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Evolution of diapause in the African turquoise killifish by remodeling ancient gene regulatory landscape

View ORCID ProfileParam Priya Singh, G. Adam Reeves, View ORCID ProfileKévin Contrepois, Mathew Ellenberger, Chi-Kuo Hu, Michael P. Snyder, Anne Brunet
doi: https://doi.org/10.1101/2021.10.25.465616
Param Priya Singh
1Department of Genetics, Stanford University, Stanford, CA, USA
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G. Adam Reeves
1Department of Genetics, Stanford University, Stanford, CA, USA
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Kévin Contrepois
1Department of Genetics, Stanford University, Stanford, CA, USA
2Stanford Cardiovascular Institute, Stanford University, Stanford, CA, USA
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Mathew Ellenberger
1Department of Genetics, Stanford University, Stanford, CA, USA
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Chi-Kuo Hu
1Department of Genetics, Stanford University, Stanford, CA, USA
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Michael P. Snyder
1Department of Genetics, Stanford University, Stanford, CA, USA
2Stanford Cardiovascular Institute, Stanford University, Stanford, CA, USA
3Stanford Diabetes Research Center, Stanford University, Stanford, CA, USA
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Anne Brunet
1Department of Genetics, Stanford University, Stanford, CA, USA
4Glenn Laboratories for the Biology of Aging, Stanford University, Stanford, CA, USA
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  • For correspondence: abrunet1@stanford.edu
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ABSTRACT

Suspended animation states such as hibernation or diapause allow organisms to survive extreme environments. But the mechanisms underlying the evolution of these extreme survival states are unknown. The African turquoise killifish has evolved diapause as a form of suspended development to survive the complete drought that occurs every year in its habitat. Here we show that many gene duplicates – paralogs – exhibit specialized expression in diapause versus normal development in the African turquoise killifish. Surprisingly, paralogs with specialized expression in diapause are evolutionarily very ancient, and they are also present even in vertebrates that do not exhibit diapause. Profiling the chromatin accessibility landscape among different fish species reveals an evolutionarily recent increase in chromatin accessibility at these very ancient paralogs, suggesting rewiring of their regulatory landscape. The increase in chromatin accessibility in the African turquoise killifish is linked to the presence of new binding sites for transcription factors (e.g., FOXO, REST, and PPAR), due to both de novo mutations and transposable element insertion. Interestingly, accessible chromatin regions in diapause are enriched for lipid metabolism genes. By performing lipidomics in different fish species, we uncover a specific lipid profile in African turquoise killifish embryos in diapause. Notably, select very long-chain fatty acids are high in diapause, suggesting they may be used for long-term survival in this state. Together, our multi-omic analysis indicates that diapause is driven by regulatory innovation of very ancient gene programs that are critical for survival. Our work also suggests a mechanism for how complex adaptations evolve in nature and offers strategies by which a suspended animation program could be reactivated in other species for long-term preservation.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted October 25, 2021.
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Evolution of diapause in the African turquoise killifish by remodeling ancient gene regulatory landscape
Param Priya Singh, G. Adam Reeves, Kévin Contrepois, Mathew Ellenberger, Chi-Kuo Hu, Michael P. Snyder, Anne Brunet
bioRxiv 2021.10.25.465616; doi: https://doi.org/10.1101/2021.10.25.465616
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Evolution of diapause in the African turquoise killifish by remodeling ancient gene regulatory landscape
Param Priya Singh, G. Adam Reeves, Kévin Contrepois, Mathew Ellenberger, Chi-Kuo Hu, Michael P. Snyder, Anne Brunet
bioRxiv 2021.10.25.465616; doi: https://doi.org/10.1101/2021.10.25.465616

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