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Title: Regulation of yeast-to-hyphae transition in Yarrowia lipolytica

Journal Article · · mSphere

© 2018 Pomraning et al. The yeast Yarrowia lipolytica undergoes a morphological transition from yeast-to-hyphal growth in response to environmental conditions. A forward genetic screen was used to identify mutants that reliably remain in the yeast phase, which were then assessed by whole-genome sequencing. All the smooth mutants identified, so named because of their colony morphology, exhibit independent loss of DNA at a repetitive locus made up of interspersed ribosomal DNA and short 10- to 40-mer telomere-like repeats. The loss of repetitive DNA is associated with downregulation of genes with stress response elements (5'-CCCCT-3') and upregulation of genes with cell cycle box (5'-ACGCG-3') motifs in their promoter region. The stress response element is bound by the transcription factor Msn2p in Saccharomyces cerevisiae. We confirmed that the Y. lipolytica msn2 (Ylmsn2) ortholog is required for hyphal growth and found that overexpression of Ylmsn2 enables hyphal growth in smooth strains. The cell cycle box is bound by the Mbp1p/Swi6p complex in S. cerevisiae to regulate G1-to-S phase progression. We found that overexpression of either the Ylmbp1 or Ylswi6 homologs decreased hyphal growth and that deletion of either Ylmbp1 or Ylswi6 promotes hyphal growth in smooth strains. A second forward genetic screen for reversion to hyphal growth was performed with the smooth-33 mutant to identify additional genetic factors regulating hyphal growth in Y. lipolytica. Thirteen of the mutants sequenced from this screen had coding mutations in five kinases, including the histidine kinases Ylchk1 and Ylnik1 and kinases of the high-osmolarity glycerol response (HOG) mitogen-activated protein (MAP) kinase cascade Ylssk2, Ylpbs2, and Ylhog1. Together, these results demonstrate that Y. lipolytica transitions to hyphal growth in response to stress through multiple signaling pathways.

Research Organization:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC)
DOE Contract Number:
AC02-05CH11231
OSTI ID:
1546627
Journal Information:
mSphere, Vol. 3, Issue 6
Country of Publication:
United States
Language:
English

References (96)

