The Good, the Bad, and the Ugly: Mycotoxin Production During Postharvest Decay and Their Influence on Tritrophic Host-Pathogen-Microbe Interactions

Abstract

Mycotoxins are a prevalent problem for stored fruits, grains, and vegetables. Alternariol, aflatoxin, and patulin, produced by Alternaria spp., Aspergillus spp., and Penicillium spp., are the major mycotoxins that negatively affect human and animal health and reduce fruit and produce quality. Control strategies for these toxins are varied, but one method that is increasing in interest is through host microbiome manipulation, mirroring a biocontrol approach. While the majority of mycotoxins and other secondary metabolites (SM) produced by fungi impact host-fungal interactions, there is also an interplay between the various organisms within the host microbiome. In addition to SMs, these interactions involve compounds such as signaling molecules, plant defense and growth hormones, and metabolites produced by both the plants and microbial community. Therefore, studies to understand the impact of the various toxins impacting the beneficial and harmful microorganisms that reside within the microbiome is warranted, and could lead to identification of safe analogs for antimicrobial activity to reduce fruit decay. Additionally, exploring the composition of the microbial carposphere of host plants is likely to shed light on developing a microbial consortium to maintain quality during storage and abate mycotoxin contamination.

Keywords: biocontrol; biofilm; carposphere; metabolite; microbiome; mycotoxin; postharvest pathogen.

FIGURE 1

The relationship between the host, pathogen and biofilm is an intricate process containing multiple components. Hormones, volatile organic compounds (VOC), and signaling molecules, such as ethylene, gibberellin, salicylic acid, jasmonic acid, and brassinosteroids, are translocated throughout the fruit as well as produced by microbes and used in postharvest control efforts. Mycotoxins like aflatoxin, patulin, and alternariol are produced by phytopathogenic fungi, and quorum sensing molecules (acyl-homoserine-lactones and autoinducer peptides) are secreted by biofilm-forming microbes. Elicitors are recognized by the fruit in response to pathogens, resulting in an oxidative burst. Both plant and microbial cell wall degrading enzymes (CWDE) and additional antimicrobial compounds are released to manipulate the surrounding species composition. These molecules and abiotic factors during postharvest storage can impact virulence or disease susceptibility, growth, and development of all the interacting organisms within the carposphere. Color variety within molecule categories represents variability within the grouping (e.g., multiple hormones present in the interaction). This figure was produced using Biorender.com.

FIGURE 2

Impacts of signaling molecules (center; example molecules listed clockwise are ethylene, salicylic acid, abscisic acid, and jasmonic acid) on the microbial composition associated with the host (left) and direct fruit host processes (right). In addition to influencing their own biology and/or populations, producers of these molecules can also impact other species within the vicinity, including facilitating interactions between the host fruit and carposphere. This figure was produced using Biorender.com.