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Environmental and Genetic Determinants of Colony Morphology in Yeast


Nutrient stresses trigger a variety of developmental switches in the budding yeast Saccharomyces cerevisiae. One of the least understood of such responses is the development of complex colony morphology, characterized by intricate, organized, and strain-specific patterns of colony growth and architecture. The genetic bases of this phenotype and the key environmental signals involved in its induction have heretofore remained poorly understood. By surveying multiple strain backgrounds and a large number of growth conditions, we show that limitation for fermentable carbon sources coupled with a rich nitrogen source is the primary trigger for the colony morphology response in budding yeast. Using knockout mutants and transposon-mediated mutagenesis, we demonstrate that two key signaling networks regulating this response are the filamentous growth MAP kinase cascade and the Ras-cAMP-PKA pathway. We further show synergistic epistasis between Rim15, a kinase involved in integration of nutrient signals, and other genes in these pathways. Ploidy, mating-type, and genotype-by-environment interactions also appear to play a role in the controlling colony morphology. Our study highlights the high degree of network reuse in this model eukaryote; yeast use the same core signaling pathways in multiple contexts to integrate information about environmental and physiological states and generate diverse developmental outputs.


Vyšlo v časopise: Environmental and Genetic Determinants of Colony Morphology in Yeast. PLoS Genet 6(1): e32767. doi:10.1371/journal.pgen.1000823
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1000823

Souhrn

Nutrient stresses trigger a variety of developmental switches in the budding yeast Saccharomyces cerevisiae. One of the least understood of such responses is the development of complex colony morphology, characterized by intricate, organized, and strain-specific patterns of colony growth and architecture. The genetic bases of this phenotype and the key environmental signals involved in its induction have heretofore remained poorly understood. By surveying multiple strain backgrounds and a large number of growth conditions, we show that limitation for fermentable carbon sources coupled with a rich nitrogen source is the primary trigger for the colony morphology response in budding yeast. Using knockout mutants and transposon-mediated mutagenesis, we demonstrate that two key signaling networks regulating this response are the filamentous growth MAP kinase cascade and the Ras-cAMP-PKA pathway. We further show synergistic epistasis between Rim15, a kinase involved in integration of nutrient signals, and other genes in these pathways. Ploidy, mating-type, and genotype-by-environment interactions also appear to play a role in the controlling colony morphology. Our study highlights the high degree of network reuse in this model eukaryote; yeast use the same core signaling pathways in multiple contexts to integrate information about environmental and physiological states and generate diverse developmental outputs.


Zdroje

1. GagianoM

BauerFF

PretoriusIS

2002 The sensing of nutritional status and the relationship to filamentous growth in Saccharomyces cerevisiae. FEMS Yeast Res 2 433 470

2. GancedoJM

2001 Control of pseudohyphae formation in Saccharomyces cerevisiae. FEMS Microbiol Rev 25 107 123

3. PanX

HarashimaT

HeitmanJ

2000 Signal transduction cascades regulating pseudohyphal differentiation of Saccharomyces cerevisiae. Curr Opin Microbiol 3 567 572

4. CullenPJ

SpragueGF

2000 Glucose depletion causes haploid invasive growth in yeast. Proc Natl Acad Sci USA 97 13619 13624

5. DickinsonJR

2008 Filament formation in Saccharomyces cerevisiae–a review. Folia Microbiol (Praha) 53 3 14

6. KernK

NunnCD

PichovaA

DickinsonJR

2004 Isoamyl alcohol-induced morphological change in Saccharomyces cerevisiae involves increases in mitochondria and cell wall chitin content. FEMS Yeast Res 5 43 49

7. LorenzMC

CutlerNS

HeitmanJ

2000 Characterization of alcohol-induced filamentous growth in Saccharomyces cerevisiae. Mol Biol Cell 11 183 199

8. DeutschbauerAM

WilliamsRM

ChuAM

DavisRW

2002 Parallel phenotypic analysis of sporulation and postgermination growth in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 99 15530 15535

