Floral Scent Mimicry and Vector-Pathogen Associations in a Pseudoflower-Inducing Plant Pathogen System

Abstract

Several fungal plant pathogens induce ‘pseudoflowers’ on their hosts to facilitate insect-mediated transmission of gametes and spores. When spores must be transmitted to host flowers to complete the fungal life cycle, we predict that pseudoflowers should evolve traits that mimic flowers and attract the most effective vectors in the flower-visiting community. We quantified insect visitation to flowers, healthy leaves and leaves infected with Monilinia vaccinii-corymbosi (Mvc), the causative agent of mummy berry disease of blueberry. We developed a nested PCR assay for detecting Mvc spores on bees, flies and other potential insect vectors. We also collected volatiles from blueberry flowers, healthy leaves and leaves infected with Mvc, and experimentally manipulated specific pathogen-induced volatiles to assess attractiveness to potential vectors. Bees and flies accounted for the majority of contacts with flowers, leaves infected with Mvc and healthy leaves. Flowers were contacted most often, while there was no difference between bee or fly contacts with healthy and infected leaves. While bees contacted flowers more often than flies, flies contacted infected leaves more often than bees. Bees were more likely to have Mvc spores on their bodies than flies, suggesting that bees may be more effective vectors than flies for transmitting Mvc spores to flowers. Leaves infected with Mvc had volatile profiles distinct from healthy leaves but similar to flowers. Two volatiles produced by flowers and infected leaves, cinnamyl alcohol and cinnamic aldehyde, were attractive to bees, while no volatiles manipulated were attractive to flies or any other insects. These results suggest that Mvc infection of leaves induces mimicry of floral volatiles, and that transmission occurs primarily via bees, which had the highest likelihood of carrying Mvc spores and visited flowers most frequently.

Evolution and Manipulation of Vector Host Choice

“…Phytoplasma are bacterial plant pathogens that are known to convert infected plants into more attractive hosts for their leafhopper vectors [48]. The causative agent of mummy berry disease of blueberry is the fungal pathogen Monilinia vaccinia-corymbosi which induces the production of pseudoflowers and mimicry of floral volatiles that attract insect vectors towards infected plats [49].…”

Pathogen-induced changes in floral scent may increase honeybee-mediated dispersal of Erwinia amylovora

“…Many pollinatorvectored pathogens have been described previously [8], but only few of them are bacterial pathogens, mainly belonging to the genus Erwinia. In addition, the influence of VOC changes induced by pathogen infection on pollinators' behaviour was investigated only for two highly specialised fungal pathogens [10][11][12][13].…”

“…Some of these pathogens manipulate insect behaviour to enhance their own spread, primarily by modifying host scent and/or nutritional reward [9]. However, the role of VOCs in pollinator-mediated pathogen transmission has been investigated only for a few, highly specialised fungal species: pseudoflower-producing foliar pathogens, such as Puccinia spp., attract insects to promote their own spread or sexual conjugation [10][11][12], while the infection by anther pathogen Microbotryum violaceum, associated to lower nutritional reward and VOC release, reduces the visitation rate by oviposing moths [13].…”

A Novel In Silico Method for Molecular Mimicry Detection Finds a Formin with the Potential to Manipulate the Maize Cell Cytoskeleton

“…To achieve this, some microbial pathogens have evolved the capacity to mimic characteristics of their host. For example, the conidia of the fungus Monilinia vaccinii-corymbosi mimics the germinating pollen of the blueberry, thus enabling it to gain access to the plant ovary (McArt et al 2016;Ngugi and Scherm 2006). Similarly, the rice false smut fungus mimics successful fertilization (producing false smut balls).…”