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Transcriptional Rewiring of the Sex Determining Gene Duplicate by Transposable Elements


Control and coordination of eukaryotic gene expression rely on transcriptional and posttranscriptional regulatory networks. Evolutionary innovations and adaptations often require rapid changes of such networks. It has long been hypothesized that transposable elements (TE) might contribute to the rewiring of regulatory interactions. More recently it emerged that TEs might bring in ready-to-use transcription factor binding sites to create alterations to the promoters by which they were captured. A process where the gene regulatory architecture is of remarkable plasticity is sex determination. While the more downstream components of the sex determination cascades are evolutionary conserved, the master regulators can switch between groups of organisms even on the interspecies level or between populations. In the medaka fish (Oryzias latipes) a duplicated copy of dmrt1, designated dmrt1bY or DMY, on the Y chromosome was shown to be the master regulator of male development, similar to Sry in mammals. We found that the dmrt1bY gene has acquired a new feedback downregulation of its expression. Additionally, the autosomal dmrt1a gene is also able to regulate transcription of its duplicated paralog by binding to a unique target Dmrt1 site nested within the dmrt1bY proximal promoter region. We could trace back this novel regulatory element to a highly conserved sequence within a new type of TE that inserted into the upstream region of dmrt1bY shortly after the duplication event. Our data provide functional evidence for a role of TEs in transcriptional network rewiring for sub- and/or neo-functionalization of duplicated genes. In the particular case of dmrt1bY, this contributed to create new hierarchies of sex-determining genes.


Vyšlo v časopise: Transcriptional Rewiring of the Sex Determining Gene Duplicate by Transposable Elements. PLoS Genet 6(2): e32767. doi:10.1371/journal.pgen.1000844
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1000844

Souhrn

Control and coordination of eukaryotic gene expression rely on transcriptional and posttranscriptional regulatory networks. Evolutionary innovations and adaptations often require rapid changes of such networks. It has long been hypothesized that transposable elements (TE) might contribute to the rewiring of regulatory interactions. More recently it emerged that TEs might bring in ready-to-use transcription factor binding sites to create alterations to the promoters by which they were captured. A process where the gene regulatory architecture is of remarkable plasticity is sex determination. While the more downstream components of the sex determination cascades are evolutionary conserved, the master regulators can switch between groups of organisms even on the interspecies level or between populations. In the medaka fish (Oryzias latipes) a duplicated copy of dmrt1, designated dmrt1bY or DMY, on the Y chromosome was shown to be the master regulator of male development, similar to Sry in mammals. We found that the dmrt1bY gene has acquired a new feedback downregulation of its expression. Additionally, the autosomal dmrt1a gene is also able to regulate transcription of its duplicated paralog by binding to a unique target Dmrt1 site nested within the dmrt1bY proximal promoter region. We could trace back this novel regulatory element to a highly conserved sequence within a new type of TE that inserted into the upstream region of dmrt1bY shortly after the duplication event. Our data provide functional evidence for a role of TEs in transcriptional network rewiring for sub- and/or neo-functionalization of duplicated genes. In the particular case of dmrt1bY, this contributed to create new hierarchies of sex-determining genes.


Zdroje

1. Davidson

2006 The regulatory genome. Gene regulatory networks in development and evolution Burlington Elsevier 289

2. BrittenRJ

DavidsonEH

1969 Gene regulation for higher cells: a theory. Science 165 349 357

3. BrittenRJ

DavidsonEH

1971 Repetitive and non-repetitive DNA sequences and a speculation on the origins of evolutionary novelty. Q Rev Biol 46 111 138

4. BejeranoG

LoweCB

AhituvN

KingB

SiepelA

2006 A distal enhancer and an ultraconserved exon are derived from a novel retroposon. Nature 441 87 90

5. FeschotteC

2008 Transposable elements and the evolution of regulatory networks. Nat Rev Genet 9 397 405

6. LoweCE

CooperJD

BruskoT

WalkerNM

SmythDJ

2007 Large-scale genetic fine mapping and genotype-phenotype associations implicate polymorphism in the IL2RA region in type 1 diabetes. Nat Genet 39 1074 1082

7. FeschotteC

PrithamEJ

2007 DNA transposons and the evolution of eukaryotic genomes. Annu Rev Genet 41 331 368

8. Marino-RamirezL

LewisKC

LandsmanD

JordanIK

2005 Transposable elements donate lineage-specific regulatory sequences to host genomes. Cytogenet Genome Res 110 333 341

9. van de LagemaatLN

LandryJR

MagerDL

MedstrandP

2003 Transposable elements in mammals promote regulatory variation and diversification of genes with specialized functions. Trends Genet 19 530 536

