Infection Strategies Deployed by Botrytis cinerea, Fusarium acuminatum, and Rhizopus stolonifer as a Function of Tomato Fruit Ripening Stage

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2019-03Department
Bioquímica y Biología Molecular, Microbiología, Medicina Preventiva, Salud PúblicaSource
Front. Plant Sci. 2019 10:223.Abstract
Worldwide, 20–25% of all harvested fruit and vegetables are lost annually in the field
and throughout the postharvest supply chain due to rotting by fungal pathogens.
Most postharvest pathogens exhibit necrotrophic or saprotrophic lifestyles, resulting in
decomposition of the host tissues and loss of marketable commodities. Necrotrophic
fungi can readily infect ripe fruit leading to the rapid establishment of disease symptoms.
However, these pathogens generally fail to infect unripe fruit or remain quiescent until
host conditions stimulate a successful infection. Previous research on infections of
fruit has mainly been focused on the host’s genetic and physicochemical factors that
inhibit or promote disease. Here, we investigated if fruit pathogens can modify their own
infection strategies in response to the ripening stage of the host. To test this hypothesis,
we profiled global gene expression of three fungal pathogens that display necrotrophic
behavior—Botrytis cinerea, Fusarium acuminatum, and Rhizopus stolonifer—during
interactions with unripe and ripe tomato fruit. We assembled and functionally annotated
the transcriptomes of F. acuminatum and R. stolonifer as no genomic resources
were available. Then, we conducted differential gene expression analysis to compare
each pathogen during inoculations versus in vitro conditions. Through characterizing
patterns of overrepresented pathogenicity and virulence functions (e.g., phytotoxin
production, cell wall degradation, and proteolysis) among the differentially expressed
genes, we were able to determine shared strategies among the three fungi during
infections of compatible (ripe) and incompatible (unripe) fruit tissues. Though each
pathogen’s strategy differed in the details, interactions with unripe fruit were commonly
characterized by an emphasis on the degradation of cell wall components, particularly
pectin, while colonization of ripe fruit featured more heavily redox processes, proteolysis,
metabolism of simple sugars, and chitin biosynthesis. Furthermore, we determined that
the three fungi were unable to infect fruit from the non-ripening (nor) tomato mutant, confirming that to cause disease, these pathogens require the host tissues to undergo
specific ripening processes. By enabling a better understanding of fungal necrotrophic
infection strategies, we move closer to generating accurate models of fruit diseases and
the development of early detection tools and effective management strategies.
Subjects
broad host range pathogens; necrotrophic fungi; fruit-pathogen interactions; rotting; necrotic response; cell wall degrading enzymes; redox; de novo transcriptomesCollections
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