9. KupiecM

ByersB

EspositoR

MitchellAP

1997 Meiosis and sporulation in Saccharomyces cerevisiae. The Molecular Biology of the Yeast Saccharomyces 889 1036

10. NeimanAM

2005 Ascospore formation in the yeast Saccharomyces cerevisiae. Microbiol Mol Biol Rev 69 565 584

11. PrimigM

WilliamsRM

WinzelerEA

TevzadzeGG

ConwayAR

2000 The core meiotic transcriptome in budding yeasts. Nat Genet 26 415 423

12. ReynoldsTB

FinkGR

2001 Bakers' yeast, a model for fungal biofilm formation. Science 291 878 881

13. EngelbergD

MimranA

MartinettoH

OttoJ

SimchenG

1998 Multicellular stalk-like structures in Saccharomyces cerevisiae. J Bacteriol 180 3992 3996

14. VerstrepenKJ

KlisFM

2006 Flocculation, adhesion and biofilm formation in yeasts. Mol Microbiol 60 5 15

15. ChenH

FinkGR

2006 Feedback control of morphogenesis in fungi by aromatic alcohols. Genes Dev 20 1150 1161

16. KuthanM

DevauxF

JanderováB

SlaninováI

JacqC

2003 Domestication of wild Saccharomyces cerevisiae is accompanied by changes in gene expression and colony morphology. Mol Microbiol 47 745 754

17. PalkováZ

VáchováL

2006 Life within a community: benefit to yeast long-term survival. FEMS Microbiol Rev 30 806 824

18. VaronM

ChoderM

2000 Organization and cell-cell interaction in starved Saccharomyces cerevisiae colonies. J Bacteriol 182 3877 3880

19. VopálenskáI

HůlkováM

JanderováB

PalkováZ

2005 The morphology of Saccharomyces cerevisiae colonies is affected by cell adhesion and the budding pattern. Res Microbiol 156 921 931

20. GrosbergRK

StrathmannRR

2007 The Evolution of Multicellularity: A Minor Major Transition? Annual Review of Ecology, Evolution, and Systematics 38 621 654

21. AguilarC

VlamakisH

LosickR

KolterR

2007 Thinking about Bacillus subtilis as a multicellular organism. Curr Opin Microbiol

22. MagasanikB

1991 The Molecular and cellular biology of the yeast Saccharomyces;

BroachJR

PringleJR

JonesEW

Cold Spring Harbor, N.Y. Cole Spring Harbor Laboratory Press

23. ZamanS

LippmanSI

ZhaoX

BroachJR

2008 How Saccharomyces responds to nutrients. Annu Rev Genet 42 27 81

24. MagwenePM

2009 Pleiotropy and Tradeoffs in Yeast Development. Submitted

25. LorenzMC

HeitmanJ

1997 Yeast pseudohyphal growth is regulated by GPA2, a G protein alpha homolog. EMBO J 16 7008 7018

26. DreesB

ThorssonV

CarterG

RivesA

RaymondM

2005 Derivation of genetic interaction networks from quantitative phenotype data. Genome Biol 6 R38

27. Styles CA History of Sigma

28. McCleanMN

ModyA

BroachJR

RamanathanS

2007 Cross-talk and decision making in MAP kinase pathways. Nat Genet 39 409 414

29. O'RourkeSM

HerskowitzI

1998 The Hog1 MAPK prevents cross talk between the HOG and pheromone response MAPK pathways in Saccharomyces cerevisiae. Genes Dev 12 2874 2886

30. ShockTR

ThompsonJ

YatesJR3rd

MadhaniHD

2009 Hog1 MAP kinase interrupts signal transduction between the Kss1 MAP kinase and the Tec1 transcription factor to maintain pathway specificity. Eukaryot Cell

31. KumarA

SeringhausM

BieryMC

SarnovskyRJ

UmanskyL

2004 Large-scale mutagenesis of the yeast genome using a Tn7-derived multipurpose transposon. Genome Res 14 1975 1986

32. AbdullahU

CullenPJ

2009 The tRNA modification complex elongator regulates the Cdc42-dependent mitogen-activated protein kinase pathway that controls filamentous growth in yeast. Eukaryot Cell 8 1362 1372

33. FischerC

ValeriusO

RupprechtH

DumkowM

KrappmannS

2008 Posttranscriptional regulation of FLO11 upon amino acid starvation in Saccharomyces cerevisiae. FEMS Yeast Res 8 225 236

