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Slc7a11 downregulation is rapidly reversed after cessation of competitive social stress in zebra finches

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Abstract

Gene expression can be modulated by epigenetic modifications, which may lead to a rapid adaptation to environmental stress. After stress cessation, changes in gene expression could be reversed, which would allow organisms to maintain their phenotype under transient environments, but this mechanism is poorly understood. Social stress downregulates a gene directly involved in pheomelanin synthesis (Slc7a11) by changing DNA m5C levels, avoiding cellular damage caused by stress. We thus investigated if Slc7a11 expression is reversed in melanocytes of growing flank feathers to avoid changes in the pigmentation phenotype. We measured the expression level of Slc7a11 at three time points: before stress exposure, immediately after stress exposure and six weeks after stress cessation in 37 male zebra finches (Taeniopygia guttata). No differences in Slc7a11 expression were detected between birds exposed to stress and controls six weeks after stress elimination, indicating that stress removal led to a cessation of Slc7a11 downregulation. Reversibility in Slc7a11 expression, probably mediated by reversible changes in DNA methylation, may thus avoid altering the pigmentation phenotype during transient stressful conditions. This is one of the few studies in vertebrates supporting the idea that reversible gene expression responses allow organisms adapting to changing environmental conditions.

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References

  1. Weake VM, Workman JL (2010) Inducible gene expression: diverse regulatory mechanisms. Nat Rev Genet 11(6):426

    Article  CAS  Google Scholar 

  2. Storey KB (1996) Oxidative stress: animal adaptations in nature. BJMBR 29:1715–1733

    CAS  Google Scholar 

  3. Schröder P, Krutmann J (2005) Environmental oxidative stress–Environmental sources of ROS. Reactions. Processes. Springer, Berlin, Heidelberg, pp 19–31

    Google Scholar 

  4. López-Maury L, Marguerat S, Bähler J (2008) Tuning gene expression to changing environments: from rapid responses to evolutionary adaptation. Nat Rev Genet 9(8):583

    Article  Google Scholar 

  5. Champagne FA (2010) Epigenetic influence of social experiences across the lifespan. Dev Psychobiol 52(4):299–311

    Article  CAS  Google Scholar 

  6. Weaver IC, Cervoni N, Champagne FA, D’Alessio AC, Sharma S, Seckl JR, Sergiy Dymov S, Szyf M, Meaney MJ (2004) Epigenetic programming by maternal behavior. Nat Neurosci 7(8):847

    Article  CAS  Google Scholar 

  7. Zhang TY, Meaney MJ (2010) Epigenetics and the environmental regulation of the genome and its function. Ann Rev Psychol 61:439–466

    Article  Google Scholar 

  8. Sørensen JG, Nielsen MM, Kruhoffer M, Justesen J, Loeschcke V (2005) Full genome gene expression analysis of the heat stress response in Drosophila melanogaster. Cell Stress Chaperones 10:312–328

    Article  Google Scholar 

  9. Yale J, Bohnert HJ (2001) Transcript expression in Saccharomyces cerevisiae at high salinity. Biol Chem 276:15996–16007

    Article  CAS  Google Scholar 

  10. Gabriel W (1999) Evolution of reversible plastic responses: inducible defenses and environmental tolerance. In: Tollrian R, Harvell CD (eds) The Ecology and Evolution of Inducible Defenses. Princeton University Press, Princeton, pp 286–305

    Google Scholar 

  11. Hawkins LJ, Storey KB (2020) Advances and applications of environmental stress adaptation research. Comp Biochem Phys A 240:110623

    Article  CAS  Google Scholar 

  12. Tung J, Gilad Y (2013) Social environmental effects on gene regulation. Cell Mol Life Sci 70(22):4323–4339

    Article  CAS  Google Scholar 

  13. Rodríguez-Martínez S, Galván I (2019) Exposure to a competitive social environment activates an epigenetic mechanism that limits pheomelanin synthesis in zebra finches. Mol Ecol 28:3698–3708

