Cis-regulatory differences in isoform expression associate with life history strategy variation in Atlantic salmon


Autoři: Jukka-Pekka Verta aff001;  Paul Vincent Debes aff001;  Nikolai Piavchenko aff001;  Annukka Ruokolainen aff001;  Outi Ovaskainen aff001;  Jacqueline Emmanuel Moustakas-Verho aff001;  Seija Tillanen aff001;  Noora Parre aff001;  Tutku Aykanat aff001;  Jaakko Erkinaro aff003;  Craig Robert Primmer aff001
Působiště autorů: Organismal and Evolutionary Biology Research Programme, University of Helsinki, Viikinkaari, Helsinki, Finland aff001;  Organismal and Evolutionary Biology Research Programme, University of Helsinki, Helsinki, Finland aff001;  Institute of Biotechnology, University of Helsinki, Finland aff002;  Natural Resources Institute Finland (LUKE), Oulu, Finland aff003
Vyšlo v časopise: Cis-regulatory differences in isoform expression associate with life history strategy variation in Atlantic salmon. PLoS Genet 16(9): e32767. doi:10.1371/journal.pgen.1009055
Kategorie: Research Article
doi: 10.1371/journal.pgen.1009055

Souhrn

A major goal in biology is to understand how evolution shapes variation in individual life histories. Genome-wide association studies have been successful in uncovering genome regions linked with traits underlying life history variation in a range of species. However, lack of functional studies of the discovered genotype-phenotype associations severely restrains our understanding how alternative life history traits evolved and are mediated at the molecular level. Here, we report a cis-regulatory mechanism whereby expression of alternative isoforms of the transcription co-factor vestigial-like 3 (vgll3) associate with variation in a key life history trait, age at maturity, in Atlantic salmon (Salmo salar). Using a common-garden experiment, we first show that vgll3 genotype associates with puberty timing in one-year-old salmon males. By way of temporal sampling of vgll3 expression in ten tissues across the first year of salmon development, we identify a pubertal transition in vgll3 expression where maturation coincided with a 66% reduction in testicular vgll3 expression. The late maturation allele was not only associated with a tendency to delay puberty, but also with expression of a rare transcript isoform of vgll3 pre-puberty. By comparing absolute vgll3 mRNA copies in heterozygotes we show that the expression difference between the early and late maturity alleles is largely cis-regulatory. We propose a model whereby expression of a rare isoform from the late allele shifts the liability of its carriers towards delaying puberty. These results exemplify the potential importance of regulatory differences as a mechanism for the evolution of life history traits.

Klíčová slova:

Alleles – Fish – Genetic polymorphism – Gonads – Heterozygosity – Puberty – Testes – 5' UTR


Zdroje

1. Stearns SC. The evolution of life histories. Oxford University Press; 1992.

2. Stearns SC. Life history evolution: successes, limitations, and prospects. Naturwissenschaften. 2000;87: 476–486. doi: 10.1007/s001140050763 11151666

3. Johnston SE, Gratten J, Berenos C, Pilkington JG, Clutton-Brock TH, Pemberton JM, et al. Life history trade-offs at a single locus maintain sexually selected genetic variation. Nature. 2013;502: 93–95. doi: 10.1038/nature12489 23965625

4. Barson NJ, Aykanat T, Hindar K, Baranski M, Bolstad GH, Fiske P, et al. Sex-dependent dominance at a single locus maintains variation in age at maturity in salmon. Nature. 2015;528: 405–408. doi: 10.1038/nature16062 26536110

5. Ayllon F, Kjaerner-Semb E, Furmanek T, Wennevik V, Solberg MF, Dahle G, et al. The vgll3 locus controls age at maturity in wild and domesticated Atlantic salmon (Salmo salar L.) males. PLoS Genet. 2015;11. doi: 10.1371/journal.pgen.1005628 26551894

6. Prince DJ, O’Rourke SM, Thompson TQ, Ali OA, Lyman HS, Saglam IK, et al. The evolutionary basis of premature migration in Pacific salmon highlights the utility of genomics for informing conservation. Sci Adv. 2017;3: e1603198. doi: 10.1126/sciadv.1603198 28835916

7. Narum SR, Genova AD, Micheletti SJ, Maass A. Genomic variation underlying complex life-history traits revealed by genome sequencing in Chinook salmon. Proc Biol Sci. 2018;285. doi: 10.1098/rspb.2018.0935 30051839

