Diversified regulation of circadian clock gene expression following whole genome duplication

English version

Autoři: Alexander C. West ^aff001; Marianne Iversen ^aff001; Even H. Jørgensen ^aff001; Simen R. Sandve ^aff002; David G. Hazlerigg ^aff001; Shona H. Wood ^aff001
Působiště autorů: Arctic chronobiology and physiology research group, Department of Arctic and Marine Biology, UiT – The Arctic University of Norway, Tromsø, Norway ^aff001; Centre for Integrative Genetics (CIGENE), Department of Animal and Aquacultural Sciences (IHA), Faculty of Life Sciences (BIOVIT), Norwegian University of Life Sciences (NMBU), Ås, Norway ^aff002
Vyšlo v časopise: Diversified regulation of circadian clock gene expression following whole genome duplication. PLoS Genet 16(10): e32767. doi:10.1371/journal.pgen.1009097
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1009097

Souhrn

Across taxa, circadian control of physiology and behavior arises from cell-autonomous oscillations in gene expression, governed by a networks of so-called ‘clock genes’, collectively forming transcription-translation feedback loops. In modern vertebrates, these networks contain multiple copies of clock gene family members, which arose through whole genome duplication (WGD) events during evolutionary history. It remains unclear to what extent multiple copies of clock gene family members are functionally redundant or have allowed for functional diversification. We addressed this problem through an analysis of clock gene expression in the Atlantic salmon, a representative of the salmonids, a group which has undergone at least 4 rounds of WGD since the base of the vertebrate lineage, giving an unusually large complement of clock genes. By comparing expression patterns across multiple tissues, and during development, we present evidence for gene -⁠ and tissue-specific divergence in expression patterns, consistent with functional diversification of clock gene duplicates. In contrast to mammals, we found no evidence for coupling between cortisol and circadian gene expression, but cortisol mediated non-circadian regulated expression of a subset of clock genes in the salmon gill was evident. This regulation is linked to changes in gill function necessary for the transition from fresh -⁠ to sea-water in anadromous fish. Overall, this analysis emphasises the potential for a richly diversified clock gene network to serve a mixture of circadian and non-circadian functions in vertebrate groups with complex genomes.

Klíčová slova:

Circadian oscillators – Circadian rhythms – Cortisol – Fish – Gene expression – Gene regulation – Gills – Fish genomics

Zdroje

1. Shi M, Zheng X. Interactions between the circadian clock and metabolism: there are good times and bad times. Acta Biochim Biophys Sin (Shanghai). 2013;45 : 61–69. doi: 10.1093/abbs/gms110 23257295

2. Rosbash M. The Implications of Multiple Circadian Clock Origins. Young Michael, editor. PLoS Biol. 2009;7: e1000062. doi: 10.1371/journal.pbio.1000062 19296723

3. Young MW, Kay SA. Time zones: a comparative genetics of circadian clocks. Nat Rev Genet. 2001;2 : 702–715. doi: 10.1038/35088576 11533719

4. Taylor JS, Raes J. Duplication and divergence: the evolution of new genes and old ideas. Annu Rev Genet. 2004;38 : 615–43. doi: 10.1146/annurev.genet.38.072902.092831 15568988

5. Ohno S. Evolution by Gene Duplication. Berlin, Heidelberg: Springer Berlin Heidelberg; 1970. doi: 10.1007/978-3-642-86659-3

6. van der Horst GTJ, Muijtjens M, Kobayashi K, Takano R, Kanno S, Takao M, et al. Mammalian Cry1 and Cry2 are essential for maintenance of circadian rhythms. Nature. 1999;398 : 627–630. doi: 10.1038/19323 10217146

7. Erzberger A, Hampp G, Granada AE, Albrecht U, Herzel H. Genetic redundancy strengthens the circadian clock leading to a narrow entrainment range. J R Soc Interface. 2013;10 : 20130221. doi: 10.1098/rsif.2013.0221 23676895