10. Marino-RamirezL

JordanIK

2006 Transposable element derived DNaseI-hypersensitive sites in the human genome. Biol Direct 1 20

11. CharlesworthD

CharlesworthB

2005 Sex chromosomes: evolution of the weird and wonderful. Curr Biol 15 R129 131

12. HerpinA

SchartlM

2008 Regulatory putsches create new ways of determining sexual development. EMBO Rep

13. GrahamP

PennJK

SchedlP

2003 Masters change, slaves remain. Bioessays 25 1 4

14. RaymondCS

ShamuCE

ShenMM

SeifertKJ

HirschB

1998 Evidence for evolutionary conservation of sex-determining genes. Nature 391 691 695

15. RaymondCS

ParkerED

KettlewellJR

BrownLG

PageDC

1999 A region of human chromosome 9p required for testis development contains two genes related to known sexual regulators. Hum Mol Genet 8 989 996

16. NandaI

ShanZ

SchartlM

BurtDW

KoehlerM

1999 300 million years of conserved synteny between chicken Z and human chromosome 9. Nat Genet 21 258 259

17. ShettyS

KirbyP

ZarkowerD

GravesJA

2002 DMRT1 in a ratite bird: evidence for a role in sex determination and discovery of a putative regulatory element. Cytogenet Genome Res 99 245 251

18. MatsudaM

NagahamaY

ShinomiyaA

SatoT

MatsudaC

2002 DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature 417 559 563

19. NandaI

KondoM

HornungU

AsakawaS

WinklerC

2002 A duplicated copy of DMRT1 in the sex-determining region of the Y chromosome of the medaka, Oryzias latipes. Proc Natl Acad Sci U S A 99 11778 11783

20. YoshimotoS

OkadaE

UmemotoH

TamuraK

UnoY

2008 A W-linked DM-domain gene, DM-W, participates in primary ovary development in Xenopus laevis. Proc Natl Acad Sci U S A 105 2469 2474

21. MatsudaM

ShinomiyaA

KinoshitaM

SuzukiA

KobayashiT

2007 DMY gene induces male development in genetically female (XX) medaka fish. Proc Natl Acad Sci U S A 104 3865 3870

22. MatsudaM

2005 Sex determination in the teleost medaka, Oryzias latipes. Annu Rev Genet 39 293 307

23. SwainA

2002 Vertebrate sex determination: a new player in the field. Curr Biol 12 R602 603

24. RossAJ

CapelB

2005 Signaling at the crossroads of gonad development. Trends Endocrinol Metab 16 19 25

25. SekidoR

Lovell-BadgeR

2009 Sex determination and SRY: down to a wink and a nudge? Trends Genet 25 19 29

26. WilhelmD

PalmerS

KoopmanP

2007 Sex determination and gonadal development in mammals. Physiol Rev 87 1 28

27. SekidoR

Lovell-BadgeR

2008 Sex determination involves synergistic action of SRY and SF1 on a specific Sox9 enhancer. Nature 453 930 934

28. KleinjanDA

BancewiczRM

GautierP

DahmR

SchonthalerHB

2008 Subfunctionalization of duplicated zebrafish pax6 genes by cis-regulatory divergence. PLoS Genet 4 e29 doi:10.1371/journal.pgen.0040029

29. WoolfeA

ElgarG

2007 Comparative genomics using Fugu reveals insights into regulatory subfunctionalization. Genome Biol 8 R53

30. KondoM

HornungU

NandaI

ImaiS

SasakiT

2006 Genomic organization of the sex-determining and adjacent regions of the sex chromosomes of medaka. Genome Res 16 815 826

31. ChanTM

LongabaughW

BolouriH

ChenHL

TsengWF

2009 Developmental gene regulatory networks in the zebrafish embryo. Biochim Biophys Acta 1789 279 298

32. BrunnerB

HornungU

ShanZ

NandaI

KondoM

2001 Genomic organization and expression of the doublesex-related gene cluster in vertebrates and detection of putative regulatory regions for DMRT1. Genomics 77 8 17

33. WickerT

SabotF

Hua-VanA

BennetzenJL

CapyP

2007 A unified classification system for eukaryotic transposable elements. Nat Rev Genet 8 973 982

34. RoussigneM

KossidaS

LavigneAC

ClouaireT

EcochardV

2003 The THAP domain: a novel protein motif with similarity to the DNA-binding domain of P element transposase. Trends Biochem Sci 28 66 69

35. HagemannS

HammerSE

2006 The implications of DNA transposons in the evolution of P elements in zebrafish (Danio rerio). Genomics 88 572 579

36. HammerSE

StrehlS

HagemannS

2005 Homologs of Drosophila P transposons were mobile in zebrafish but have been domesticated in a common ancestor of chicken and human. Mol Biol Evol 22 833 844