8. Hess JE, Zendt JS, Matala AR, Narum SR. Genetic basis of adult migration timing in anadromous steelhead discovered through multivariate association testing. Proc Biol Sci. 2016;283: 20153064. doi: 10.1098/rspb.2015.3064 27170720

9. Troth A, Puzey JR, Kim RS, Willis JH, Kelly JK. Selective trade-offs maintain alleles underpinning complex trait variation in plants. Science. 2018;361: 475–478. doi: 10.1126/science.aat5760 30072534

10. Lamichhaney S, Fan G, Widemo F, Gunnarsson U, Thalmann DS, Hoeppner MP, et al. Structural genomic changes underlie alternative reproductive strategies in the ruff (Philomachus pugnax). Nat Genet. 2016;48: 84–88. doi: 10.1038/ng.3430 26569123

11. Heyland A, Flatt T. Mechanisms of Life History Evolution: The Genetics and Physiology of Life History Traits and Trade-Offs. OUP Oxford; 2011.

12. Fleming IA, Einum S. Reproductive Ecology: A Tale of Two Sexes. In: Aas O, Einum S, Klemetsen A, Skurdal J, editors. Atlantic Salmon Ecology. Wiley-Blackwell; 2010. pp. 33–65. doi: 10.1002/9781444327755.ch2

13. Mobley KB, Granroth-Wilding H, Ellmen M, Vaha J-P, Aykanat T, Johnston SE, et al. Home ground advantage: Local Atlantic salmon have higher reproductive fitness than dispersers in the wild. Sci Adv. 2019;5: eaav1112. doi: 10.1126/sciadv.aav1112 30820455

14. Fleming IA. Pattern and variability in the breeding system of Atlantic salmon (Salmo salar), with comparisons to other salmonids. Can J Fish Aquat Sci. 1998;55: 59–76.

15. Czorlich Y, Aykanat T, Erkinaro J, Orell P, Primmer CR. Rapid sex-specific evolution of age at maturity is shaped by genetic architecture in Atlantic salmon. Nat Ecol Evol. 2018;2: 1800–1807. doi: 10.1038/s41559-018-0681-5 30275465

16. Cousminer DL, Berry DJ, Timpson NJ, Ang W, Thiering E, Byrne EM, et al. Genome-wide association and longitudinal analyses reveal genetic loci linking pubertal height growth, pubertal timing and childhood adiposity. Hum Mol Genet. 2013;22: 2735–2747. doi: 10.1093/hmg/ddt104 23449627

17. Perry JRB, Day F, Elks CE, Sulem P, Thompson DJ, Ferreira T, et al. Parent-of-origin-specific allelic associations among 106 genomic loci for age at menarche. Nature. 2014;514: 92–+. doi: 10.1038/nature13545 25231870

18. Pearse DE, Barson NJ, Nome T, Gao G, Campbell MA, Abadía-Cardoso A, et al. Sex-dependent dominance maintains migration supergene in rainbow trout. Nat Ecol Evol. 2019;69: 1–12. doi: 10.1038/s41559-019-1044-6

19. Lamichhaney S, Fuentes-Pardo AP, Rafati N, Ryman N, McCracken GR, Bourne C, et al. Parallel adaptive evolution of geographically distant herring populations on both sides of the North Atlantic Ocean. Proc Natl Acad Sci U S A. 2017;54: 201617728–E3461. doi: 10.1073/pnas.1617728114 28389569

20. Bateman JR, Johnson JE, Locke MN. Comparing enhancer action in cis and in trans. Genetics. 2012;191: 1143–1155. doi: 10.1534/genetics.112.140954 22649083

21. Tian K, Henderson RE, Parker R, Brown A, Johnson JE, Bateman JR. Two modes of transvection at the eyes absent gene of Drosophila demonstrate plasticity in transcriptional regulatory interactions in cis and in trans. Bosco G, editor. PLoS Genet. 2019;15: e1008152. doi: 10.1371/journal.pgen.1008152 31075100

22. Reyes A, Huber W. Alternative start and termination sites of transcription drive most transcript isoform differences across human tissues. Nucleic Acids Res. 2018;46: 582–592. doi: 10.1093/nar/gkx1165 29202200

23. Wang X, Hou J, Quedenau C, Chen W. Pervasive isoform-specific translational regulation via alternative transcription start sites in mammals. Mol Syst Biol. 2016;12: 875. doi: 10.15252/msb.20166941 27430939