34. TackettAJ

DilworthDJ

DaveyMJ

O'DonnellM

AitchisonJD

2005 Proteomic and genomic characterization of chromatin complexes at a boundary. J Cell Biol 169 35 47

35. BarralesRR

JimenezJ

IbeasJI

2008 Identification of novel activation mechanisms for FLO11 regulation in Saccharomyces cerevisiae. Genetics 178 145 156

36. JinR

DobryCJ

McCownPJ

KumarA

2008 Large-scale analysis of yeast filamentous growth by systematic gene disruption and overexpression. Mol Biol Cell 19 284 296

37. GrayM

PiccirilloS

PurnapatreK

SchneiderBL

HonigbergSM

2008 Glucose induction pathway regulates meiosis in Saccharomyces cerevisiae in part by controlling turnover of Ime2p meiotic kinase. FEMS Yeast Res 8 676 684

38. SudaY

RodriguezRK

ColuccioAE

NeimanAM

2009 A screen for spore wall permeability mutants identifies a secreted protease required for proper spore wall assembly. PLoS One 4 e7184 doi:10.1371/journal.pone.0007184

39. SwinnenE

WankeV

RoosenJ

SmetsB

DuboulozF

2006 Rim15 and the crossroads of nutrient signalling pathways in Saccharomyces cerevisiae. Cell Div 1 3

40. VidanS

MitchellAP

1997 Stimulation of yeast meiotic gene expression by the glucose-repressible protein kinase Rim15p. Mol Cell Biol 17 2688 2697

41. PanX

HeitmanJ

1999 Cyclic AMP-dependent protein kinase regulates pseudohyphal differentiation in Saccharomyces cerevisiae. Mol Cell Biol 19 4874 4887

42. GalitskiT

SaldanhaAJ

StylesCA

LanderES

FinkGR

1999 Ploidy regulation of gene expression. Science 285 251 254

43. LitiG

CarterDM

MosesAM

WarringerJ

PartsL

2009 Population genomics of domestic and wild yeasts. Nature

44. ReynoldsTB

JansenA

PengX

FinkGR

2008 Mat formation in Saccharomyces cerevisiae requires nutrient and pH gradients. Eukaryotic Cell 7 122 130

45. PalecekSP

ParikhAS

KronSJ

2002 Sensing, signalling and integrating physical processes during Saccharomyces cerevisiae invasive and filamentous growth. Microbiology 148 893 907

46. ElionEA

2000 Pheromone response, mating and cell biology. Curr Opin Microbiol 3 573 581

47. BardwellL

CookJG

Zhu-ShimoniJX

VooraD

ThornerJ

1998 Differential regulation of transcription: repression by unactivated mitogen-activated protein kinase Kss1 requires the Dig1 and Dig2 proteins. Proc Natl Acad Sci U S A 95 15400 15405

48. ChouS

LaneS

LiuH

2006 Regulation of mating and filamentation genes by two distinct Ste12 complexes in Saccharomyces cerevisiae. Mol Cell Biol 26 4794 4805

49. CullenPJ

SabbaghW,Jr.

GrahamE

IrickMM

van OldenEK

2004 A signaling mucin at the head of the Cdc42- and MAPK-dependent filamentous growth pathway in yeast. Genes Dev 18 1695 1708

50. GimenoCJ

LjungdahlPO

StylesCA

FinkGR

1992 Unipolar cell divisions in the yeast S. cerevisiae lead to filamentous growth: regulation by starvation and RAS. Cell 68 1077 1090

51. HalmeA

BumgarnerS

StylesC

FinkGR

2004 Genetic and epigenetic regulation of the FLO gene family generates cell-surface variation in yeast. Cell 116 405 415

52. TanakaK

LinBK

WoodDR

TamanoiF

1991 IRA2, an upstream negative regulator of RAS in yeast, is a RAS GTPase-activating protein. Proc Natl Acad Sci U S A 88 468 472

53. RobertsonLS

CaustonHC

YoungRA

FinkGR

2000 The yeast A kinases differentially regulate iron uptake and respiratory function. Proc Natl Acad Sci U S A 97 5984 5988

