Cited by 266Fungal and yeast genetics researchAntifungal resistance and susceptibilityBacterial Genetics and Biotechnology

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Our Paths Might Cross: the Role of the Fungal Cell Wall Integrity Pathway in Stress Response and Cross Talk with Other Stress Response Pathways

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Fuchs, Beth Burgwyn, Mylonakis, Eleftherios·2009·Eukaryotic Cell

DOI 10.1128/ec.00193-09PMC PMC2772411

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Abstract

Fungi occupy diverse environments and are subjected to many extreme conditions. Among the stressful conditions faced by fungi are pH changes, osmotic changes, thermal changes, oxide radicals, nutrient deprivation, and exposure to chemicals. These adversities can be found either in the environment or in animal and human hosts. The cell wall integrity (CWI) pathway provides a means to fortify and repair damages to the cell wall in order to withstand stressful environments. The CWI pathway in comprised of cell wall stress sensors that lead to activation of a mitogen-activated protein kinase (MAPK) cascade. Signaling through the MAPK cascade leads to expression of transcription factors that facilitate biosynthesis of cell wall components and actin organization. Given the relatively limited number of components of the CWI pathway and the very diverse stimuli, there must be a means of expanding the pathway. To manage the diverse stress conditions, the CWI pathway cross talks with other pathways or proteins, and these cross talk events enhance the signaling capabilities of the CWI pathway. Lateral influences that facilitate maintaining the cell wall under stress conditions are TOR signaling, calcineurin signaling, the high-osmolarity glycerol pathway, the cyclic AMP-protein kinase A pathway, and additional proteins. In this article, we highlight several of the cross talk events that have been described for Saccharomyces cerevisiae and several other fungi.