    Article  Google Scholar 

  14. De Nadal E, Ammerer G, Posas F (2011) Controlling gene expression in response to stress. Nat Rev Genet 12(12):833–845

    Article  Google Scholar 

  15. Gabriel W (2005) How stress selects for reversible phenotypic plasticity. J Evol Biol 18(4):873–883

    Article  CAS  Google Scholar 

  16. Rodríguez-Martínez S, Márquez R, Inácio Â, Galván I (2019) Changes in melanocyte RNA and DNA methylation favour pheomelanin synthesis and may avoid systemic oxidative stress after dietary cysteine supplementation in birds. Mol Ecol 28(5):1030–1042

    Article  Google Scholar 

  17. Galván I, Inácio Â, Romero-Haro AA, Alonso-Alvarez C (2017) Adaptive downregulation of pheomelanin-related Slc7a11 gene expression by environmentally induced oxidative stress. Mol Ecol 26(3):849–858

    Article  Google Scholar 

  18. Galván I (2018) Predation risk determines pigmentation phenotype in nuthatches by melanin-related gene expression effects. J Evol Biol 31(12):1760–1771

    Article  Google Scholar 

  19. Galván I, Rodríguez-Martínez S (2018) Females mate with males with diminished pheomelanin-based coloration in the Eurasian nuthatch Sitta europaea. J Avian Biol 49(9):e01854

    Article  Google Scholar 

  20. Boyko A, Kovalchuk I (2008) Epigenetic control of plant stress response. Environ Mol Mutagen 49(1):61–72

    Article  CAS  Google Scholar 

  21. Hijazi K, Malyszko B, Steiling K, Xiao X, Liu G, Alekseyev YO, Brooks DR (2019) Tobacco-Related alterations in airway gene expression are rapidly reversed within weeks following smoking-cessation. Sci Rep 9(1):1–10

    Article  CAS  Google Scholar 

  22. Tung J, Barreiro LB, Johnson ZP, Hansen KD, Michopoulos V, Toufexis D, Gilad Y (2012) Social environment is associated with gene regulatory variation in the Rhesus macaque immune system. Proc Natl Acad Sci 109(17):6490–6495

    Article  CAS  Google Scholar 

  23. Herb BR, Wolschin F, Hansen KD, Aryee MJ, Langmead B, Irizarry R, Feinberg AP (2012) Reversible switching between epigenetic states in honeybee behavioral subcastes. Nat Neurosci 15(10):1371

    Article  CAS  Google Scholar 

  24. Burmeister SS, Jarvis ED, Fernald RD (2005) Rapid behavioral and genomic responses to social opportunity. PLoS Biol. https://doi.org/10.1371/journal.pbio.0030363

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank Sara Borrego for help with laboratory work. This work was supported by Spain’s Ministry of Science, Innovation and Universities: Project CGL2015‐67796‐P, Ramón y Cajal Fellowship RYC‐2012‐10237 to I.G., and Grant BES‐2016‐077112 to S.R‐M.

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SRM and IG conceived the study and wrote the manuscript. SRM conducted the experiment and performed laboratory and statistical analysis.

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Correspondence to Sol Rodríguez-Martínez.

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The authors declare no conflicts of interest.

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This study was approved by the Bioethics Subcommittee of Consejo Superior de Investigaciones Cientificas (CSIC; Ref. 651/2018) and local authorities (Consejería de Agricultura, Pesca y Medio Ambiente, Junta de Andalucía; Ref. 23/02/2018/016).

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Rodríguez-Martínez, S., Galván, I. Slc7a11 downregulation is rapidly reversed after cessation of competitive social stress in zebra finches. Mol Biol Rep 48, 3007–3010 (2021). https://doi.org/10.1007/s11033-021-06256-6

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  • DOI: https://doi.org/10.1007/s11033-021-06256-6

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