Systematic characterization of the peroxidase gene family provides new insights into fungal pathogenicity in Magnaporthe oryzae

Abstract

Plants respond to microbial attack by the rapid generation of reactive oxygen species (ROS) as part of innate immunity. Fungal pathogens have evolved effective anti-oxidant defense system as countermeasure. Recent studies proposed peroxidases as components of antioxidant defense system. However, significance of role of fungal peroxidases during interaction with host plants has not been addressed at genomic level to date. Here, we systematically identified peroxidase genes and analyzed their impact on fungal pathogenesis in a model plant pathogenic fungus, Magnaporthe oryzae. Phylogeny reconstruction among 6 fungal species placed Magnaporthe oryzae 27 putative peroxidase genes into 15 clades. Expression profiles showed that majority of them are responsive to in planta condition and in vitro H2O2 where 23 genes were up-regulated during plant infection, and 15 genes were responsive to in vitro H2O2. Among them, seven genes (MoAPX1, MoAPX2, MoCCP1, MoHPX1, MoLDS1, TPX1, and MoPRX1) were selected from clades that do not contain previously characterized genes for functional analysis except TPX1. Our analysis of individual deletion mutants for seven selected genes including MoPRX1 revealed that these genes contribute to fungal development and/or pathogenesis. Importantly, we found significant positive correlation among sensitivity to H2O2, peroxidase activity and fungal pathogenicity. In-depth analysis of MoPRX1 demonstrated that it is a functional ortholog of thioredoxin peroxidase in Saccharomyces cerevisiae and required for detoxification of oxidative burst within host cells. Furthermore, transcriptional profiling of other peroxidases in ΔMoprx1 suggested interwoven nature of peroxidase-mediated anti-oxidation defense system. Taken together, this work provides overview and insights into infection strategy built on evolutionarily conserved peroxidases in the rice blast fungus.