8. Pilorz V, Cunningham PS, Jackson A, West AC, Wager TT, Loudon ASI, et al. A Novel Mechanism Controlling Resetting Speed of the Circadian Clock to Environmental Stimuli. Curr Biol. 2014;24 : 766–773. doi: 10.1016/j.cub.2014.02.027 24656826

9. Tamai TK, Young LC, Whitmore D. Light signaling to the zebrafish circadian clock by Cryptochrome 1a. Proc Natl Acad Sci. 2007;104 : 14712–14717. doi: 10.1073/pnas.0704588104 17785416

10. Shi S, Hida A, McGuinness OP, Wasserman DH, Yamazaki S, Johnson CH. Circadian Clock Gene Bmal1 Is Not Essential; Functional Replacement with its Paralog, Bmal2. Curr Biol. 2010;20 : 316–321. doi: 10.1016/j.cub.2009.12.034 20153195

11. Tauber E, Last KS, Olive PJW, Kyriacou CP. Clock Gene Evolution and Functional Divergence. J Biol Rhythms. 2004;19 : 445–458. doi: 10.1177/0748730404268775 15534324

12. Looby P, Loudon ASI. Gene duplication and complex circadian clocks in mammals. Trends Genet. 2005;21 : 46–53. doi: 10.1016/j.tig.2004.11.012 15680514

13. Daan S, Albrecht U, Van der Horst GTJ, Illnerová H, Roenneberg T, Wehr TA, et al. Assembling a Clock for All Seasons: Are There M and E Oscillators in the Genes? J Biol Rhythms. 2001;16 : 105–116. doi: 10.1177/074873001129001809 11302553

14. Hastings M. Modeling the Molecular Calendar. J Biol Rhythms. 2001;16 : 117–123. doi: 10.1177/074873001129001818 11302554

15. Meng Q-J, Logunova L, Maywood ES, Gallego M, Lebiecki J, Brown TM, et al. Setting Clock Speed in Mammals: The CK1ɛ tau Mutation in Mice Accelerates Circadian Pacemakers by Selectively Destabilizing PERIOD Proteins. Neuron. 2008;58 : 78–88. doi: 10.1016/j.neuron.2008.01.019 18400165

16. Meng Q-J, Maywood ES, Bechtold DA, Lu W-Q, Li J, Gibbs JE, et al. Entrainment of disrupted circadian behavior through inhibition of casein kinase 1 (CK1) enzymes. Proc Natl Acad Sci. 2010;107 : 15240–15245. doi: 10.1073/pnas.1005101107 20696890

17. Lee H, Chen R, Lee Y, Yoo S, Lee C. Essential roles of CKIδ and CKIε in the mammalian circadian clock. Proc Natl Acad Sci. 2009;106 : 21359–21364. doi: 10.1073/pnas.0906651106 19948962

18. Etchegaray J-P, Machida KK, Noton E, Constance CM, Dallmann R, Di Napoli MN, et al. Casein Kinase 1 Delta Regulates the Pace of the Mammalian Circadian Clock. Mol Cell Biol. 2009;29 : 3853–3866. doi: 10.1128/MCB.00338-09 19414593

19. Macqueen DJ, Johnston IA. A well-constrained estimate for the timing of the salmonid whole genome duplication reveals major decoupling from species diversification. Proc R Soc B Biol Sci. 2014;281 : 20132881. doi: 10.1098/rspb.2013.2881 24452024

20. Alexandrou MA, Swartz BA, Matzke NJ, Oakley TH. Molecular Phylogenetics and Evolution Genome duplication and multiple evolutionary origins of complex migratory behavior in Salmonidae. Mol Phylogenet Evol. 2013;69 : 514–523.

