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NADPH Oxidase Regulates the Growth and Pathogenicity of Penicillium expansum.

ABSTRACT: The occurrence of reactive oxygen species (ROS) during the colonization of necrotrophic pathogens attacking fruit is critical during the attack, but its importance in Penicillium expansum remains unclear. This study aimed to determine the regulatory effects of NADPH oxidase (Nox) genes on the growth and pathogenicity of P. expansum in apple fruits. Deletion mutants of ΔPeNoxA, ΔPeNoxR, and ΔPeRacA genes were constructed to determine the contribution to the colonization process. The ΔPeRacA strain had a significant effect on the reduction of growth and pathogenicity, the ΔPeNoxA strain negatively regulated the growth and development of P. expansum and did not show any significant effect on the pathogenicity, and the ΔPeNoxR strain showed no effect on the growth or pathogenicity of P. expansum in the apple fruits. However, analysis of the content of O₂ ^- and H₂O₂ in the mycelium of all the Nox mutants showed a significant reduction, confirming the functionality of Nox mutations. Growth under stress conditions in the presence of Congo red, sodium lauryl sulfate, and H₂O₂ showed a negative effect on the radial growth of ΔPeNoxA, but a positive effect on radial growth reduction by ΔPeNoxR and ΔPeRacA mutants was shown. Interestingly, the host antioxidant activity levels of superoxide dismutase (SOD) andcatalase (CAT) in the fruits after inoculation with ΔPeNoxA, ΔPeNoxR, and ΔPeRacA mutants declined, suggesting reduced ROS accumulation in the colonized region. These results suggest that PeNoxA, PeNoxR, and PeRacA differentially regulate the growth and pathogenicity of P. expansum by producing ROS, and that PeRacA showed the strongest regulatory effect.

SUBMITTER: Zhang X

PROVIDER: S-EPMC8387719 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Fruit blue mold disease and patulin contamination caused by Penicillium expansum lead to huge economic losses and food safety concerns worldwide. Many genes have been proven to be involved in the regulation of pathogenic and toxigenic processes of P. expansum. Histone H3 lysine 4 (H3K4) methylation is well recognized for its association with chromatin regulation and gene transcription. However, it is not clear whether H3K4 methylation is related to infection and patulin biosynthesis in Penicillium. Here, we characterized PeSet1, which is responsible for H3K4me1/me2/me3 in P. expansum. The deletion of PeSet1 caused severe defects in hyphal growth, conidiation, colonization, patulin biosynthesis, and stress responses. Moreover, we demonstrated that PeSet1 is involved in the regulation of patulin biosynthesis by mediating the expression of patulin cluster genes and crucial global regulatory factors. Likewise, PeSet1 positively regulated key genes in β-1,3-glucan biosynthesis and the reactive oxygen species scavenging process to modulate cell wall integrity and oxidative stress responses, respectively. Collectively, we have proven for the first time the function of Set1 in patulin biosynthesis and the crucial role of Set1 in colonization and stress responses in P. expansum. IMPORTANCE Penicillium expansum is one of the most important plant fungal pathogens, which not only causes blue mold rot in various fruits, leading to huge decay losses, but also produces mycotoxin patulin, posing a threat to human health. Both pathogenesis and patulin biosynthesis in P. expansum are regulated by complex and sophisticated networks. We focused on the epigenetic modification and identified a conserved histone H3K4 methyltransferase PeSet1 in P. expansum. Our work revealed the important role of PeSet1 in growth, development, colonization, patulin production, and stress responses of P. expansum. In particular, we originally described the regulation of Set1 on patulin biosynthetic pathway. These findings will provide new targets for the prevention and control of blue mold disease and patulin contamination.

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NADPH Oxidase Regulates the Growth and Pathogenicity of Penicillium expansum.

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