#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Environmental Sex Determination in the Branchiopod Crustacean : Deep Conservation of a Gene in the Sex-Determining Pathway


Sex-determining mechanisms are diverse among animal lineages and can be broadly divided into two major categories: genetic and environmental. In contrast to genetic sex determination (GSD), little is known about the molecular mechanisms underlying environmental sex determination (ESD). The Doublesex (Dsx) genes play an important role in controlling sexual dimorphism in genetic sex-determining organisms such as nematodes, insects, and vertebrates. Here we report the identification of two Dsx genes from Daphnia magna, a freshwater branchiopod crustacean that parthenogenetically produces males in response to environmental cues. One of these genes, designated DapmaDsx1, is responsible for the male trait development when expressed during environmental sex determination. The domain organization of DapmaDsx1 was similar to that of Dsx from insects, which are thought to be the sister group of branchiopod crustaceans. Intriguingly, the molecular basis for sexually dimorphic expression of DapmaDsx1 is different from that of insects. Rather than being regulated sex-specifically at the level of pre–mRNA splicing in the coding region, DapmaDsx1 exhibits sexually dimorphic differences in the abundance of its transcripts. During embryogenesis, expression of DapmaDsx1 was increased only in males and its transcripts were primarily detected in male-specific structures. Knock-down of DapmaDsx1 in male embryos resulted in the production of female traits including ovarian maturation, whereas ectopic expression of DapmaDsx1 in female embryos resulted in the development of male-like phenotypes. Expression patterns of another D. magna Dsx gene, DapmaDsx2, were similar to those of DapmaDsx1, but silencing and overexpression of this gene did not induce any clear phenotypic changes. These results establish DapmaDsx1 as a key regulator of the male phenotype. Our findings reveal how ESD is implemented by selective expression of a fundamental genetic component that is functionally conserved in animals using GSD. We infer that there is an ancient, previously unidentified link between genetic and environmental sex determination.


Vyšlo v časopise: Environmental Sex Determination in the Branchiopod Crustacean : Deep Conservation of a Gene in the Sex-Determining Pathway. PLoS Genet 7(3): e32767. doi:10.1371/journal.pgen.1001345
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1001345

Souhrn

Sex-determining mechanisms are diverse among animal lineages and can be broadly divided into two major categories: genetic and environmental. In contrast to genetic sex determination (GSD), little is known about the molecular mechanisms underlying environmental sex determination (ESD). The Doublesex (Dsx) genes play an important role in controlling sexual dimorphism in genetic sex-determining organisms such as nematodes, insects, and vertebrates. Here we report the identification of two Dsx genes from Daphnia magna, a freshwater branchiopod crustacean that parthenogenetically produces males in response to environmental cues. One of these genes, designated DapmaDsx1, is responsible for the male trait development when expressed during environmental sex determination. The domain organization of DapmaDsx1 was similar to that of Dsx from insects, which are thought to be the sister group of branchiopod crustaceans. Intriguingly, the molecular basis for sexually dimorphic expression of DapmaDsx1 is different from that of insects. Rather than being regulated sex-specifically at the level of pre–mRNA splicing in the coding region, DapmaDsx1 exhibits sexually dimorphic differences in the abundance of its transcripts. During embryogenesis, expression of DapmaDsx1 was increased only in males and its transcripts were primarily detected in male-specific structures. Knock-down of DapmaDsx1 in male embryos resulted in the production of female traits including ovarian maturation, whereas ectopic expression of DapmaDsx1 in female embryos resulted in the development of male-like phenotypes. Expression patterns of another D. magna Dsx gene, DapmaDsx2, were similar to those of DapmaDsx1, but silencing and overexpression of this gene did not induce any clear phenotypic changes. These results establish DapmaDsx1 as a key regulator of the male phenotype. Our findings reveal how ESD is implemented by selective expression of a fundamental genetic component that is functionally conserved in animals using GSD. We infer that there is an ancient, previously unidentified link between genetic and environmental sex determination.


Zdroje

1. MarinI

BakerBS

1998

The evolutionary dynamics of sex determination.

Science

281

1990

1994

2. ZarkowerD

2001

Establishing sexual dimorphism: conservation amidst diversity?

Nat Rev Genet

2

175

185

3. BullJJ

1985

Sex determining mechanisms: an evolutionary perspective.

