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
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2010 Číslo 1
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- A Major Role of the RecFOR Pathway in DNA Double-Strand-Break Repair through ESDSA in
- Kidney Development in the Absence of and Requires
- The Werner Syndrome Protein Functions Upstream of ATR and ATM in Response to DNA Replication Inhibition and Double-Strand DNA Breaks
- Alternative Epigenetic Chromatin States of Polycomb Target Genes