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PreprintCited by 3Fungal and yeast genetics researchPlant-Microbe Interactions and ImmunityPlant Pathogens and Fungal Diseases

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Enhanced Oxidative Stress Resistance in Ustilago maydis and Its Implications on the Virulence

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Cuamatzi-Flores, Jorge, Colón-González, Maritrini, Requena-Romo, Fernanda, Quiñones-Galeana, Samuel, Cervantes-Chávez, José Antonio, Morales, Lucía·2023·International Microbiology
DOI 10.21203/rs.3.rs-3517082/v1PMC PMC11452521

Preprint — published as 10.1007/s10123-024-00489-8 · Paper page

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Abstract

The phytopathogenic fungus Ustilago maydis causes corn smut by suppressing host plant defenses, including the oxidative burst response. While many studies have investigated how U. maydis responds to oxidative stress during infection, the consequences of heightened resistance to oxidative stress on virulence remain understudied. This study aimed to identify the effects on virulence in U. maydis strains exhibiting enhanced resistance to hydrogen peroxide (H 2 O 2). To achieve this, we exposed U. maydis SG200 to 20 escalating H 2 O 2 shocks, resulting in an adapted strain resistant to concentrations as high as 60 mM of H 2 O 2, a lethal dose for the initial strain. Genetic analysis of the adapted strain revealed five nucleotide substitutions, two minor copy number variants, and a large amplification event on chromosome nine (1-149 kb) encompassing the sole catalase gene. Overexpressing catalase increased resistance to H 2 O 2; however, this resistance was lower than that observed in the adapted strain. Additionally, virulence was reduced in both strains with enhanced H 2 O 2-resistance. In summary, enhanced H 2 O 2 resistance, achieved through either continuous exposure to the oxidative agent or through catalase overexpression, decreased virulence. This suggests that the response to the oxidative stress burst in U. maydis is optimal and that increasing the resistance to H 2 O 2 does not translate into increased virulence. These findings illuminate the intricate relationship between oxidative stress resistance and virulence in U. maydis, offering insights into its infection mechanisms.

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Fig. 1 Hydrogen Peroxide Resistance in Ustilago maydis. A Percentage of cells surviving H2O2 shocks at 5 and 60 mM in the initial strain U. maydis SG200 and the adapted strain (UmH2O2-R). B Inhibition zone areas produced by H2O2 of the initial strain and of UmH2O2-R immediately after isolation, and after 7 days of culture with daily dilutions in the absence of H2O2 (UmH2O2-R + 7 days)
Fig. 1 Hydrogen Peroxide Resistance in Ustilago maydis. A Percentage of cells surviving H2O2 shocks at 5 and 60 mM in the initial strain U. maydis SG200 and the adapted strain (UmH2O2-R). B Inhibition zone areas produced by H2O2 of the initial strain and of UmH2O2-R immediately after isolation, and after 7 days of culture with daily dilutions in the absence of H2O2 (UmH2O2-R + 7 days)CC BY · PubMed Central
Fig. 2 Changes in catalase gene expression. Fold change gene expression of UMAG_11067 (catalase encoding gene) following an exposure at 10 mM of H2O2
Fig. 2 Changes in catalase gene expression. Fold change gene expression of UMAG_11067 (catalase encoding gene) following an exposure at 10 mM of H2O2CC BY · PubMed Central
Fig. 3 Hydrogen peroxide resistance and virulence profiles of oexUMAG_11067 and UmH2O2-R. A Percentage of viable cells determined through CFU counts after exposure to 10 mM H2O2 shock. B Virulence assessment on maize seedlings analyzed at 12 days post infection. Color coding represents the severity of infection
Fig. 3 Hydrogen peroxide resistance and virulence profiles of oexUMAG_11067 and UmH2O2-R. A Percentage of viable cells determined through CFU counts after exposure to 10 mM H2O2 shock. B Virulence assessment on maize seedlings analyzed at 12 days post infection. Color coding represents the severity of infectionCC BY · PubMed Central

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Metadata

Authors
Cuamatzi-Flores, J., Colón-González, M., Requena-Romo, F., Quiñones-Galeana, S., Cervantes-Chávez, J. A., & Morales, L.
Affiliations
  • Autonomous University of Queretaro (MX)
  • Universidad Nacional Autónoma de México
  • Universidad Nacional Autónoma de México (MX)
  • Universidad Autónoma de Querétaro
Corresponding author
  • Cuamatzi-Flores, Jorge
  • Morales, Lucía
ORCID
Venue
International Microbiology
Publisher
Research Square Platform LLC
Published
2023-11-07
Volume
27
Issue
5
Pages
1501-1511
ISSN
1139-6709 (ISSN-L)
DOI
10.21203/rs.3.rs-3517082/v1
PMC
PMC11452521
OpenAlex
W4392135996
Cited by
3
References
1
Citations by year
2026: 2 · 2025: 1
FWCI
0.41
Type
journal article
Language
en
Open access
Licence
Locations
  • International Microbiology (publishedVersion, cc-by)
  • Research Square (acceptedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
  • Universidad Autónoma de Querétaro
  • Deutscher Akademischer Austauschdienst
  • Consejo Nacional de Ciencia y Tecnología (CF-103000)
  • Consejo de Ciencia y Tecnología del Estado de Querétaro (NT/21/2022)
  • Directorate for Biological Sciences
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant-Microbe Interactions and Immunity
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Pathogens and Fungal Diseases
Keywords
Ustilago maydis, corn smut, oxidative stress resistance, hydrogen peroxide resistance, fungal virulence, catalase overexpression, respiratory burst, host defense suppression, copy number variation, adaptive evolution
MeSH terms
Basidiomycota, Catalase, Zea mays, Fungal Proteins, Hydrogen Peroxide, Plant Diseases, Ustilago, Virulence, Oxidative Stress

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Cuamatzi-Flores, J., Colón-González, M., Requena-Romo, F., Quiñones-Galeana, S., Cervantes-Chávez, J. A., & Morales, L. (2023). Enhanced Oxidative Stress Resistance in Ustilago maydis and Its Implications on the Virulence. International Microbiology. https://doi.org/10.21203/rs.3.rs-3517082/v1

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