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The Heat Shock Transcription Factor HsfA Is Essential for Thermotolerance and Regulates Cell Wall Integrity in Aspergillus fumigatus
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Growth study under combined effects of temperature, pH and salinity and transcriptome analysis revealed adaptations of Aspergillus terreus NTOU4989 to the extreme conditions at Kueishan Island Hydrothermal Vent Field, Taiwan
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Involvement of the Cell Wall–Integrity Pathway in Signal Recognition, Cell-Wall Biosynthesis, and Virulence in Magnaporthe oryzae
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A Myb Transcription Factor of Phytophthora sojae, Regulated by MAP Kinase PsSAK1, Is Required for Zoospore Development
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Updating Insights into the Regulatory Mechanisms of Calcineurin-Activated Transcription Factor Crz1 in Pathogenic Fungi
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Protein Kinase A and High-Osmolarity Glycerol Response Pathways Cooperatively Control Cell Wall Carbohydrate Mobilization in Aspergillus fumigatus
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“Often, substantial cross talk exists between these signaling pathways, governed by either direct or indirect interactions between pathway-speciﬁc proteins (37, 47, 48).”
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“It should be noted 480 that the response to environmental stresses, including elevated temperatures, are coordinated 481 through cross-talk between multiple signaling pathways including the TOR, calcineurin, MAPK and 482 cAMP-protein kinase A pathways (Fuchs and Mylonakis 2009).”
BackgroundInfluential
FvBck1, a component of cell wall integrity MAP kinase pathway, is required for virulence and oxidative stress response in sugarcane Pokkah Boeng pathogen
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SCWISh network is essential for survival under mechanical pressure
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“fumigatus might also be activated as a part of the general response to in vivo stress, so it might lead to survival in the host (13).”
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Comparative transcriptome and gene co-expression network analysis reveal genes and signaling pathways adaptively responsive to varied adverse stresses in the insect fungal pathogen, Beauveria bassiana
He, Z., Zhao, X., Lu, Z., Wang, H., Liu, P., Zeng, F., & Zhang, Y. (2017) · Journal of Invertebrate Pathology · doi:10.1016/j.jip.2017.12.002 · Cited by 30
“Slt2 MAP kinase pathway mediates cell wall integrity, heat shock, low osmotic stress response and fungal virulence (Fuchs and Mylonakis, 2009; Luo et al., 2012; Valiante et al., 2009).”
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Impact of the Environment upon the Candida albicans Cell Wall and Resultant Effects upon Immune Surveillance
Childers, D. S., Avelar, G. M., Bain, J. M., Larcombe, D. E., Pradhan, A., Budge, S., Heaney, H., & Brown, A. J. P. (2019) · Current topics in microbiology and immunology · doi:10.1007/82_2019_182 · Cited by 31
Proof-of-principle for SERS imaging of Aspergillus nidulans hyphae using in vivo synthesis of gold nanoparticles
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Osmoregulation in Saccharomyces cerevisiae via mechanisms other than the high-osmolarity glycerol pathway
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“…forming a complex with Fpr1p, which is subsequently complexed to Tor1p, a serine/threonine (Ser/Thr) kinase, eventually inhibiting TOR signalling (Fuchs & Mylonakis, 2009). http://mic.microbiologyresearch.org 1517 Downloaded from www.microbiologyresearch.org by IP: 54.70.40.11 On: Sat, 08 Dec…”
BackgroundInfluential
Understanding the effect of postharvest tomato temperatures on two toxigenic Alternaria spp. strains: growth, mycotoxins and cell‐wall integrity‐related gene expression
Cabral, L. D. C., Rodríguez, A., Delgado, J., & Patriarca, A. (2019) · Journal of the Science of Food and Agriculture · doi:10.1002/jsfa.9950 · Cited by 32
A high-throughput RNA-Seq approach to elucidate the transcriptional response of Piriformospora indica to high salt stress
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The Coupling Between Cell Wall Integrity Mediated by MAPK Kinases and SsFkh1 Is Involved in Sclerotia Formation and Pathogenicity of Sclerotinia sclerotiorum
Cong, J., Xiao, K., Jiao, W., Zhang, C., Zhang, X., Liu, J., Zhang, Y., & Pan, H. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.816091 · Cited by 28
“The CWI pathway is important for the highly controlled and polarized restructuring of the fungal cell walls during development, morphological changes, and the environmental challenges (Fuchs and Mylonakis, 2009).”
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Global Proteomic Profiling of the Secretome of Candida albicans ecm33 Cell Wall Mutant Reveals the Involvement of Ecm33 in Sap2 Secretion
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Phosphorylation by the stress-activated MAPK Slt2 down-regulates the yeast TOR complex 2Preprint
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“Significant cross-talk exists between the HOG and CWI pathways (Hahn and Thiele 2002; García-Rodríguez et al. 2005; Fuchs and Mylonakis 2009; García et al. 2009) and between these MAPK pathways and TORC2 function.”
Regulation of Neurospora crassa cell wall remodeling via the cot-1 pathway is mediated by gul-1
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Physiological responses of Saccharomyces cerevisiae to industrially relevant conditions: Slow growth, low pH, and high CO2 levels
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HgrA is necessary and sufficient to drive hyphal growth in the dimorphic pathogen P enicillium marneffei
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“…including oxidative and osmotic stress, and those regulating the integrity of the cell wall and the activation of development and morphogenesis (Aguirre et al., 2005; Roman et al., 2005; Fuchs and Mylonakis, 2009; Duran et al., 2010; Etxebeste et al., 2010; Nahlik et al., 2010; Jain et al., 2011).”
Background
Mtl1 O-mannosylation mediated by both Pmt1 and Pmt2 is important for cell survival under oxidative conditions and TOR blockade
Petkova, M. I., Pujol‐Carrion, N., & de la Torre-Ruiz, M. Á. (2012) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2012.08.005 · Cited by 25
A Cdc42 homolog in Colletotrichum gloeosporioides regulates morphological development and is required for ROS-mediated plant infection
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Differential response to synthetic and natural antifungals by Alternaria tenuissima in wheat simulating media: Growth, mycotoxin production and expression of a gene related to cell wall integrity
Cabral, L. D. C., Delgado, J., Patriarca, A., & Rodríguez, A. (2018) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2018.12.005 · Cited by 25
The DUF1996 and WSC domain‐containing protein Wsc1I acts as a novel sensor of multiple stress cues in Beauveria bassiana
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“…cellular stress responses via a cross‐talk with the high‐osmolarity glycerol (HOG) pathway governed by three‐ module MAPK Hog1 cascade in the yeast (Fuchs & Mylonakis, 2009; García, Rodríguez‐Peña, Bermejo, Nombela, & Arroyo, 2009; wileyonlinelibrary.com/j Rodríguez‐Peña, García, Nombela, &…”
Background
Tracking nickel‐adaptive biomarkers in Pisolithus albus from New Caledonia using a transcriptomic approach
Majorel, C., Hannibal, L., Soupé-Gilbert, M.-E., Carriconde, F., Ducousso, M., Lebrun, M., & Jourand, P. (2012) · Molecular Ecology · doi:10.1111/j.1365-294x.2012.05527.x · Cited by 24
“In this way, such modifications could confer tolerance to metals and affect the ability of fungi to survive in stressful environments (Meharg 2003; Bellion et al. 2006; Fuchs & Mylonakis 2009).”
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Evaluation of Saccharomyces cerevisiae GAS1 with respect to its involvement in tolerance to low pH and salt stress
Matsushika, A., Suzuki, T., Goshima, T., & Hoshino, T. (2017) · Journal of Bioscience and Bioengineering · doi:10.1016/j.jbiosc.2017.03.004 · Cited by 24
The stuA gene controls development, adaptation, stress tolerance, and virulence of the dermatophyte Trichophyton rubrum
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cpsA regulates mycotoxin production, morphogenesis and cell wall biosynthesis in the fungus Aspergillus nidulans
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“For example, the fungal cell wall is the first line of defense for protection against exogenous oxidative stress (Fuchs and Mylonakis, 2009).”
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Application of recyclable CRISPR/Cas9 tools for targeted genome editing in the postharvest pathogenic fungi Penicillium digitatum and Penicillium expansum
Garrigues, S., Manzanares, P., & Marcos, J. F. (2022) · Current Genetics · doi:10.1007/s00294-022-01236-0 · Cited by 25
“Asterisks (*) show significant differences between the mutant and the control strains (Student’s t-test, p 0.05) 1 3 defense to withstand stressing agents and harsh environmental conditions (Fuchs and Mylonakis 2009).”
BackgroundInfluential
Actin - a biosensor that determines cell fate in yeasts
Smethurst, D. G. J., Dawes, I. W., & Gourlay, C. W. (2013) · FEMS Yeast Research · doi:10.1111/1567-1364.12119 · Cited by 23
Low temperature highlights the functional role of the cell wall integrity pathway in the regulation of growth in Saccharomyces cerevisiae
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Cbk1 kinase and Bck2 control MAP kinase activation and inactivation during heat shock
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“…pathways, the Cell Wall Integrity (CWI) and the Regulation of Ace2 and Morphogenesis (RAM) signaling networks, provide insight into the mechanisms that coordinate cell growth control and stress signaling (Nelson et al., 2003; Levin, 2005; Chen and Thorner, 2007; Fuchs and Mylonakis, 2009).”
BackgroundInfluential