The cytoplasmic helical linker domain of receptor histidine kinase and methyl-accepting proteins is common to many prokaryotic signalling proteins journal July 1999
HOY1, a homeo gene required for hyphal formation in Yarrowia lipolytica. journal November 1997
The TEA/ATTS transcription factor YlTec1p represses the yeast-to-hypha transition in the dimorphic yeast Yarrowia lipolytica journal October 2012
Mutational analysis of the linker region of EnvZ, an osmosensor in Escherichia coli. journal July 1997
DREME: motif discovery in transcription factor ChIP-seq data journal May 2011
Candida albicans: A molecular revolution built on lessons from budding yeast journal December 2002
Origin of the Yeast Whole-Genome Duplication journal August 2015
Characterization of mutations in the two-component histidine kinase gene that confer fludioxonil resistance and osmotic sensitivity in theos-1 mutants ofNeurospora crassa journal January 2001
Variations in the number of ribosomal DNA units in morphological mutants and normal strains of Candida albicans and in normal strains of Saccharomyces cerevisiae. journal November 1993
Fast and accurate short read alignment with Burrows-Wheeler transform journal May 2009
Characterization of mutations in the two-component histidine kinase gene AbNIK1 from Alternaria brassicicola that confer high dicarboximide and phenylpyrrole resistance journal March 2005
Signaling through Adenylyl Cyclase Is Essential for Hyphal Growth and Virulence in the Pathogenic Fungus Candida albicans journal November 2001
Polarized Growth Controls Cell Shape and Bipolar Bud Site Selection in Saccharomyces cerevisiae journal July 2000
Subcellular localization of the histidine kinase receptors Sln1p, Nik1p and Chk1p in the yeast CTG clade species Candida guilliermondii journal April 2014
Identification of the Transcription Factor Znc1p, which Regulates the Yeast-to-Hypha Transition in the Dimorphic Yeast Yarrowia lipolytica journal June 2013
Environmental Sensing and Signal Transduction Pathways Regulating Morphopathogenic Determinants of Candida albicans journal June 2007
Yeast HOG1 MAP Kinase Cascade Is Regulated by a Multistep Phosphorelay Mechanism in the SLN1–YPD1–SSK1 “Two-Component” Osmosensor journal September 1996
Control of pseudohyphae formation in Saccharomyces cerevisiae journal January 2001
EMS and UV Mutagenesis in Yeast journal April 2008
Automatic Generation of Predictive Dynamic Models Reveals Nuclear Phosphorylation as the Key Msn2 Control Mechanism journal May 2013
DNA replication stress restricts ribosomal DNA copy number journal September 2017
The Saccharomyces cerevisiae zinc finger proteins Msn2p and Msn4p are required for transcriptional induction through the stress response element (STRE). journal May 1996
Roles of the three Ras proteins in the regulation of dimorphic transition in the yeast Yarrowia lipolytica journal December 2013
The Hog1 Mitogen-Activated Protein Kinase Is Essential in the Oxidative Stress Response and Chlamydospore Formation in Candida albicans journal April 2003
Lrg1p functions as a putative GTPase-activating protein in the Pkc1p-mediated cell integrity pathway in Saccharomyces cerevisiae journal November 2001
Yeast cell differentiation: Lessons from pathogenic and non-pathogenic yeasts journal September 2016
CNVnator: An approach to discover, genotype, and characterize typical and atypical CNVs from family and population genome sequencing journal February 2011
Heterogeneity in the ribosomal RNA genes of the yeast Yarrowia lipolytica; cloning and analysis of two size classes of repeats journal January 1985
A role for the transcription factors Mbp1 and Swi4 in progression from G1 to S phase journal September 1993
Full-length transcriptome assembly from RNA-Seq data without a reference genome journal May 2011
Cdc28 tyrosine phosphorylation and the morphogenesis checkpoint in budding yeast. journal November 1996
Cell-Cycle Control of Gene Expression in Budding and Fission Yeast journal December 2005
FunRich: An open access standalone functional enrichment and interaction network analysis tool journal June 2015
Segregation of heterogeneous rDNA segments during demagnification of a Neurospora crassa strain possessing a double nucleolar organizer journal September 1983
A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data journal September 2011
NIH Image to ImageJ: 25 years of image analysis journal June 2012
Proteomic analysis reveals metabolic changes during yeast to hypha transition inYarrowia lipolytica journal January 2007
Effect of benzoic acid on metabolic fluxes in yeasts: A continuous-culture study on the regulation of respiration and alcoholic fermentation journal July 1992
Isolation of the gene encoding adenylate cyclase in Saccharomyces cerevisiae. journal August 1985
Characterization of the DNA-Binding Domains from the Yeast Cell-Cycle Transcription Factors Mbp1 and Swi4 journal April 2000
InterPro in 2017—beyond protein family and domain annotations journal November 2016
The complex structure and dynamic evolution of human subtelomeres journal February 2002
Genome evolution in yeasts journal July 2004
High Functional Overlap Between MluI Cell-Cycle Box Binding Factor and Swi4/6 Cell-Cycle Box Binding Factor in the G1/S Transcriptional Program in Saccharomyces cerevisiae journal June 2005
Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration journal April 2012
Hyperphosphorylation of Msn2p and Msn4p in response to heat shock and the diauxic shift is inhibited by cAMP in Saccharomyces cerevisiae journal September 2000
Hybrid histidine kinases in pathogenic fungi: Fungal hybrid histidine kinases journal January 2015
Tay1 Protein, a Novel Telomere Binding Factor from Yarrowia lipolytica journal October 2010