Experientia

41

1285

1296

4. CrewsD

BullJJ

2009

Mode and tempo in environmental sex determination in vertebrates.

Semin Cell Dev Biol

20

251

255

5. KorpelainenH

1990

Sex-Ratios and conditions required for environmental sex determination in animals.

Biol Rev Camb Philos Soc

65

147

184

6. BullJJ

VogtRC

1979

Temperature-dependent sex Determination in turtles.

Science

206

1186

1188

7. OrganCL

JanesDE

2008

Evolution of sex chromosomes in Sauropsida.

Integ Comp Biol

48

512

519

8. WarnerDA

ShineR

2008

The adaptive significance of temperature-dependent sex determination in a reptile.

Nature

451

566-U565

9. BullJJ

1981

Evolution of environmental sex determination from genotypic sex determination.

Heredity

47

173

184

10. BulmerMG

BullJJ

1982

Models of polygenic sex determination and sex-ratio control.

Evolution

36

13

26

11. EpperF

BryantPJ

1983

Sex-specific control of growth and differentiation in the Drosophila genital disk, studied using a temperature-sensitive transformer-2 mutation.

Dev Biol

100

294

307

12. HodgkinJ

2002

Exploring the envelope: Systematic alteration in the sex-determination system of the nematode Caeraorhabditis elegans.

Genetics

162

767

780

13. ShoemakerCM

CrewsD

2009

Analyzing the coordinated gene network underlying temperature-dependent sex determination in reptiles.

Semin Cell Dev Biol

20

293

303

14. HebertPDN

1978

The population biology of Daphnia (Crustacea, Daphnidae).

Biol Rev

53

387

426

15. OlmsteadAW

LeBlancGA

2000

Effects of endocrine-active chemicals on the development of sex characteristics of Daphnia magna.

Environ Toxicol Chem

19

2107

2113

16. MitchellSE

2001

Intersex and male development in Daphnia magna.

Hydrobiologia

442

145

156

17. SagawaK

YamagataH

ShigaY

2005

Exploring embryonic germ line development in the water flea, Daphnia magna, by zinc-finger-containing VASA as a marker.

Gene Expr Patterns

5

669

678

18. ZaffagniniF

1987

Reproduction in Daphnia.

Mem Inst Ital Idrobiol

45

245

284

19. OjimaY

1958

A cytological study on the development and maturation of the parthenogenetic and sexual eggs of Daphnia pulex (Crustacea–Cladocera).

Kwansei Gakuen Univ Ann Stud

6

123

176

20. StrossRG

HillJC

1965

Diapause induction in Daphnia requires two stimuli.

Science

150

1462

1464

21. HebertPD

1987

Genotypic characteristics of cyclic parthenogens and their obligately asexual derivatives.

Experientia Suppl

55

175

195

22. OlmsteadAW

LeblancGA

2002

Juvenoid hormone methyl farnesoate is a sex determinant in the crustacean Daphnia magna.

J Exp Zool

293

736

739

23. OdaS

TatarazakoN

WatanabeH

MoritaM

IguchiT

2005

Production of male neonates in four cladoceran species exposed to a juvenile hormone analog, fenoxycarb.

Chemosphere

60

74

78

24. BantaAM

BrownLA

1929

Control of sex in cladocera. III. Localization of the critical period for control of sex.

Proc Natl Acad Sci U S A

15

71

81

25. TatarazakoN

OdaS

WatanabeH

MoritaM

IguchiT

2003

Juvenile hormone agonists affect the occurrence of male Daphnia.

Chemosphere

53

827

833

26. KatoY

KobayashiK

OdaS

TatarazakoN

WatanabeH

2010

Sequence divergence and expression of a transformer gene in the branchiopod crustacean, Daphnia magna.

Genomics

95

160

165

27. WatanabeH

TatarazakoN

OdaS

NishideH

UchiyamaI

2005

Analysis of expressed sequence tags of the water flea Daphnia magna.

Genome

48

606

609

28. ColbourneJK

SinganVR

GilbertDG

2005

wFleaBase: The Daphnia genome database.

BMC Bioinformatics

6

45

29. ShawJR

PfrenderME

EadsBD

KlaperR

CallaghanA

ColsonI

JansenB

GilbertD

ColbourneJK

2008

Daphnia as an emerging model for toxicological genomics.