24. Wiestner A, Schlemper RJ, Maas A van der, Skoda RC. An activating splice donor mutation in the thrombopoietin gene causes hereditary thrombocythaemia. Nat Genet. 1998;18: 49–52. doi: 10.1038/ng0198-49 9425899

25. Halperin DS, Pan C, Lusis AJ, Tontonoz P. Vestigial-like 3 is an inhibitor of adipocyte differentiation. J Lipid Res. 2013;54: 473–481. doi: 10.1194/jlr.M032755 23152581

26. Figeac N, Mohamed AD, Sun C, Schönfelder M, Matallanas D, Garcia-Munoz A, et al. VGLL3 operates via TEAD1, TEAD3 and TEAD4 to influence myogenesis in skeletal muscle. J Cell Sci. 2019;132: jcs225946. doi: 10.1242/jcs.225946 31138678

27. Kjaerner-Semb E, Ayllon F, Kleppe L, Sørhus E, Skaftnesmo K, Furmanek T, et al. Vgll3 and the Hippo pathway are regulated in Sertoli cells upon entry and during puberty in Atlantic salmon testis. Sci Rep. 2018;8: 1912. doi: 10.1038/s41598-018-20308-1 29382956

28. Kurko J, Debes PV, House A, Aykanat T, Erkinaro J, Primmer CR. Transcription Profiles of Age-at-Maturity-Associated Genes Suggest Cell Fate Commitment Regulation as a Key Factor in the Atlantic Salmon Maturation Process. G3 (Bethesda). 2019; g3.400882.2019. doi: 10.1534/g3.119.400882 31740454

29. Taranger GL, Carrillo M, Schulz RW, Fontaine P, Zanuy S, Felip A, et al. Control of puberty in farmed fish. Gen Comp Endocrinol. 2010;165: 483–515. doi: 10.1016/j.ygcen.2009.05.004 19442666

30. Debes PV, Piavchenko N, Ruokolainen A, Ovaskainen O, Moustakas-Verho JE, Parre N, et al. Large single-locus effects for maturation timing are mediated via condition variation in Atlantic salmon. bioRxiv. 2019;11: 780437. doi: 10.1101/780437

31. Schulz RW, Franca LR, Lareyre J-J, LeGac F, Chiarini-Garcia H, Nobrega RH, et al. Spermatogenesis in fish. Gen Comp Endocrinol. 2010;165: 390–411. doi: 10.1016/j.ygcen.2009.02.013 19348807

32. Pfennig F, Standke A, Gutzeit HO. The role of Amh signaling in teleost fish—Multiple functions not restricted to the gonads. Gen Comp Endocrinol. 2015;223: 87–107. doi: 10.1016/j.ygcen.2015.09.025 26428616

33. Morais R, Crespo D, Nobrega RH, Lemos MS, Kant HJG van de, Franca LR, et al. Antagonistic regulation of spermatogonial differentiation in zebrafish (Danio rerio) by Igf3 and Amh. Mol Cell Endocrinol. 2017;454: 112–124. doi: 10.1016/j.mce.2017.06.017 28645700

34. Skaftnesmo KO, Edvardsen RB, Furmanek T, Crespo D, Andersson E, Kleppe L, et al. Integrative testis transcriptome analysis reveals differentially expressed miRNAs and their mRNA targets during early puberty in Atlantic salmon. BMC Genomics. 2017;18: 801. doi: 10.1186/s12864-017-4205-5 29047327

35. Scrucca L, Fop M, Murphy TB, Raftery AE. mclust 5: Clustering, classification and density estimation using Gaussian finite mixture models. R journal. 2016;8: 289–317. doi: 10.1186/s12942-015-0017-5 27818791

36. Meng Z, Moroishi T, Guan K-L. Mechanisms of Hippo pathway regulation. Genes Dev. 2016;30: 1–17. doi: 10.1101/gad.274027.115 26728553

37. Simon E, Faucheux C, Zider A, Theze N, Thiebaud P. From vestigial to vestigial-like: the Drosophila gene that has taken wing. Dev Genes Evol. 2016;226: 297–315. doi: 10.1007/s00427-016-0546-3 27116603

38. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc. 2012;7: 562–578. doi: 10.1038/nprot.2012.016 22383036

