Pseudozyma aphidis activates reactive oxygen species production, programmed cell death and morphological alterations in the necrotrophic fungus Botrytis cinerea

Abstract

Summary Many types of yeast have been studied in the last few years as potential biocontrol agents against different phytopathogenic fungi. Their ability to control plant diseases is mainly through combined modes of action. Among them, antibiosis, competition for nutrients and niches, induction of systemic resistance in plants and mycoparasitism have been the most studied. In previous work, we have established that the epiphytic yeast Pseudozyma aphidis inhibits Botrytis cinerea through induced resistance and antibiosis. Here, we demonstrate that P. aphidis adheres to B. cinerea hyphae and competes with them for nutrients. We further show that the secreted antifungal compounds activate the production of reactive oxygen species and programmed cell death in B. cinerea mycelium. Finally, P. aphidis and its secreted compounds negatively affect B. cinerea hyphae, leading to morphological alterations, including hyphal curliness, vacuolization and branching, which presumably affects the colonization ability and infectivity of B. cinerea . This study demonstrates additional modes of action for P. aphidis and its antifungal compounds against the plant pathogen B. cinerea .

Biocontrol yeasts: mechanisms and applications

“…P. guilliermondii was shown to strongly adhere to hyphae of the plant pathogen B. cinerea and to cause hyphal collapse, presumably due to the secretion of hydrolytic enzymes such as glucanases (see above) (Wisniewski et al 1991). Similarly, the yeast-like Ustilaginomycete Pseudozyma aphidis parasitises the powdery mildew pathogen Podosphaera xanthii and B. cinerea (Calderon et al 2019; Gafni et al 2015). The genus Saccharomycopsis , comprising predacious yeasts directly feeding on their prey, was studied with respect to biocontrol of different Penicillium species as well as clinically relevant yeasts (Junker et al 2017, 2018, 2019; Lachance and Pang 1997; Pimenta et al 2008).…”

Secretion-Based Modes of Action of Biocontrol Agents with a Focus on Pseudozyma aphidis

“…tomato and Xanthomonas campestris pv. campestris [ 61 ].Those metabolites have not yet been identified but they are largely lipophilic and found to induce reactive oxygen species (ROS) accumulation and PCD in B. cinerea hyphal cells [ 62 ].…”

“…In contrast, we have shown that to control gray mold disease caused by B. cinerea, P. aphidis remains as a yeast-like structure and thus does not coil around B. cinerea hyphae [ 44 ]. However, the P. aphidis cells could adhere to B. cinerea hyphae and secrete lytic enzymes and proteases when exposed to B. cinerea cell wall extract, suggesting that close proximity enhances the antibiotic activity and cell wall-degrading enzyme efficiency, thereby also supporting the parasitism dogma [ 62 ]. The dimorphic switch from hypha-like to yeast-like is a well-known phenomenon in fungal pathogens [ 128 ].…”

“…P. aphidis accumulated and proliferated significantly more in the lesion area of B. cinerea than in the uninfected area, suggesting competition for space [ 43 ]. Furthermore, using excess sugar on tomato fruit reduces the competition for nutrients between the fungi and thus decreases the efficacy of P. aphidis against B. cinerea [ 62 ]. The ability to utilize more sources of carbon or nitrogen will give the BCA the advantage over the pathogen, and this will eventually reduce the infection.…”

Response of brassinosteroids to nitrogen rates and their regulation on rice spikelet degeneration during meiosis

“…Like all aerobic organisms, plants have well‐developed metabolic pathways that utilize their energetic potential in the presence of oxygen (Calderón, Rotem, Harris, Vela‐Corcía, & Levy, 2019; Navrot, Rouhier, Gelhaye, & Jacquot, 2007). One potentially damaging effect of metabolism is the deleterious production of reactive oxygen species (ROS), such as hydrogen peroxide (H 2 O 2 ), during normal respiration, photosynthesis, N fixation, and abiotic stress responses (Ahmad, Jaleel, Salem, Nabi, & Sharma, 2010; Chen, Zhang, & Zhang, 2019; Choudhury, Rivero, Blumwald, & Mittler, 2017).…”