37. QuesnevilleH

NouaudD

AnxolabehereD

2005 Recurrent recruitment of the THAP DNA-binding domain and molecular domestication of the P-transposable element. Mol Biol Evol 22 741 746

38. GaoS

ZhangT

ZhouX

ZhaoY

LiQ

2005 Molecular cloning, expression of Sox5 and its down-regulation of Dmrt1 transcription in zebrafish. J Exp Zoolog B Mol Dev Evol 304 476 483

39. PilonN

DaneauI

ParadisV

HamelF

LussierJG

2003 Porcine SRY promoter is a target for steroidogenic factor 1. Biol Reprod 68 1098 1106

40. MurphyMW

ZarkowerD

BardwellVJ

2007 Vertebrate DM domain proteins bind similar DNA sequences and can heterodimerize on DNA. BMC Mol Biol 8 58

41. KondoM

NandaI

HornungU

SchmidM

SchartlM

2004 Evolutionary origin of the medaka Y chromosome. Curr Biol 14 1664 1669

42. KobayashiT

MatsudaM

Kajiura-KobayashiH

SuzukiA

SaitoN

2004 Two DM domain genes, DMY and DMRT1, involved in testicular differentiation and development in the medaka, Oryzias latipes. Dev Dyn 231 518 526

43. HornungU

HerpinA

SchartlM

2007 Expression of the male determining gene dmrt1bY and its autosomal coorthologue dmrt1a in medaka. Sex Dev 1 197 206

44. HerpinA

NakamuraS

WagnerTU

TanakaM

SchartlM

2009 A highly conserved cis-regulatory motif directs differential gonadal synexpression of Dmrt1 transcripts during gonad development. Nucleic Acids Res 37 1510 1520

45. MeyerA

SchartlM

1999 Gene and genome duplications in vertebrates: the one-to-four (-to-eight in fish) rule and the evolution of novel gene functions. Curr Opin Cell Biol 11 699 704

46. MeyerA

Van de PeerY

2005 From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). Bioessays 27 937 945

47. PostlethwaitJ

AmoresA

CreskoW

SingerA

YanYL

2004 Subfunction partitioning, the teleost radiation and the annotation of the human genome. Trends Genet 20 481 490

48. WrightS

FinneganD

2001 Genome evolution: sex and the transposable element. Curr Biol 11 R296 299

49. FrazerKA

PachterL

PoliakovA

RubinEM

DubchakI

2004 VISTA: computational tools for comparative genomics. Nucleic Acids Res 32 W273 279

50. BrudnoM

MaldeS

PoliakovA

DoCB

CouronneO

2003 Glocal alignment: finding rearrangements during alignment. Bioinformatics 19 Suppl 1 i54 62

51. HallTA

1999 BioEdit: a user -friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp 41 95 98

52. TamuraK

DudleyJ

NeiM

KumarS

2007 MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24 1596 1599

53. LemaireP

GarrettN

GurdonJB

1995 Expression cloning of Siamois, a Xenopus homeobox gene expressed in dorsal-vegetal cells of blastulae and able to induce a complete secondary axis. Cell 81 85 94

54. BeverdamA

WilhelmD

KoopmanP

2003 Molecular characterization of three gonad cell lines. Cytogenet Genome Res 101 242 249

55. HongY

LiuT

ZhaoH

XuH

WangW

2004 Establishment of a normal medakafish spermatogonial cell line capable of sperm production in vitro. Proc Natl Acad Sci U S A 101 8011 8016

56. KomuraJ

MitaniH

ShimaA

1988 Fish cell culture: Establishment of two fibroblast-like cell lines (OL-17 and OL-32) from fins of the medaka, Oryzias latipes. In Vitro Cellular & Developmental Biology 24 294 298

57. KuhnC

VielkindU

AndersF

1979 Cell cultures derived from embryos and melanoma of poeciliid fish. In Vitro 15 537 544

58. AltschmiedJ

DuschlJ

1997 Set of optimized luciferase reporter gene plasmids compatible with widely used CAT vectors. Biotechniques 23 436 438

59. ThermesV

GrabherC

RistoratoreF

BourratF

ChoulikaA

2002 I-SceI meganuclease mediates highly efficient transgenesis in fish. Mech Dev 118 91 98

60. AltschmiedJ

HornungU

SchluppI

GadauJ

KolbR

1997 Isolation of DNA suitable for PCR for field and laboratory work. Biotechniques 23 228 229

61. HerpinA

SchindlerD

KraissA

HornungU

WinklerC

2007 Inhibition of primordial germ cell proliferation by the medaka male determining gene Dmrt I bY. BMC Dev Biol 7 99

62. NakamuraS

SaitoD

TanakaM

2008 Generation of transgenic medaka using modified bacterial artificial chromosome. Dev Growth Differ 50 415 419

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