two populations ofA. mexicanus. We observed that both the DDR and DNA repair were diminished in the cavefish cells, corroborating thein vivofindings and suggesting that the acute response to DNA damage is lost in cavefish. To investigate the long-term impact of these changes, we compared the transcriptome in the brain and gut of aged surface fish and cavefish. Strikingly, many genes that are differentially expressed between young and old surface fish do not transcriptionally vary by age in cavefish. Taken together, these findings suggest that have developed resilience to sleep loss, despite possessing cellular hallmarks of chronic sleep deprivation.

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Decoding transcriptional regulation in response to visible light in vertebrates

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