Plant Pathogens
Fungal plant pathogens
The life histories of fungal pathogens that exploit flowers are remarkably diverse, and these pathogens can be transmitted by invertebrates (Jennersten
1988; Roy
1993) as well as vertebrates (Lara & Ornelas
2003). The most well-studied floral fungal pathogen is
Microbotryum violaceum, which infects plants in the family Caryophyllaceae. Spores are vectored by insect visitors from diseased to healthy flowers (Jennersten
1988; Shykoff & Bucheli
1995), where, following germination and meiosis, the fungal cells conjugate and directly penetrate the plant epidermis (Schafer
et al.
2010). Mature flowers on which spores are deposited do not typically become diseased; rather, the fungus grows into the plant meristem and destroys developing pollen mother cells, replacing anther sacs with fungal spores (Schafer
et al.
2010). A more manipulative tactic used by fungal pathogens involves the induction of pseudoflowers to attract floral visitors. For example, primary infection by mummyberry disease (
Monilinia vaccinii-corymbosi) causes infected shoots of blueberry (
Vaccinium spp.) to exude a sugar-rich solution, reflect UV light (Batra & Batra
1985) and produce floral odour compounds (McArt
et al. unpublished data). Insects visit the pathogen-induced pseudoflowers, acquire asexual conidia and vector this infectious stage to the stigmas of blueberry flowers. Conidia morphologically and chemically mimic pollen grains, and hyphae ingress down the stylar canal in a manner similar to pollen tube growth (Ngugi & Scherm
2004), culminating in fruit infection.
Bacterial plant pathogens
Only two bacterial pathogens of plants are known to rely on pollinators as vectors, but both cause extensive agricultural losses.
Erwinia amylovora (fire blight) infects plants in the family Rosaceae, including fruit crops such as apple and pear (Farkas
et al.
2011). The most common site of
E. amylovora infection is the hypanthium, where nectar is secreted. The pathogen then gains entry to inner floral tissues via the nectar-secreting stomata (Farkas
et al.
2011). Bees are common vectors of
E. amylovora, moving the pathogen from diseased to healthy flowers (Alexandrova
et al.
2002).
Erwinia tracheiphila, the causative agent of bacterial wilt disease in cucurbits, is transmitted via the frass of cucumber beetles that have fed on infected vegetative tissues. While infection via beetle-damaged leaves is well-studied, pollen-feeding beetles can also infect plants when frass falls onto the nectary and bacteria pass into the xylem (Sasu
et al.
2010a).
Viral plant pathogens
All viral plant pathogens known to be vectored by floral visitors are transmitted in pollen (Card
et al.
2007). These viruses are located in or on pollen grains, occasionally cause the pollen to become inviable and typically lead to systemic plant infections.
Prunus necrotic ringspot virus, prune dwarf virus, tobacco streak virus and sowbane mosaic virus are all pollen vectored by thrips (Card
et al.
2007 and references therein). In each case, infected pollen attaches mechanically to the insect exoskeleton during foraging in flowers. The disease is vectored to additional plants when the pollen-associated virus detaches and enters feeding wounds caused by thrips in various plant tissues. Several additional pollen viruses are vectored by larger floral visitors, such as bees. For example, blueberry shock ilarvirus is transmitted by honey bees during foraging for pollen and nectar (Bristow & Martin
1999).
Nectar yeast and bacteria
Nectar itself is prone to microbial colonisation by yeast and bacteria that can tolerate high sugar concentrations, and several studies suggest that pollinators vector these nectar microbes (e.g. Herrera
et al.
2009; Schaeffer & Irwin in press). Nectar-inhabiting microorganisms can negatively affect plants through both indirect and direct pathways. For example, nectar microbes can alter nectar pH, H2O2 concentration and sugar concentration and composition, thus altering floral attractiveness and pollination (Vannette
et al.
2013). Alternatively, nectar microbes can directly reduce seed production by drawing carbohydrate resources away from developing ovaries (Golonka
2002) or inhibiting pollen germination and pollen tube formation (Eisikowitch
et al.
1990). It is important to note, however, that nectar microbes do not always harm plants. In some systems nectar microbes increase pollinator visitation to flowers (e.g. Herrera
et al.
2013; Schaeffer & Irwin in press). This increase in pollinator visitation increases pollen donation, a component of male plant reproduction, in
Delphinium nuttallianum (Schaeffer & Irwin in press). A major challenge for future research is to understand how ecological factors shape conditionally mutualistic or antagonistic interactions between nectar microbes and plants.