21. Robertson FM, Gundappa MK, Grammes F, Hvidsten TR, Redmond AK, Lien S, et al. Lineage-specific rediploidization is a mechanism to explain time-lags between genome duplication and evolutionary diversification. Genome Biol. 2017;18 : 111. doi: 10.1186/s13059-017-1241-z 28615063

22. Lien S, Koop BF, Sandve SR, Miller JR, Matthew P, Leong JS, et al. The Atlantic salmon genome provides insights into rediploidization. Nature. 2016;533 : 200–205. doi: 10.1038/nature17164 27088604

23. Moriyama Y, Koshiba-takeuchi K. Significance of whole-genome duplications on the emergence of evolutionary novelties. 2018;17 : 329–338. doi: 10.1093/bfgp/ely007 29579140

24. Li WH. Rate of gene silencing at duplicate loci: a theoretical study and interpretation of data from tetraploid fishes. Genetics. 1980;95 : 237–58. 7429144

25. Cho H, Zhao X, Hatori M, Yu RT, Barish GD, Lam MT, et al. Regulation of circadian behaviour and metabolism by REV-ERB-α and REV-ERB-β. Nature. 2012;485 : 123–127. doi: 10.1038/nature11048 22460952

26. Holmqvist BI, Östholm T, Ekström P. Neuroanatomical analysis of the visual and hypophysiotropic systems in Atlantic salmon (Salmo salar) with emphasis on possible mediators of photoperiodic cues during parr-smolt transformation. Aquaculture. 1994;121 : 1–12. doi: 10.1016/0044-8486(94)90003-5

27. Meyer RL. Eye-in-water electrophysiological mapping of goldfish with and without tectal lesions. Exp Neurol. 1977;56 : 23–41. doi: 10.1016/0014-4886(77)90136-4 558902

28. Sandbakken M, Ebbesson L, Stefansson S, Helvik JV. Isolation and characterization of melanopsin photoreceptors of atlantic salmon (Salmo salar). J Comp Neurol. 2012;520 : 3727–3744. doi: 10.1002/cne.23125 22522777

29. Mazurais D, Brierley I, Anglade I, Drew J, Randall C, Bromage N, et al. Central melatonin receptors in the rainbow trout: Comparative distribution of ligand binding and gene expression. J Comp Neurol. 1999;409 : 313–324. doi: 10.1002/(sici)1096-9861(19990628)409 : 2<313::aid-cne11>3.0.co;2-1 10379923

30. Nakane Y, Ikegami K, Iigo M, Ono H, Takeda K, Takahashi D, et al. The saccus vasculosus of fish is a sensor of seasonal changes in day length. Nat Commun. 2013;4 : 2108. doi: 10.1038/ncomms3108 23820554

31. Evans DH, Piermarini PM, Choe KP. The Multifunctional Fish Gill: Dominant Site of Gas Exchange, Osmoregulation, Acid-Base Regulation, and Excretion of Nitrogenous Waste. Physiol Rev. 2005;85 : 97–177. doi: 10.1152/physrev.00050.2003 15618479

32. Hughes ME, Hogenesch JB, Kornacker K. JTK_CYCLE: An Efficient Nonparametric Algorithm for Detecting Rhythmic Components in Genome-Scale Data Sets. J Biol Rhythms. 2010;25 : 372–380. doi: 10.1177/0748730410379711 20876817

33. Vatine G, Vallone D, Appelbaum L, Mracek P, Ben-Moshe Z, Lahiri K, et al. Light Directs Zebrafish period2 Expression via Conserved D and E Boxes. Kramer A, editor. PLoS Biol. 2009;7: e1000223. doi: 10.1371/journal.pbio.1000223 19859524

34. Björnsson BT, Stefansson SO, McCormick SD. Environmental endocrinology of salmon smoltification. Gen Comp Endocrinol. 2011;170 : 290–298. doi: 10.1016/j.ygcen.2010.07.003 20627104

35. Dumbell R, Matveeva O, Oster H. Circadian Clocks, Stress, and Immunity. Front Endocrinol (Lausanne). 2016;7. doi: 10.3389/fendo.2016.00037 27199894