Authors: Fuchs, B. B., & Mylonakis, E.
Affiliations: Harvard University (US)
ORCID: Fuchs, Beth Burgwyn
Mylonakis, Eleftherios
Venue: Eukaryotic Cell
Publisher: American Society for Microbiology
Published: 2009-11
Volume: 8
Issue: 11
Pages: 1616-1625
ISSN: 1535-9778 (ISSN-L)
1535-9786
DOI: 10.1128/ec.00193-09
PMC: PMC2772411
OpenAlex: W2136493024
Cited by: 266
References: 87
Citations by year: 2026: 17 · 2025: 14 · 2024: 12 · 2023: 9 · 2022: 21 · 2021: 17 · 2020: 22 · 2019: 12 · 2018: 22 · 2017: 16 · 2016: 17 · 2015: 20 · 2014: 17 · 2013: 12 · 2012: 14
FWCI: 0.97
Type: journal article
Language: en
Open access: diamond
doi.org
Licence: journals.asm.org/non-commercial-tdm-license (tdm)
Locations: Eukaryotic Cell (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health
National Institute of Allergy and Infectious Diseases (R21AI079569, R01AI075286)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Keywords: stress response, MAPK signaling, pathway crosstalk, TOR signaling, calcineurin signaling, high-osmolarity glycerol pathway, cAMP/protein kinase A pathway, transcription factors, actin organization, cell wall biosynthesis, Saccharomyces cerevisiae, pH stress, osmotic stress, oxidative stress, nutrient deprivation
MeSH terms: Cell Wall, Fungal Proteins, Fungi, Saccharomyces cerevisiae, Stress, Physiological, Signal Transduction, Receptor Cross-Talk

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Our Paths Might Cross: the Role of the Fungal Cell Wall Integrity Pathway in Stress Response and Cross Talk with Other Stress Response Pathways

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