Adv Exp Biol

2

165

219

327-328

30. ColbourneJK

PfrenderME

GilbertD

ThomasWK

TuckerA

2011

The ecoresponsive genome of Daphnia pulex.

Science

331

555

561

31. SchuttC

NothigerR

2000

Structure, function and evolution of sex-determining systems in Dipteran insects.

Development

127

667

677

32. ZarkowerD

2006

Somatic sex determination.

WormBook

1

12

33. SekidoR

Lovell-BadgeR

2009

Sex determination and SRY: down to a wink and a nudge?

Trends Genet

25

19

29

34. BurtisKC

BakerBS

1989

Drosophila doublesex gene controls somatic sexual differentiation by producing alternatively spliced mRNAs encoding related sex-specific polypeptides.

Cell

56

997

1010

35. VolffJN

ZarkowerD

BardwellVJ

SchartlM

2003

Evolutionary dynamics of the DM domain gene family in metazoans.

J Mol Evol

57

Suppl 1

S241

249

36. BayrerJR

ZhangW

WeissMA

2005

Dimerization of doublesex is mediated by a cryptic ubiquitin-associated domain fold - Implications for sex-specific gene regulation.

J Biol Chem

280

32989

32996

37. ShenMM

HodgkinJ

1988

mab-3, a gene required for sex-specific yolk protein expression and a male-specific lineage in C. elegans.

Cell

54

1019

1031

38. RaymondCS

ShamuCE

ShenMM

SeifertKJ

HirschB

1998

Evidence for evolutionary conservation of sex-determining genes.

Nature

391

691

695

39. RaymondCS

MurphyMW

O'SullivanMG

BardwellVJ

ZarkowerD

2000

Dmrt1, a gene related to worm and fly sexual regulators, is required for mammalian testis differentiation.

Genes Dev

14

2587

2595

40. WilliamsTM

CarrollSB

2009

Genetic and molecular insights into the development and evolution of sexual dimorphism.

Nature Rev Genet

10

883

883

41. KatoY

ShigaY

KobayashiK

TokishitaS

YamagataH

2011

Development of an RNA interference method in the cladoceran crustacean Daphnia magna.

Dev Genes Evol In press

42. GlennerH

ThomsenPF

HebsgaardMB

SorensenMV

WillerslevE

2006

The origin of insects.

Science

314

1883

1884

43. KatoY

KobayashiK

OdaS

ColbourneJK

TatarazakoN

2008

Molecular cloning and sexually dimorphic expression of DM-domain genes in Daphnia magna.

Genomics

91

94

101

44. RegierJC

ShultzJW

1997

Molecular phylogeny of the major arthropod groups indicates polyphyly of crustaceans and a new hypothesis for the origin of hexapods.

Mol Biol Evol

14

902

913

45. RegierJC

ShultzJW

KambicRE

2005

Pancrustacean phylogeny: hexapods are terrestrial crustaceans and maxillopods are not monophyletic.

Proc Biol Sci

272

395

401

46. MallattJ

WinchellCJ

2007

Ribosomal RNA genes and deuterostome phylogeny revisited: more cyclostomes, elasmobranchs, reptiles, and a brittle star.

Mol Phylogenet Evol

43

1005

1022

47. AverofM

AkamM

1995

Hox genes and the diversification of insect and crustacean body plans.

Nature

376

420

423

48. AverofM

CohenSM

1997

Evolutionary origin of insect wings from ancestral gills.

Nature

385

627

630

49. OdaS

TatarazakoN

WatanabeH

MoritaM

IguchiT

2005

Production of male neonates in Daphnia magna (Cladocera, Crustacea) exposed to juvenile hormones and their analogs.

Chemosphere

61

1168

1174

50. KatoY

KobayashiK

WatanabeH

IguchiT

2010

Introduction of foreign DNA into the water flea, Daphnia magna, by electroporation.

Ecotoxicology

19

589

592

51. 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

52. 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

53. SmithCA

RoeszlerKN

OhnesorgT

CumminsDM

FarliePG

2009

The avian Z-linked gene DMRT1 is required for male sex determination in the chicken.

Nature

461

267

271

54. KettlewellJR

RaymondCS

ZarkowerD

2000

Temperature-dependent expression of turtle Dmrt1 prior to sexual differentiation.

Genesis

26

174

178

55. MurdockC

WibbelsT

2006

Dmrt1 expression in response to estrogen treatment in a reptile with temperature-dependent sex determination.

