The Effect of Environmental pH during Trichothecium roseum (Pers.:Fr.) Link Inoculation of Apple Fruits on the Host Differential Reactive Oxygen Species Metabolism

Abstract

Trichothecium roseum is an important postharvest pathogen, belonging to an alkalizing group of pathogens secreting ammonia during fungal growth and colonization of apple fruits. Fungal pH modulation is usually considered a factor for improving fungal gene expression, contributing to its pathogenicity. However, the effects of inoculation with T. roseum spore suspensions at increasing pH levels from pH 3 up to pH 7, on the reactive oxygen species (ROS) production and scavenging capability of the apple fruits, affecting host susceptibility, indicate that the pH regulation by the pathogens also affects host response and may contribute to colonization. The present results indicate that the inoculation of T. roseum spores at pH 3 caused the lowest cell membrane permeability, and reduced malondialdehyde content, NADPH oxidases activity, O2●− and H2O2 production in the colonized fruit. Observations of the colonized area on the 9th day after inoculation at pH 3, showed that the rate of O2●− production and H2O2 content was reduced by 57% and 25%, compared to their activities at pH 7. In contrast, antioxidative activities of superoxide dismutase, catalase and peroxidases of fruit tissue inoculated with spores’ suspension in the presence of a solution at pH 3.0 showed their highest activity. The catalase and peroxidases activities in the colonized tissue at pH 3 were higher by almost 58% and 55.9%, respectively, on the 6th day after inoculation compared to inoculation at pH 7. The activities of key enzymes of the ascorbate-glutathione (AsA-GSH) cycle and their substrates and products by the 9th day after fruit inoculation at pH 3 showed 150%, 31%, 16%, and 110% higher activities of ascorbate peroxidase, monodehydroascorbate reductase, dehydroascorbate reductase and glutathione reductase, respectively, compared to pH 7. A similar pattern of response was also observed in the accumulation of ascorbic acid and dehydroascorbate which showed a higher accumulation at pH 3 compared to the colonization at pH 7. The present results indicate that the metabolic regulation of the pH environment by the T. roseum not only modulates the fungal pathogenicity factors reported before, but it induces metabolic host changes contributing both together to fungal colonization.