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Cited by 206Fungal and yeast genetics researchBacterial Genetics and BiotechnologyAntifungal resistance and susceptibility

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Phylogenetic diversity of stress signalling pathways in fungi

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Nikolaou, Elissavet, Agrafioti, Ino, Stumpf, Michael, Quinn, Janet, Stansfield, Ian, Brown, Alistair JP·2009·BMC Evolutionary Biology
DOI 10.1186/1471-2148-9-44PMC PMC2666651
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Abstract

BACKGROUND: Microbes must sense environmental stresses, transduce these signals and mount protective responses to survive in hostile environments. In this study we have tested the hypothesis that fungal stress signalling pathways have evolved rapidly in a niche-specific fashion that is independent of phylogeny. To test this hypothesis we have compared the conservation of stress signalling molecules in diverse fungal species with their stress resistance. These fungi, which include ascomycetes, basidiomycetes and microsporidia, occupy highly divergent niches from saline environments to plant or mammalian hosts. RESULTS: The fungi displayed significant variation in their resistance to osmotic (NaCl and sorbitol), oxidative (H2O2 and menadione) and cell wall stresses (Calcofluor White and Congo Red). There was no strict correlation between fungal phylogeny and stress resistance. Rather, the human pathogens tended to be more resistant to all three types of stress, an exception being the sensitivity of Candida albicans to the cell wall stress, Calcofluor White. In contrast, the plant pathogens were relatively sensitive to oxidative stress. The degree of conservation of osmotic, oxidative and cell wall stress signalling pathways amongst the eighteen fungal species was examined. Putative orthologues of functionally defined signalling components in Saccharomyces cerevisiae were identified by performing reciprocal BLASTP searches, and the percent amino acid identities of these orthologues recorded. This revealed that in general, central components of the osmotic, oxidative and cell wall stress signalling pathways are relatively well conserved, whereas the sensors lying upstream and transcriptional regulators lying downstream of these modules have diverged significantly. There was no obvious correlation between the degree of conservation of stress signalling pathways and the resistance of a particular fungus to the corresponding stress. CONCLUSION: Our data are consistent with the hypothesis that fungal stress signalling components have undergone rapid recent evolution to tune the stress responses in a niche-specific fashion.

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Crossref · 10.1186/1471-2148-9-44

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Figures

Figure 1 Neighbour-joining phylogeny constructed using a concatenated alignment of 8 genes for each of the 18 fungal species. Bootstrap scores for all the nodes are displayed. Encephalitozoon cuniculi was selected as an outgroup. The basidiomycetes and ascomycetes form distinct clades. Dotted lines indicate yeast-like fungi, thick straight lines indicate filamentous fungi, whereas dashed lines indicate dimorphic fungi [information adapted [144]]: red, human pathogens; green, plant pathogens; blue, benign fungi. Scale bar corresponds to 0.05 amino acid changes/site.
Figure 1 Neighbour-joining phylogeny constructed using a concatenated alignment of 8 genes for each of the 18 fungal species. Bootstrap scores for all the nodes are displayed. Encephalitozoon cuniculi was selected as an outgroup. The basidiomycetes and ascomycetes form distinct clades. Dotted lines indicate yeast-like fungi, thick straight lines indicate filamentous fungi, whereas dashed lines indicate dimorphic fungi [information adapted [144]]: red, human pathogens; green, plant pathogens; blue, benign fungi. Scale bar corresponds to 0.05 amino acid changes/site.CC BY · PubMed Central
Figure 2 Comparison of fungal NaCl sensitivities. Growth of fungi on media containing various NaCl concentrations, the control plates lacking NaCl. Serial dilutions were plated as described in Materials and Methods.
Figure 2 Comparison of fungal NaCl sensitivities. Growth of fungi on media containing various NaCl concentrations, the control plates lacking NaCl. Serial dilutions were plated as described in Materials and Methods.CC BY · PubMed Central
Figure 3 Degree of conservation of fungal osmotic stress regulators. (A) Orthologues of S. cerevisiae osmotic stress regulators in the fungi analysed. The organisms are ordered according to their position in the phylogeny, and the regulators ordered according to their mean %ID across all of the fungal species examined. Closed indicates no orthologue identified. (B) Mean conservation (%ID) of osmotic stress regulators across the fungal species examined based on the model of the osmotic stress pathway in S. cerevisiae described by Krantz and co-workers (2006) [18].
Figure 3 Degree of conservation of fungal osmotic stress regulators. (A) Orthologues of S. cerevisiae osmotic stress regulators in the fungi analysed. The organisms are ordered according to their position in the phylogeny, and the regulators ordered according to their mean %ID across all of the fungal species examined. Closed indicates no orthologue identified. (B) Mean conservation (%ID) of osmotic stress regulators across the fungal species examined based on the model of the osmotic stress pathway in S. cerevisiae described by Krantz and co-workers (2006) [18].CC BY · PubMed Central
Figure 4 Degree of conservation of fungal oxidative stress regulators. (A) Orthologues of S. cerevisiae oxidative stress regulators in the fungi analysed. As before, the fungi are ordered according to their position in the phylogeny, and the regulators ordered according to their mean %ID. Closed indicates no orthologue identified. (B) Mean conservation (%ID) of oxidative stress regulators across the fungal species examined based on the S. cerevisiae oxidative stress pathway adapted from reviews by Moye-Rowley (2003) [19] and Ikner and Shiozaki (2005) [20].
Figure 4 Degree of conservation of fungal oxidative stress regulators. (A) Orthologues of S. cerevisiae oxidative stress regulators in the fungi analysed. As before, the fungi are ordered according to their position in the phylogeny, and the regulators ordered according to their mean %ID. Closed indicates no orthologue identified. (B) Mean conservation (%ID) of oxidative stress regulators across the fungal species examined based on the S. cerevisiae oxidative stress pathway adapted from reviews by Moye-Rowley (2003) [19] and Ikner and Shiozaki (2005) [20].CC BY · PubMed Central
Figure 5 Degree of conservation of fungal cell wall stress regulators. (A) Orthologues of S. cerevisiae cell wall stress regulators in the fungi analysed. As before, the fungi are ordered according to their position in the phylogeny, and the regulators ordered according to their mean %ID. Closed indicates no orthologue identified. (B) Mean conservation (%ID) of cell wall stress regulators across the fungal species examined based on the S. cerevisiae cell wall stress pathway adapted from Levin (2005) [25].
Figure 5 Degree of conservation of fungal cell wall stress regulators. (A) Orthologues of S. cerevisiae cell wall stress regulators in the fungi analysed. As before, the fungi are ordered according to their position in the phylogeny, and the regulators ordered according to their mean %ID. Closed indicates no orthologue identified. (B) Mean conservation (%ID) of cell wall stress regulators across the fungal species examined based on the S. cerevisiae cell wall stress pathway adapted from Levin (2005) [25].CC BY · PubMed Central