36. Langhorne P, Simpson TH. The interrelationship of cortisol, Gill (Na + K) ATPase, and homeostasis during the Parr-Smolt transformation of atlantic salmon (Salmo salar L.). Gen Comp Endocrinol. 1986;61 : 203–213. doi: 10.1016/0016-6480(86)90198-x 3007267

37. Mulugeta TD, Nome T, To T-H, Gundappa MK, Macqueen DJ, Våge DI, et al. SalMotifDB: a tool for analyzing putative transcription factor binding sites in salmonid genomes. BMC Genomics. 2019;20 : 694. doi: 10.1186/s12864-019-6051-0 31477007

38. McCormick SD. Effects of Growth Hormone and Insulin-like Growth Factor I on Salinity Tolerance and Gill Na+, K+-ATPase in Atlantic Salmon (Salmo salar): Interaction with Cortisol. Gen Comp Endocrinol. 1996;101 : 3–11. doi: 10.1006/gcen.1996.0002 8713639

39. McCormick SD. Endocrine Control of Osmoregulation in Teleost Fish. Am Zool. 2001;41 : 781–794. doi: 10.1093/icb/41.4.781

40. Accili D, Arden KC. FoxOs at the Crossroads of Cellular Metabolism, Differentiation, and Transformation. Cell. 2004;117 : 421–426. doi: 10.1016/s0092-8674(04)00452-0 15137936

41. Barthel A, Schmoll D, Unterman TG. FoxO proteins in insulin action and metabolism. Trends Endocrinol Metab. 2005;16 : 183–189. doi: 10.1016/j.tem.2005.03.010 15860415

42. Dong XC, Copps KD, Guo S, Li Y, Kollipara R, DePinho RA, et al. Inactivation of Hepatic Foxo1 by Insulin Signaling Is Required for Adaptive Nutrient Homeostasis and Endocrine Growth Regulation. Cell Metab. 2008;8 : 65–76. doi: 10.1016/j.cmet.2008.06.006 18590693

43. Li J, Labbadia J, Morimoto RI. Rethinking HSF1 in Stress, Development, and Organismal Health. Trends Cell Biol. 2017;27 : 895–905. doi: 10.1016/j.tcb.2017.08.002 28890254

44. Barna J, Princz A, Kosztelnik M, Hargitai B, Takács-Vellai K, Vellai T. Heat shock factor-1 intertwines insulin/IGF-1, TGF-β and cGMP signaling to control development and aging. BMC Dev Biol. 2012;12 : 32. doi: 10.1186/1471-213X-12-32 23116063

45. Ronchetti S, Migliorati G, Riccardi C. GILZ as a Mediator of the Anti-Inflammatory Effects of Glucocorticoids. Front Endocrinol (Lausanne). 2015;6. doi: 10.3389/fendo.2015.00170 26617572

46. Carroll SB. Evo-Devo and an Expanding Evolutionary Synthesis: A Genetic Theory of Morphological Evolution. Cell. 2008;134 : 25–36. doi: 10.1016/j.cell.2008.06.030 18614008

47. Carroll SB. Endless Forms. Cell. 2000;101 : 577–580. doi: 10.1016/s0092-8674(00)80868-5 10892643

48. McCormick SD, Saunders R. Preparatory Physiological Adaptations for Marine Life of Salmonids: Osmoregulation, Growth, and Metabolism. Am Fish Soc Symp. 1987;1 : 211–229.

49. McCarthy ID. Temporal repeatability of relative standard metabolic rate in juvenile Atlantic salmon and its relation to life history variation. J Fish Biol. 2000;57 : 224–238. doi: 10.1111/j.1095-8649.2000.tb00788.x

50. McCormick SD, Moyes CD, Ballantyne JS. Influence of salinity on the energetics of gill and kidney of Atlantic salmon (Salmo salar). Fish Physiol Biochem. 1989;6 : 243–254. doi: 10.1007/BF01875027 24221555

51. Davie A, Minghetti M, Migaud H. Seasonal Variations in Clock-Gene Expression in Atlantic Salmon (Salmo salar). Chronobiol Int. 2009;26 : 379–395. doi: 10.1080/07420520902820947 19360485

