Mechanisms of primed defense: plant immunity induced by endophytic colonization of a mycovirus-induced hypovirulent fungal pathogen

Authors: Pedersen, Connar; Marzano, Shin-Yi

Submitted to: Molecular Plant-Microbe Interactions
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/17/2023
Publication Date: 7/17/2023
Citation: Pedersen, C.J., Marzano, S.L. 2023. Mechanisms of primed defense: plant immunity induced by endophytic colonization of a mycovirus-induced hypovirulent fungal pathogen. Molecular Plant-Microbe Interactions. 36(11):726-736. https://doi.org/10.1094/mpmi-06-23-0083-r.
DOI: https://doi.org/10.1094/mpmi-06-23-0083-r

Interpretive Summary: The widespread family Genomoviridae includes viruses with circular single-stranded DNA genomes encoding two proteins. All members of the family have no host identified except for two that have been identified infecting fungi. Both genomoviruses identified in fungi show an induction of hypovirulence, or reduc-tion of virulence, in their fungal hosts. A plant endophyte is a microbe growing in plant which may be beneficial or detrimental to the plant. The effects and eco-logical interactions of a mycovirus-infected fungal strain growing as an endo-phyte has not been elucidated. Here we report a genomovirus capable of repro-gramming the parasitic Sclerotinia sclerotiorum into a symbiotic endophyte which confers disease resistance traits and boosts photosynthetic ability of the plant, with potential to increase plant resilience.

Technical Abstract: Bio-priming of seeds is usually achieved through the colonization of plant-growth promoting rhizobacteria to increase resistance to biotic or abiotic stresses. This study characterized the effects of a mycovirus-infected fungal phytopathogen, Sclerotinia sclerotiorum, colonization on plant seeds. Pinto bean (Phaseolus vulgaris) and soybean (Glycine max) seeds were inoculated via root colonization in the field and in the greenhouse, respectively. The impact was examined through phenotype measurements in the field, including biomass, chlorophyll fluorescence efficiency and yield data, as well as greenhouse pathogenicity assay and gene differential expression analysis. The mycovirus abolished the virulence of S. sclerotiorum which induced a defense response upon colonizing plants evidenced by reduced lesion growth of pathogenic S. sclerotiorum in a cut-petiole assay. RNA-Seq analysis reveals 1,500 differentially expressed genes and indicates an increase in the expression of salicylic acid and jasmonic acid pathways. Gene ontology groups relating to photosynthetic function were enriched which also was reflected in an in-crease in photosystem II photochemical efficiency (Fv/Fm) values in both the field and green-house measurements. In test tubes, an ectomycorrhizal growth of the endophytic fungus was observed under the sectioning microscope. Therefore, a mycovirus can modulate the pathogenic fungus, S. sclerotiorum, to become a beneficial endophyte and induce plant resistance as well as improve photosynthetic capacity, likely due to a downregulation of an fungal virulence effector, revealing the influence of mycovirus infection on the fungus-plant interaction.