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Oxidative stress response pathways in fungi

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Abstract

Fungal response to any stress is intricate, specific, and multilayered, though it employs only a few evolutionarily conserved regulators. This comes with the assumption that one regulator operates more than one stress-specific response. Although the assumption holds true, the current understanding of molecular mechanisms that drive response specificity and adequacy remains rudimentary. Deciphering the response of fungi to oxidative stress may help fill those knowledge gaps since it is one of the most encountered stress types in any kind of fungal niche. Data have been accumulating on the roles of the HOG pathway and Yap1- and Skn7-related pathways in mounting distinct and robust responses in fungi upon exposure to oxidative stress. Herein, we review recent and most relevant studies reporting the contribution of each of these pathways in response to oxidative stress in pathogenic and opportunistic fungi after giving a paralleled overview in two divergent models, the budding and fission yeasts. With the concept of stress-specific response and the importance of reactive oxygen species in fungal development, we first present a preface on the expanding domain of redox biology and oxidative stress.

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Fig. 1

source of ROS production in cells is mitochondria, followed by the plasma membrane-embedded NADPH oxidase (NOX) complex. Electrons may leak during the gradual reduction process of oxygen (O2) to water by the mitochondrial respiratory chain, mainly from complexes I and III, leading to the formation of superoxide anion O2⋅─. The latter constitutes the main precursor for the formation of other ROS, including hydrogen peroxide (H2O2) by the activity of superoxide dismutase (SOD), hydroxyl radical (OH) via the Fenton or Haber–Weiss reaction favored by metal catalysts, and hydroperoxyl radical (HOO) via the protonation of O2⋅─. The oxygen singlet (1O2) corresponds to the oxygen molecule in an electronically excited state due to inputs of energy that rearrange the electrons. These ROS can diffuse from the intermembrane space to (i) the mitochondrial matrix, where the mitochondrial Mn-SOD (known as Sod2) converts O2⋅─ to H2O2 which is further reduced to water by the mitochondrial peroxiredoxin Prx1; or to (ii) the cytosol, where they are neutralized by the predominantly cytosolic Cu, Zn-SOD (known as Sod1), catalase, and components of the NADPH-dependent systems, the glutathione and thioredoxin systems. High concentrations of ROS molecules (oxidative distress), whether produced endogenously or exogenously, may damage vital macromolecules, including nucleic acids, proteins, and lipids. Nontoxic concentrations are still beneficial for cellular signaling in growth and differentiation (oxidative eustress). e, electron; H+, proton; ETC, electron transport chain. Undashed black arrows refer to reactions allowing ROS formation. Dashed black arrows signify diffusion across compartments. Blue arrows point final neutralization step of ROS into water. This figure was created using BioRender

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