52. Huang T, Ruoff P, Fjelldal PG. Diurnal expression of clock genes in pineal gland and brain and plasma levels of melatonin and cortisol in Atalantic salmon parr and smolts. Chronobiol Int. 2010;27 : 1697–1714. doi: 10.3109/07420528.2010.514630

53. Huang T, Ruoff P, Fjelldal PG. Effect of continuous light on daily levels of plasma melatonin and cortisol and expression of clock genes in the pineal gland, brain, and liver in Atalantic salmon postsmolts. Chronobiol Int. 2010;27 : 1715–1734. doi: 10.3109/07420528.2010.521272

54. Davies WIL, Tamai TK, Zheng L, Fu JK, Rihel J, Foster RG, et al. An extended family of novel vertebrate photopigments is widely expressed and displays a diversity of function. Genome Res. 2015;25 : 1666–1679. doi: 10.1101/gr.189886.115 26450929

55. Pagano C, Siauciunaite R, Idda ML, Ruggiero G, Ceinos RM, Pagano M, et al. Evolution shapes the responsiveness of the D-box enhancer element to light and reactive oxygen species in vertebrates. Sci Rep. 2018;8 : 13180. doi: 10.1038/s41598-018-31570-8 30181539

56. Gavriouchkina D, Fischer S, Ivacevic T, Stolte J, Benes V, Dekens MPS. Thyrotroph Embryonic Factor Regulates Light-Induced Transcription of Repair Genes in Zebrafish Embryonic Cells. Riley BB, editor. PLoS One. 2010;5: e12542. doi: 10.1371/journal.pone.0012542 20830285

57. Wendelaar Bonga SE. The stress response in fish. Physiol Rev. 1997;77 : 591–625. doi: 10.1152/physrev.1997.77.3.591 9234959

58. Isorna E, De Pedro N, Valenciano AI, Alonso-gómez ÁL. Interplay between the endocrine and circadian systems in fishes. 2017. doi: 10.1530/JOE-16-0330 27999088

59. Mommsen TP, Vijayan MM, Moon TW. Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev Fish Biol Fish. 1999;9 : 211–268.

60. Liu C, Hu J, Qu C, Wang L, Huang G, Niu P, et al. Molecular evolution and functional divergence of zebrafish (Danio rerio) cryptochrome genes. Sci Rep. 2015;5 : 8113. doi: 10.1038/srep08113 25630924

61. Emms DM, Kelly S. OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol. 2015; 1–14.

Článek The O-GlcNAc transferase OGT is a conserved and essential regulator of the cellular and organismal response to hypertonic stress

Článek Chromosome separation during Drosophila male meiosis I requires separase-mediated cleavage of the homolog conjunction protein UNO

Článek How noncrossover homologs are conjoined and segregated in Drosophila male meiosis I: Stable but reversible homolog linkers require a novel Separase target protein

Článek Dbp5 associates with RNA-bound Mex67 and Nab2 and its localization at the nuclear pore complex is sufficient for mRNP export and cell viability

Článek Phenotype-genotype comorbidity analysis of patients with rare disorders provides insight into their pathological and molecular bases

Článek Comparing DNA replication programs reveals large timing shifts at centromeres of endocycling cells in maize roots

Článek A single Ho-induced double-strand break at the MAT locus is lethal in Candida glabrata

Článek A Rad51-independent pathway promotes single-strand template repair in gene editing

Článek Novel loci for childhood body mass index and shared heritability with adult cardiometabolic traits

Článek C. elegans CLASP/CLS-2 negatively regulates membrane ingression throughout the oocyte cortex and is required for polar body extrusion

Článek Dual function of perivascular fibroblasts in vascular stabilization in zebrafish

Článek Drosophila phosphatidylinositol-4 kinase fwd promotes mitochondrial fission and can suppress Pink1/parkin phenotypes