CTD kinase I is required for the integrity of the rDNA tandem array journal August 2006
The TORC1-Sch9-Rim15 signaling pathway represses yeast-to-hypha transition in response to glycerol availability in the oleaginous yeast Yarrowia lipolytica : TORC1-Sch9 pathway represses dimorphic transition journal March 2017
HTSeq--a Python framework to work with high-throughput sequencing data journal September 2014
When the Stress of Your Environment Makes You Go HOG Wild journal November 2004
Yeast go the whole HOG for the hyperosmotic response journal August 2002
Isolation of CaSLN1 and CaNIK1, the genes for osmosensing histidine kinase homologues, from the pathogenic fungus Candida albicans journal February 1998
Fungal dimorphism: the switch from hyphae to yeast is a specialized morphogenetic adaptation allowing colonization of a host journal August 2015
MHY1 Encodes a C2H2-Type Zinc Finger Protein That Promotes Dimorphic Transition in the Yeast Yarrowia lipolytica journal May 1999
Regulation of phenotypic transitions in the fungal pathogen Candida albicans journal May 2012
Canu: scalable and accurate long-read assembly via adaptive k -mer weighting and repeat separation journal March 2017
BreakDancer: an algorithm for high-resolution mapping of genomic structural variation journal August 2009
Identification of a putative histidine kinase two-component phosphorelay gene (CaHK1) inCandida albicans journal May 1998
Fast gapped-read alignment with Bowtie 2 journal March 2012
Msn2p, a zinc finger DNA-binding protein, is the transcriptional activator of the multistress response in Saccharomyces cerevisiae. journal June 1996
Identification of dimorphism-involved genes of Yarrowia lipolytica by means of microarray analysis journal June 2012
Mutational analysis reveals functional similarity between NARX, a nitrate sensor in Escherichia coli K-12, and the methyl-accepting chemotaxis proteins. journal June 1992
RAM: A Conserved Signaling Network That Regulates Ace2p Transcriptional Activity and Polarized Morphogenesis journal September 2003
Quantifying similarity between motifs journal January 2007
Deletion of the HAMP domains from the histidine kinase CaNik1p of Candida albicans or treatment with fungicides activates the MAP kinase Hog1p in S. cerevisiae transformants journal January 2013
Physiology and genetics of the dimorphic fungus Yarrowia lipolytica journal April 1997
The Ras/cAMP/PKA signaling pathway and virulence in Candida albicans journal December 2009
Transduction of envelope stress in Escherichia coli by the Cpx two-component system. journal December 1997
voom: precision weights unlock linear model analysis tools for RNA-seq read counts journal January 2014
Synthetic Lethal Analysis Implicates Ste20p, a p21-activated Protein Kinase, in Polarisome Activation journal April 2003
Characterization of the NikA Histidine Kinase Implicated in the Phosphorelay Signal Transduction of Aspergillus nidulans , with Special Reference to Fungicide Responses journal March 2007
Stress-controlled transcription factors, stress-induced genes and stress tolerance in budding yeast journal October 2000
JASPAR 2016: a major expansion and update of the open-access database of transcription factor binding profiles journal November 2015
Regulation of Nitrogen Metabolism by GATA Zinc Finger Transcription Factors in Yarrowia lipolytica journal February 2017
Magnification of rRNA gene number in a Neurospora crassa strain with a partial deletion of the nucleolus organizer journal March 1986
Nuclear localization of the C2H2 zinc finger protein Msn2p is regulated by stress and protein kinase A activity journal February 1998
Microbial production of sabinene—a new terpene-based precursor of advanced biofuel journal January 2014
MycoCosm portal: gearing up for 1000 fungal genomes journal December 2013
A novel functional assay for fungal histidine kinases group III reveals the role of HAMP domains for fungicide sensitivity journal January 2012
Pindel: a pattern growth approach to detect break points of large deletions and medium sized insertions from paired-end short reads journal June 2009
Trimorphic stepping stones pave the way to fungal virulence journal January 2009
Roles of Three Histidine Kinase Genes in Hyphal Development and Virulence of the Pathogenic Fungus Candida albicans journal December 1999
A yeast protein similar to bacterial two-component regulators journal October 1993
A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w journal April 2012
Genetic Control of Extracellular Protease Synthesis in the Yeast Yarrowia lipolytica journal February 2002
The chromosome end in yeast: its mosaic nature and influence on recombinational dynamics. journal March 1994
Chitinase is required for cell separation during growth of Saccharomyces cerevisiae. journal October 1991
Persistence of adoptively transferred T cells with a kinetically engineered IL-2 receptor agonist journal January 2020
Two Sides of a Coin: a Zika Virus Mutation Selected in Pregnant Rhesus Macaques Promotes Fetal Infection in Mice but at a Cost of Reduced Fitness in Nonpregnant Macaques and Diminished Transmissibility by Vectors journal September 2020
OmicLoupe: facilitating biological discovery by interactive exploration of multiple omic datasets and statistical comparisons journal March 2021
Tay1 Protein, a Novel Telomere Binding Factor from Yarrowia lipolytica text January 2010
Genome-scale model reconstruction of the methylotrophic yeast Ogataea polymorpha text January 2021
Automatic Generation of Predictive Dynamic Models Reveals Nuclear Phosphorylation as the Key Msn2 Control Mechanism text January 2013
A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data text January 2012

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