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Title: Regulation of Yeast-to-Hyphae Transition in Yarrowia lipolytica

Abstract

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 wasmore » 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. IMPORTANCE Many yeasts undergo a morphological transition from yeast-to-hyphal growth in response to environmental conditions. We used forward and reverse genetic techniques to identify genes regulating this transition in Yarrowia lipolytica. We confirmed that the transcription factor Ylmsn2 is required for the transition to hyphal growth and found that signaling by the histidine kinases Ylchk1 and Ylnik1 as well as the MAP kinases of the HOG pathway (Ylssk2, Ylpbs2, and Ylhog1) regulates the transition to hyphal growth. These results suggest that Y. lipolytica transitions to hyphal growth in response to stress through multiple kinase pathways. Intriguingly, we found that a repetitive portion of the genome containing telomere-like and rDNA repeats may be involved in the transition to hyphal growth, suggesting a link between this region and the general stress response.« less

Authors:
 [1];  [2];  [3];  [4];  [4];  [4];  [4];  [4];  [4];  [5];  [6];  [4]; ORCiD logo [7]; ORCiD logo [8];
+ Show Author Affiliations
  1. Chemical &, Biological Process Development Group, Pacific Northwest National Laboratory, Richland, Washington, USA
  2. Environmental Molecular Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USA
  3. Department of Biology and Biological Engineering, Chalmers University of Technology, Göteborg, Sweden
  4. DOE Joint Genome Institute, Walnut Creek, California, USA
  5. Chemical &, Biological Process Development Group, Pacific Northwest National Laboratory, Richland, Washington, USA, Joint BioEnergy Institute, Lawrence Berkeley National Laboratory, Berkeley, California, USA
  6. Joint BioEnergy Institute, Lawrence Berkeley National Laboratory, Berkeley, California, USA
  7. Department of Biology and Biological Engineering, Chalmers University of Technology, Göteborg, Sweden, Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, Lyngby, Denmark
  8. Environmental Molecular Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USA, Joint BioEnergy Institute, Lawrence Berkeley National Laboratory, Berkeley, California, USA
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1484405
Alternate Identifier(s):
OSTI ID: 1496567; OSTI ID: 1546633
Report Number(s):
PNNL-SA-131456
Journal ID: ISSN 2379-5042; e00541-18
Grant/Contract Number:  
AC05-76RL01830; AC02-05CH11231
Resource Type:
Published Article
Journal Name:
mSphere
Additional Journal Information:
Journal Name: mSphere Journal Volume: 3 Journal Issue: 6; Journal ID: ISSN 2379-5042
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Yarrowia lipolytica, smooth, yeast, hyphae, kinase, msn2, chk1, nik1, ssk2, pbs2, dimorphic, genomics, molecular genetics, morphology, signaling

Citation Formats

Pomraning, Kyle R., Bredeweg, Erin L., Kerkhoven, Eduard J., Barry, Kerrie, Haridas, Sajeet, Hundley, Hope, LaButti, Kurt, Lipzen, Anna, Yan, Mi, Magnuson, Jon K., Simmons, Blake A., Grigoriev, Igor V., Nielsen, Jens, Baker, Scott E., and Mitchell, ed., Aaron P. Regulation of Yeast-to-Hyphae Transition in Yarrowia lipolytica. United States: N. p., 2018. Web. doi:10.1128/mSphere.00541-18.
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Pomraning, Kyle R., Bredeweg, Erin L., Kerkhoven, Eduard J., Barry, Kerrie, Haridas, Sajeet, Hundley, Hope, LaButti, Kurt, Lipzen, Anna, Yan, Mi, Magnuson, Jon K., Simmons, Blake A., Grigoriev, Igor V., Nielsen, Jens, Baker, Scott E., & Mitchell, ed., Aaron P. Regulation of Yeast-to-Hyphae Transition in Yarrowia lipolytica. United States. https://doi.org/10.1128/mSphere.00541-18
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Pomraning, Kyle R., Bredeweg, Erin L., Kerkhoven, Eduard J., Barry, Kerrie, Haridas, Sajeet, Hundley, Hope, LaButti, Kurt, Lipzen, Anna, Yan, Mi, Magnuson, Jon K., Simmons, Blake A., Grigoriev, Igor V., Nielsen, Jens, Baker, Scott E., and Mitchell, ed., Aaron P. Wed . "Regulation of Yeast-to-Hyphae Transition in Yarrowia lipolytica". United States. https://doi.org/10.1128/mSphere.00541-18.
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@article{osti_1484405,
title = {Regulation of Yeast-to-Hyphae Transition in Yarrowia lipolytica},
author = {Pomraning, Kyle R. and Bredeweg, Erin L. and Kerkhoven, Eduard J. and Barry, Kerrie and Haridas, Sajeet and Hundley, Hope and LaButti, Kurt and Lipzen, Anna and Yan, Mi and Magnuson, Jon K. and Simmons, Blake A. and Grigoriev, Igor V. and Nielsen, Jens and Baker, Scott E. and Mitchell, ed., Aaron P.},
abstractNote = {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. IMPORTANCE Many yeasts undergo a morphological transition from yeast-to-hyphal growth in response to environmental conditions. We used forward and reverse genetic techniques to identify genes regulating this transition in Yarrowia lipolytica. We confirmed that the transcription factor Ylmsn2 is required for the transition to hyphal growth and found that signaling by the histidine kinases Ylchk1 and Ylnik1 as well as the MAP kinases of the HOG pathway (Ylssk2, Ylpbs2, and Ylhog1) regulates the transition to hyphal growth. These results suggest that Y. lipolytica transitions to hyphal growth in response to stress through multiple kinase pathways. Intriguingly, we found that a repetitive portion of the genome containing telomere-like and rDNA repeats may be involved in the transition to hyphal growth, suggesting a link between this region and the general stress response.},
doi = {10.1128/mSphere.00541-18},
journal = {mSphere},
number = 6,
volume = 3,
place = {United States},
year = {Wed Dec 26 00:00:00 EST 2018},
month = {Wed Dec 26 00:00:00 EST 2018}
}
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https://doi.org/10.1128/mSphere.00541-18
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Figures / Tables:

FIG 1 FIG 1: Isolation of Y. lipolytica mutants that lack filamentous growth. Approximately 500,000 colonies were screened for smooth morphology with no visible hyphae. From strain FKP355, five mutant strains were isolated that exhibit growth only as yeast (FKP500 to FKP504). The leu2-270 mutation was complemented in strain FKP503 to constructmore » FKP514 and confirm the phenotype in a prototrophic strain. Confocal microscopy confirmed yeast phase growth and lack of elongated cells or pseudohyphae in auxotrophic and prototrophic smooth strains.« less
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