J Exp Zool B Mol Dev Evol

306

134

139

56. ShoemakerC

RamseyM

QueenJ

CrewsD

2007

Expression of Sox9, Mis, and Dmrt1 in the gonad of a species with temperature-dependent sex determination.

Dev Dyn

236

1055

1063

57. HildrethPE

1965

Doublesex, recessive gene that transforms both males and females of Drosophila into intersexes.

Genetics

51

659

678

58. OliverB

KimYJ

BakerBS

1993

Sex-lethal, master and slave: a hierarchy of germ-line sex determination in Drosophila.

Development

119

897

908

59. BakerBS

RidgeKA

1980

Sex and the single cell. I. On the action of major loci affecting sex determination in Drosophila melanogaster.

Genetics

94

383

423

60. RobinettCC

VaughanAG

KnappJM

BakerBS

2010

Sex and the single cell. II. There is a time and place for sex.

PLoS Biol

8

e1000365

doi:10.1371/journal.pbio.1000365

61. McKeownM

BeloteJM

BakerBS

1987

A molecular analysis of transformer, a gene in Drosophila melanogaster that controls female sexual differentiation.

Cell

48

489

499

62. PaneA

SalveminiM

Delli BoviP

PolitoC

SacconeG

2002

The transformer gene in Ceratitis capitata provides a genetic basis for selecting and remembering the sexual fate.

Development

129

3715

3725

63. HedigerM

HenggelerC

MeierN

PerezR

SacconeG

2010

Molecular characterization of the key switch F provides a basis for understanding the rapid divergence of the sex-determining pathway in the housefly.

Genetics

184

155

170

64. GempeT

HasselmannM

SchiottM

HauseG

OtteM

2009

Sex determination in honeybees: Two separate mechanisms induce and maintain the female pathway.

Plos Biol

7

e1000222

doi:10.1371/journal.pbio.1000222

65. FujiiT

ShimadaT

2007

Sex determination in the silkworm, Bombyx mori: A female determinant on the W chromosome and the sex-determining gene cascade.

Semin Cell Dev Biol

18

379

388

66. VerhulstEC

van de ZandeL

BeukeboomLW

2010

Insect sex determination: it all evolves around transformer.

Curr Opin Genet Dev

20

376

383

67. LiY

ZhangZ

RobinsonGE

PalliSR

2007

Identification and characterization of a juvenile hormone response element and its binding proteins.

J Biol Chem

282

37605

37617

68. GorrTA

RiderCV

WangHY

OlmsteadAW

LeBlancGA

2006

A candidate juvenoid hormone receptor cis-element in the Daphnia magna hb2 hemoglobin gene promoter.

Mol Cell Endocrinol

247

91

102

69. HughesTA

2006

Regulation of gene expression by alternative untranslated regions.

Trends in Genetics

22

119

122

70. JiZ

LeeJY

PanZH

JiangBJ

TianB

2009

Progressive lengthening of 3' untranslated regions of mRNAs by alternative polyadenylation during mouse embryonic development.

Proc Natl Acad Sci U S A

106

7028

7033

71. RonshaugenM

McGinnisN

McGinnisW

2002

Hox protein mutation and macroevolution of the insect body plan.

Nature

415

914

917

72. WilkinsAS

1995

Moving up the hierarchy - a hypothesis on the evolution of a genetic sex determination pathway.

Bioessays

17

71

77

73. NothigerR

SteinmannzwickyM

1985

A single principle for sex determination in insects.

Cold Spring Harb Symp Quant Biol

50

615

621

74. ThompsonJD

HigginsDG

GibsonTJ

1994

CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.

Nucleic Acids Res

22

4673

4680

75. TamuraK

DudleyJ

NeiM

KumarS

2007

MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0.

Mol Biol Evol

24

1596

1599

76. ButlerK

ZornAM

GurdonJB

2001

Nonradioactive in situ hybridization to Xenopus tissue sections.

Methods

23

303

312

77. ElendtBP

BiasWR

1990

Trace nutrient deficiency in Daphnia magna cultured in standard medium for toxicity testing. Effects of the optimization of culture conditions on life history parameters of D. magna.

Water Res

24

1157

1167

78. PomiankowskiA

NothigerR

WilkinsA

2004

The evolution of the Drosophila sex-determination pathway.

Genetics

166

1761

1773

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2011 Číslo 3
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#