39. Wittkopp PJ, Haerum BK, Clark AG. Evolutionary changes in cis and trans gene regulation. Nature. 2004;430: 85–88. doi: 10.1038/nature02698 15229602

40. Sendoel A, Dunn JG, Rodriguez EH, Naik S, Gomez NC, Hurwitz B, et al. Translation from unconventional 5′ start sites drives tumour initiation. Nature. 2017;541: 494–499. doi: 10.1038/nature21036 28077873

41. (DGT) TFC and the RP and C. A promoter-level mammalian expression atlas. Nature. 2014;507: 462–470. doi: 10.1038/nature13182 24670764

42. Burtis KC, Baker BS. Drosophila doublesex gene controls somatic sexual differentiation by producing alternatively spliced mRNAs encoding related sex-specific polypeptides. Cell. 1989;56: 997–1010. doi: 10.1016/0092-8674(89)90633-8 2493994

43. Barbosa-Morais NL, Irimia M, Pan Q, Xiong HY, Gueroussov S, Lee LJ, et al. The Evolutionary Landscape of Alternative Splicing in Vertebrate Species. Science. 2012;338: 1587–1593. doi: 10.1126/science.1230612 23258890

44. Gao Q, Sun W, Ballegeer M, Libert C, Chen W. Predominant contribution of cis-regulatory divergence in the evolution of mouse alternative splicing. Mol Syst Biol. 2015;11: 816. doi: 10.15252/msb.20145970 26134616

45. Haberle V, Start A. Eukaryotic core promoters and the functional basis of transcription initiation. Nat Rev Mol Cell Bio. 2018;10: 621–637. doi: 10.1038/s41580-018-0028-8 29946135

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. Schwartz C, Balasubramanian S, Warthmann N, Michael TP, Lempe J, Sureshkumar S, et al. Cis-regulatory Changes at FLOWERING LOCUS T Mediate Natural Variation in Flowering Responses of Arabidopsis thaliana. Genetics. 2009;183: 723–732. doi: 10.1534/genetics.109.104984 19652183

48. Chan YF, Marks ME, Jones FC, Villarreal G, Shapiro MD, Brady SD, et al. Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science. 2010;327: 302–305. doi: 10.1126/science.1182213 20007865

49. Frankel N, Erezyilmaz DF, McGregor AP, Wang S, Payre F, Stern DL. Morphological evolution caused by many subtle-effect substitutions in regulatory DNA. Nature. 2011;474: 598–603. doi: 10.1038/nature10200 21720363

50. O’Brown NM, Summers BR, Jones FC, Brady SD, Kingsley DM. A recurrent regulatory change underlying altered expression and Wnt response of the stickleback armor plates gene EDA. Elife. 2015;4. doi: 10.7554/elife.05290 25629660

51. Indjeian VB, Kingman GA, Jones FC, Guenther CA, Grimwood J, Schmutz J, et al. Evolving new skeletal traits by cis-regulatory changes in mone morphogenetic proteins. Cell. 2016;164: 45–56. doi: 10.1016/j.cell.2015.12.007 26774823

52. Gautier M, Yamaguchi J, Foucaud J, Loiseau A, Ausset A, Facon B, et al. The genomic basis of color pattern polymorphism in the harlequin ladybird. Curr Biol. 2018;28: 1–7. doi: 10.1016/j.cub.2017.11.007 29249662

53. Wang J, Liu S, Heallen T, Martin JF. The Hippo pathway in the heart: pivotal roles in development, disease, and regeneration. Nat Rev Cardiol. 2018;15: 672–684. doi: 10.1038/s41569-018-0063-3 30111784

54. Stern DL, Orgogozo V. The loci of evolution: how predictable is genetic evolution? Evolution. 2008;62: 2155–2177. doi: 10.1111/j.1558-5646.2008.00450.x 18616572

55. Price T, Schluter D. ON THE LOW HERITABILITY OF LIFE-HISTORY TRAITS. Evolution. 1991;45: 853–861. doi: 10.1111/j.1558-5646.1991.tb04354.x 28564058

56. Erkinaro J, Laine A, Maki-Petays A, Karjalainen TP, Laajala E, Hirvonen A, et al. Restoring migratory salmonid populations in regulated rivers in the northernmost Baltic Sea area, Northern Finland—biological, technical and social challenges. J Appl Ichthyol. 2011;27: 45–52. doi: 10.1111/j.1439-0426.2011.01851.x

57. Aykanat T, Lindqvist M, Pritchard VL, Primmer CR. From population genomics to conservation and management: a workflow for targeted analysis of markers identified using genome-wide approaches in Atlantic salmon Salmo salar. J Fish Biol. 2016;89: 2658–2679. doi: 10.1111/jfb.13149 27709620

58. Anderson EC. Computational algorithms and user-friendly software for parentage-based tagging of Pacific salmonids. Final report submitted to the Pacific Salmon Commission's Chinook Technical Committee (US Section). 2010: 46.

