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

Abstract

Honeybees are well recognised for their key role in plant reproduction as pollinators. On the other hand, their activity may vector some pathogens, such as the bacterium Erwinia amylovora, the causative agent of fire blight disease in pomaceous plants. In this research, we evaluated whether honeybees are able to discriminate between healthy and E. amylovora-infected flowers, thus altering the dispersal of the pathogen. For this reason, honeybees were previously trained to forage either on inoculated or healthy (control) apple flower. After the training, the two honeybee groups were equally exposed to inoculated and control flowering apple plants. To assess their preference, three independent methods were used: (1) direct count of visiting bees per time frame; (2) incidence on apple flowers of a marker bacterium (Pantoea agglomerans, strain P10c) carried by foragers; (3) quantification of E. amylovora populations in the collected pollen loads, proportional to the number of visits to infected flowers. The results show that both honeybee groups preferred control flowers over inoculated ones. The characterisation of volatile compounds released by flowers revealed a different emission of several bioactive compounds, providing an explanation for honeybee preference. As an unexpected ecological consequence, the influence of infection on floral scent increasing the visit rate on healthy flowers may promote a secondary bacterial spread.

Roles of plant volatiles in defence against microbial pathogens and microbial exploitation of volatiles

“…However, honeybees are attracted to healthy as opposed to diseased flowers. Cellini et al () suggested that this discrimination may be due to differential emissions of volatile compounds. For example, methyl salicylate, known to play a significant role in plant defence against biotrophic pathogens, is released by inoculated flowers and appears to repulse the honeybees.…”

Nectar Microbial Diversity and Changes Associated with Environmental Exposure

“…The nectar of environment exposed N. pseudonarcissus was dominated by sequences similar to Erwinia (82%) and Pseudomonas (18%). Both Erwinia and Pseudomonas have been documented in nectar environments [60,61] with both being the only two genera currently reported to be directly associated with pollinating species acting as bacterial vectors [62]. Similarly, the environment exposed D. purpurea was found to have a higher detectable OTU richness in comparison to non-environment exposed D.…”

Gazing into the anthosphere: considering how microbes influence floral evolution

“…The complex mixtures of volatiles produced by flowers can affect microbial community composition (Boachon et al ., ). Floral microbes can add scent compounds to flowers, and alter floral scent emission by inducing, reducing and/or even catabolizing floral chemistry (Peñuelas et al ., ; Helletsgruber et al ., ; Burdon et al., , Cellini et al ., ). Microbially‐mediated changes to key floral volatiles (e.g.…”

“…Microbially‐mediated changes to key floral volatiles (e.g. linalool) potentially alter pollinator behavior (Burdon et al., ; Cellini et al ., ), and indeed pollinators such as bees can perceive (Rering et al ., ), respond innately, and learn to prefer or avoid microbial scents on flowers (Russell & Ashman, ). Pollinator preferences mediated by floral cues are key drivers of plant fitness and floral evolution (Schiestl & Johnson, ), thus epiphytic microbes that alter or enhance floral scent may shape plant fitness (Helletsgruber et al ., ; Burdon et al., ; Russell & Ashman, ).…”