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

Zhanhong Han,Yang Bi,Zhenyu Wang,Di Gong,Bin Wang,Baojun Li,Yuanyuan Zong,Edward Sionov,Dov Prusky

doi:10.3390/antiox10050692

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.

Highlights

Introduction distributed under the terms andPathogens can dynamically alter the local pH at an infection site to suit the increasing expression of pathogenicity factors and the enzymatic arsenal that contribute to pathogenicity [1]
Given that ammonia can activate H+ -ATPase activity, which affects the influx of Ca2+ [14], it is possible that Ca2+ can activate calciumdependent protein kinases (CDPKs) at downstream targets [29] and generate of
Apple fruits colonized by T. roseum spore suspensions at different pH values modulated the activity of pectolytic and cellulolytic enzymes at increasing pH values, but the local environmental pH levels have differential effects on reactive oxygen species (ROS) production, cell membrane integrity, and ROS scavenging systems

Summary

Introduction

Introduction distributed under the terms andPathogens can dynamically alter the local pH at an infection site to suit the increasing expression of pathogenicity factors and the enzymatic arsenal that contribute to pathogenicity [1]. The ability to modify pH may be expressed in either direction, and fungi that raise or reduce it are described as ‘alkalizing fungi’ or ‘acidifying fungi’, respectively. Antioxidants 2021, 10, 692 alkalization by fungi is achieved by active secretion of ammonia, which is produced as a result of protease activity and deamination of amino acids. Other postharvest pathogens, such as Penicillium expansum, Penicillium digitatum, Penicillium italicum [2], Botrytis cinerea [3], and Sclerotinia sclerotiorum [4,5], utilize tissue acidification by organic acids to support their attack. Trichothecium roseum is an important postharvest pathogen with a wide range of fruit hosts [6] such as apples, pears, muskmelons, apricots, tomatoes, and other fruit [6]

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