54. RobertsonLS

FinkGR

1998 The three yeast A kinases have specific signaling functions in pseudohyphal growth. Proc Natl Acad Sci USA 95 13783 13787

55. MaP

WeraS

Van DijckP

TheveleinJM

1999 The PDE1-encoded low-affinity phosphodiesterase in the yeast Saccharomyces cerevisiae has a specific function in controlling agonist-induced cAMP signaling. Mol Biol Cell 10 91 104

56. LorenzMC

HeitmanJ

1998 The MEP2 ammonium permease regulates pseudohyphal differentiation in Saccharomyces cerevisiae. EMBO J 17 1236 1247

57. LoWS

DranginisAM

1996 FLO11, a yeast gene related to the STA genes, encodes a novel cell surface flocculin. J Bacteriol 178 7144 7151

58. PalecekSP

ParikhAS

KronSJ

2000 Genetic analysis reveals that FLO11 upregulation and cell polarization independently regulate invasive growth in Saccharomyces cerevisiae. Genetics 156 1005 1023

59. LoWS

DranginisAM

1998 The cell surface flocculin Flo11 is required for pseudohyphae formation and invasion by Saccharomyces cerevisiae. Mol Biol Cell 9 161 171

60. GagianoM

van DykD

BauerFF

LambrechtsMG

PretoriusIS

1999 Msn1p/Mss10p, Mss11p and Muc1p/Flo11p are part of a signal transduction pathway downstream of Mep2p regulating invasive growth and pseudohyphal differentiation in Saccharomyces cerevisiae. Mol Microbiol 31 103 116

61. SuSS

MitchellAP

1993 Identification of functionally related genes that stimulate early meiotic gene expression in yeast. Genetics 133 67 77

62. PedruzziI

DuboulozF

CameroniE

WankeV

RoosenJ

2003 TOR and PKA signaling pathways converge on the protein kinase Rim15 to control entry into G0. Mol Cell 12 1607 1613

63. RoosenJ

EngelenK

MarchalK

MathysJ

GriffioenG

2005 PKA and Sch9 control a molecular switch important for the proper adaptation to nutrient availability. Mol Microbiol 55 862 880

64. WeiM

FabrizioP

HuJ

GeH

ChengC

2008 Life span extension by calorie restriction depends on Rim15 and transcription factors downstream of Ras/PKA, Tor, and Sch9. PLoS Genet 4 e13 doi:10.1371/journal.pgen.0040013

65. CameroniE

HuloN

RoosenJ

WinderickxJ

De VirgilioC

2004 The novel yeast PAS kinase Rim 15 orchestrates G0-associated antioxidant defense mechanisms. Cell Cycle 3 462 468

66. KaiserC

MichaelisS

MitchellA

Cold Spring Harbor Laboratory 1994 Methods in yeast genetics : a Cold Spring Harbor Laboratory course manual Cold Spring Harbor, NY Cold Spring Harbor Laboratory Press vii, 234

67. VothWP

RichardsJD

ShawJM

StillmanDJ

2001 Yeast vectors for integration at the HO locus. Nucleic Acids Res 29 E59 59

68. BaylyJC

DouglasLM

PretoriusIS

BauerFF

DranginisAM

2005 Characteristics of Flo11-dependent flocculation in Saccharomyces cerevisiae. FEMS Yeast Res 5 1151 1156

69. KumarA

SnyderM

2001 Genome-wide transposon mutagenesis in yeast. Curr Protoc Mol Biol Chapter 13 Unit13 13

70. GietzRD

SchiestlRH

2007 High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat Protoc 2 31 34

71. ChunKT

EdenbergHJ

KelleyMR

GoeblMG

1997 Rapid amplification of uncharacterized transposon-tagged DNA sequences from genomic DNA. Yeast 13 233 240

72. HoreckaJ

JigamiY

2000 Identifying tagged transposon insertion sites in yeast by direct genomic sequencing. Yeast 16 967 970

73. WinzelerEA

ShoemakerDD

AstromoffA

LiangH

AndersonK

1999 Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285 901 906

74. BrachmannCB

DaviesA

CostGJ

CaputoE

LiJ

1998 Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14 115 132

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