Biocontrol efficiency of Meyerozyma guilliermondii Y-1 against apple postharvest decay caused by Botryosphaeria dothidea and the possible mechanisms of action

Highlights

• Meyerozyma guilliermondii Y-1 effectively controls apple ring rot caused by B. dothidea;

• M. guilliermondii Y-1 inhibits mycelial growth and spore generation of B. dothidea;

• M. guilliermondii Y-1 competes for space and nutrient with pathogen;

• M. guilliermondii Y-1 promotes the activities of defensive enzymes and up-regulates pathogenesis-related genes expression.

Abstract

Apple ring rot, caused by Botryosphaeria dothidea, is one of the important diseases in China. This pathogen infects branches and fruit and also results in fruit decay during storage. Biocontrol agents have been proposed to reduce apple decays during storage and are considered as a promising alternative strategy to traditional chemical treatment. In this study, Meyerozyma guilliermondii Y-1, isolated from healthy grape fruit, was firstly evaluated for its biocontrol efficiency against B. dothidea in postharvest apple fruit, and the possible mechanisms were investigated. The results revealed that M. guilliermondii Y-1 treatment effectively reduced apple ring rot caused by B. dothidea in vivo. The disease incidence and lesion diameter were reduced by 32.22% and 57.51% compared with those of control fruit. Furthermore, the use of filtrate and autoclaved culture of M. guilliermondii Y-1 also showed a certain degree of control efficiency against fruit ring rot. M. guilliermondii Y-1 significantly inhibited the mycelial growth and spore generation of B. dothidea in vitro and exhibited an obvious ability to colonize in apple fruit wounds and surface at 25 °C or 4 °C. In addition, M. guilliermondii Y-1 treatment significantly enhanced the activities of catalase (CAT), superoxide dismutase (SOD), peroxidase (POD), phenylalanine ammonialyase (PAL), and polyphenoloxidase (PPO), promoted the total phenolics content, and alleviated lipid peroxidation in apple fruit. As expected, we found that the expression of four pathogenesis-related proteins genes (MdPR1, MdPR5, MdGLU, and MdCHI) was remarkably increased by M. guilliermondii Y-1 treatment. Our data together suggest that M. guilliermondii Y-1 is a potential biocontrol agent against B. dothidea postharvest infection in apple fruit, partially through inhibiting mycelial growth and spore germination of B. dothidea, competing for space and nutrient with pathogen, and inducing resistance in apple fruit by stimulating a series of defense responses.

Introduction

Ring rot caused by Botryosphaeria dothidea is a common postharvest disease that significantly affects apple production (Tang et al., 2012; Q. Zhang et al., 2016). Differently from other postharvest diseases, B. dothidea also infects branches of apple trees, resulting in warts and cankers. The pathogen could overwinter and survive several years on diseased or dead branches (Tang et al., 2012; Zhao et al., 2016). Due to the large amount of B. dothidea in the orchards and the pathogen could infect apple latently at the growth stage, it is difficult to control apple ring rot (Liu et al., 2011; Q. Zhang et al., 2016).

There has been an increase in the use of biological control agents as an alternative to the synthetic fungicides to contain fruit postharvest decay over the past decade (Droby et al., 2016). In the case of apple fruit, biocontrol agents have also been proposed to reduce apple decays during storage (He et al., 2020; Ippolito et al., 2000; Li et al., 2011; Q. Zhang et al., 2016). Especially, yeasts have attracted considerable interest as postharvest biocontrol agents because of their ability to colonize and grow rapidly in the wounded tissues and survive on fruit surfaces for a long period, even at low temperature (Perez et al., 2019; Rodriguez Assaf et al., 2020; Shen et al., 2019). Yeasts also inhibit spore germination and mycelia growth of pathogens, produce volatile compounds, and induce fruit resistance during postharvest (da Cunha et al., 2018; Fiori et al., 2014; He et al., 2020; Lu et al., 2013). Additionally, biocontrol yeasts are perceived as environmentally safer and more acceptable to the general public (Droby et al., 2009).

In the postharvest fruit-yeast biocontrol system, induced disease resistance can be triggered by Yarrowia lipolytica in table grapes against Penicillium rubens infection (Wang et al., 2019), by Pichia membranefaciens in peaches to control Rhizopus rot (Zhang et al., 2020), and by Rhodosporidium paludigenum in citrus and pear against P. digitatum and P. expansum, respectively (Lu et al., 2013; Sun et al., 2018). Due to the complex interactions among pathogen, host and yeast, the mechanisms of action by which biocontrol yeasts induce resistance remain largely unknown (Droby et al., 2009). Previous studies have demonstrated that Meyerozyma guilliermondii could control postharvest blue mold decay of pear and apple. However, whether M. guilliermondii is effective against B. dothidea in apple fruit and the possible mechanisms have yet to be investigated.

This study presented a biocontrol yeast M. guilliermondii Y-1, which was isolated in our laboratory from the surfaces of grape picked in a commercial orchard. The objective of current research was to determine its effects on mycelial growth and spore germination of B. dothidea and evaluate its efficiency in controlling apple ring rot. Moreover, the ability of M. guilliermondii Y-1 to colonize wounds and the surface of apple fruit was determined, and other possible mechanisms of action underlying its high efficiency against B. dothidea were explored.