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Research works printed but not linked: 5

  1. Selitrennikoff CP: Calcofluor white inhibits Neurospora chitin synthetase activity [bleaching agent for fabrics]. Plant Physiol Bioch. 1984, 8 (3): 269-272.
  2. Fleet GH: Cell walls. The Yeasts. Edited by: Rose AH, Harrison JS. 1991, New York: Academic Press, 199-277.
  3. Vogel HJ: Vogel, A convenient medium for Neurospora (medium N). Microb Genet Bull. 1956, 13: 42-43.
  4. Selitrennikoff C, Sachs MS: Lipofectin increases transformation of Neurospora crassa. Fungal Genet Newsl. 1991, 38: 90-91.
  5. Perkins DD: How to convert wild-type spreading growth to colonial. 2006, [http://www.fgsc.net/Neurospora/NeurosporaProtocolGuide.htm]

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Metadata

Authors
Nikolaou, E., Agrafioti, I., Stumpf, M., Quinn, J., Stansfield, I., & Brown, A. J.
Affiliations
  • University of Aberdeen (GB)
  • Imperial College London (GB)
  • Newcastle University (GB)
Corresponding author
Brown, Alistair JP
ORCID
Venue
BMC Evolutionary Biology
Publisher
Springer Science and Business Media LLC
Published
2009-02-21
Volume
9
Issue
1
Pages
44-44
ISSN
1471-2148 (ISSN-L)
DOI
10.1186/1471-2148-9-44
PMC
PMC2666651
OpenAlex
W1985831723
Cited by
206
References
159
Citations by year
2026: 12 · 2025: 13 · 2024: 7 · 2023: 9 · 2022: 9 · 2021: 7 · 2020: 14 · 2019: 13 · 2018: 8 · 2017: 13 · 2016: 15 · 2015: 17 · 2014: 18 · 2013: 16 · 2012: 13
FWCI
4.69
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • BMC Evolutionary Biology (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Aberdeen University Research Archive (Aberdeen University) (submittedVersion)
  • Minerva Access (University of Melbourne) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Newcastle University ePrints (Newcastle Univesity)
Funders
  • Wellcome Trust (080088)
  • University of Exeter
  • Imperial College London
  • University of Aberdeen
  • Biotechnology and Biological Sciences Research Council (BB/D009308/1, BB/C510391/1, BB/F00513X/1, BB/F013566/1)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
  • Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
Keywords
stress tolerance, osmotic stress, oxidative stress, cell wall stress, phylogenetic conservation, orthologs, human fungal pathogens, plant pathogenic fungi, Candida albicans, Ascomycota, Basidiomycota, microsporidia, signal transduction
MeSH terms
Benzenesulfonates, Candida albicans, Cell Wall, Congo Red, DNA, Fungal, Fungal Proteins, Hydrogen Peroxide, Osmotic Pressure, Phylogeny, Saccharomyces cerevisiae, Sodium Chloride, Sorbitol, Signal Transduction, Gene Expression Regulation, Fungal, Genome, Fungal, Oxidative Stress, Evolution, Molecular, Vitamin K 3

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