Tolerance to oxidative stress is associated with both oxidative stress response and inherent growth in a fungal wheat pathogen

Abstract

Reactive oxygen species are toxic byproducts of aerobic respiration that are also important in mediating a diversity of cellular functions. Reactive oxygen species form an important component of plant defenses to inhibit microbial pathogens during pathogen–plant interactions. Tolerance to oxidative stress is likely to make a significant contribution to the viability and pathogenicity of plant pathogens, but the complex network of oxidative stress responses hinders identification of the genes contributing to this trait. Here, we employed a forward genetic approach to investigate the genetic architecture of oxidative stress tolerance in the fungal wheat pathogen Zymoseptoria tritici. We used quantitative trait locus (QTL) mapping of growth and melanization under axenic conditions in two cross-populations to identify genomic regions associated with tolerance to oxidative stress. We found that QTLs associated with growth under oxidative stress as well as inherent growth can affect oxidative stress tolerance, and we identified two uncharacterized genes in a major QTL associated with this trait. Our data suggest that melanization does not affect tolerance to oxidative stress, which differs from what was found for animal pathogens. This study provides a whole-genome perspective on the genetic basis of oxidative stress tolerance in a plant pathogen.

Influence of H2O2-Induced Oxidative Stress on In Vitro Growth and Moniliformin and Fumonisins Accumulation by Fusarium proliferatum and Fusarium subglutinans

“…The data presented in this paper indicate that the investigated isolates were able to grow at higher temperatures, compared to those where they were isolated (June-August, 28.5 • ). Concerning F. proliferatum, the radial growth of the isolate PRO1 up to 30 • C was lower, when compared to PRO2 and PRO3, but PRO1 showed the best values at 35 • C. Previous studies conducted on Zymoseptoria tritici have reported that strains that grew faster under a favorable environment were the most sensitive to oxidative stress [56]. Our data-at least, those for F. proliferatum-confirmed these findings as PRO1, with the lowest growth rate in the range 15-30 • C, was the fastest to grow at 35 • and the only one able to survive at 40 • C. Concerning the three F. subglutinans isolates, their growth was optimal in the range 20-25 • C, with an average decrease of 25% at 30 • C. The best performance among F. subglutinans was observed for the SUB1 isolate, the which was the only isolate able to survive at 35 • C. The presented data, therefore, strengthen previous findings on the warmer environmental conditions required by F. proliferatum than F. subglutinans [12], but also highlight the presence of isolates characterized by adaptability to high temperature (and, thus, oxidative stress), and the possibility of a selective pressure to new conditions, as has been observed for other pathogens [57,58].…”

“…Concerning F. proliferatum , the radial growth of the isolate PRO1 up to 30 °C was lower, when compared to PRO2 and PRO3, but PRO1 showed the best values at 35 °C. Previous studies conducted on Zymoseptoria tritici have reported that strains that grew faster under a favorable environment were the most sensitive to oxidative stress [ 56 ]. Our data—at least, those for F. proliferatum —confirmed these findings as PRO1, with the lowest growth rate in the range 15–30 °C, was the fastest to grow at 35° and the only one able to survive at 40 °C.…”

“…For these reasons, it is possible to suppose that, as a side-effect of the activity of H 2 O 2 on tissues, the increased biomass could be the fungal attempt to balance the exogenous oxidative stress by consuming nutrients that provide reducing power. The fact that this aspect occurred for some isolates could be dependent on the specific thermotolerance of the strain, determined by its inherent growth capability and genetic traits (QTL) that make these isolates better-or worse-performing under stress conditions [56]. Fungi possess more or less efficient oxidant scavenging capabilities, depending on the species [35,42], isolate, and chemotype [29,56], or on physiological adaptation [64].…”

“…The fact that this aspect occurred for some isolates could be dependent on the specific thermotolerance of the strain, determined by its inherent growth capability and genetic traits (QTL) that make these isolates better-or worse-performing under stress conditions [56]. Fungi possess more or less efficient oxidant scavenging capabilities, depending on the species [35,42], isolate, and chemotype [29,56], or on physiological adaptation [64]. The above-mentioned variables could, therefore, explain the different effects that an identical H 2 O 2 concentration produced in the surveyed pathogens.…”

Genome-wide association mapping reveals genes underlying population-level metabolome diversity in a fungal crop pathogen

“…We identified genetic polymorphisms close to genes encoding a broad range of functions with an enrichment of transporter and catalytic functions. Such transporters include major facilitator superfamily (MFS) transporters known to modulate fungicide and stress tolerance (Roohparvar et al ., 2007; Omrane et al ., 2017; Zhong et al ., 2021). MFS transporters are also involved in the secretion of phytotoxins during infection and, hence, can contribute to virulence (Choquer et al ., 2007; Temme et al ., 2012; Menke et al ., 2012).…”