59. Sorensen DA, Genetics SA, 1995. Bayesian inference in threshold models using Gibbs sampling. Genet Sel Evol. 1995;27: 229–249.

60. Hadfield JD. Increasing the efficiency of MCMC for hierarchical phylogenetic models of categorical traits using reduced mixed models. O’Hara RB, editor. Methods in Ecology and Evolution. 2015;6: 706–714. doi: 10.1111/2041-210x.12354

61. R Core Team. R: A Language and Environment for Statistical Computing. 2013;

62. Hadfield J. MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J Stat Softw. 2010;33: 1–22. 20808728

63. Henderson C. Sire evaluation and genetic trends. J Anim Ecol. 1973; 10–43. doi: 10.1093/ansci/1973.symposium.10

64. Villemereuil P de, Gimenez O, Doligez B. Comparing parent–offspring regression with frequentist and Bayesian animal models to estimate heritability in wild populations: a simulation study for Gaussian and binary traits. Freckleton R, editor. Methods in Ecology and Evolution. 2013;4: 260–275. doi: 10.1111/2041-210x.12011

65. Heidelberger P, Welch PD. A spectral method for confidence interval generation and run length control in simulations. Commun ACM. 1981;24: 233–245. doi: 10.1145/358598.358630

66. Hindson CM, Chevillet JR, Briggs HA, Gallichotte EN, Ruf IK, Hindson BJ, et al. Absolute quantification by droplet digital PCR versus analog real-time PCR. Nat Meth. 2013;10: 1003–1005. doi: 10.1038/nmeth.2633 23995387

67. Laitinen RAE, Immanen J, Auvinen P, Rudd S, Alatalo E, Paulin L, et al. Analysis of the floral transcriptome uncovers new regulators of organ determination and gene families related to flower organ differentiation in Gerbera hybrida (Asteraceae). Genome Res. 2005;15: 475–486. doi: 10.1101/gr.3043705 15781570

68. Chen S, Zhou Y, Chen Y, Gu J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics. 2018;34: i884–i890. doi: 10.1093/bioinformatics/bty560 30423086

69. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2013;29: 15–21. doi: 10.1093/bioinformatics/bts635 23104886

70. Lien S, Koop BF, Sandve SR, Miller JR, Kent MP, Nome T, et al. The Atlantic salmon genome provides insights into rediploidization. Nature. 2016;533: 200–205. doi: 10.1038/nature17164 27088604

71. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome biol. 2014;15: 550. doi: 10.1186/s13059-014-0550-8 25516281

72. Abu-Jamous B, Kelly S. Clust: automatic extraction of optimal co-expressed gene clusters from gene expression data. Genome biol. 2018;19: 172. doi: 10.1186/s13059-018-1536-8 30359297

73. Yu G, Wang L-G, Han Y, He Q-Y. clusterProfiler: an R package for comparing biological themes among gene clusters. OMICS. 2012;16: 284–287. doi: 10.1089/omi.2011.0118 22455463

74. Garrido-Martín D, Palumbo E, Guigó R, Breschi A. ggsashimi: Sashimi plot revised for browser- and annotation-independent splicing visualization. Plos Comput Biol. 2018;14: e1006360. doi: 10.1371/journal.pcbi.1006360 30118475

75. Robinson JT, Thorvaldsdóttir H, Winckler W, Guttman M, Lander ES, Getz G, et al. Integrative genomics viewer. Nat biotechnol. 2011;29: 24–26. doi: 10.1038/nbt.1754 21221095

76. Verta J-P, Debes PV, Piavchenko N, Ruokolainen A, Ovaskainen O, Moustakas-Verho JE, et al. (2020) Data from: Cis-regulatory differences in isoform expression associate with life history strategy variation in Atlantic salmon. Dryad Digital Repository https://doi.org/10.5061/dryad.k6djh9w4w.


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2020 Číslo 9

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