Plant venereal diseases: insights from a messy metaphor

Abstract

SummaryThe concept of plant venereal disease is examined from definitional, operational and axiomatic viewpoints. The transmission of many plant pathogens occurs during the flowering phase and is effected either by pollinators or by wind dispersal of spores from inflorescences. Attraction of insects by pseudo-flowers or sugary secretions also serves to spread many diseases. Given the diversity of processes involved, a simple all-encompassing parallel with animal venereal diseases is not possible. Operationally establishing the routes of disease transmission, as well as quantifying the relative magnitudes of these different routes, remains critical for understanding disease dynamics and controlling spread in agricultural contexts. From an axiomatic viewpoint, sexually transmitted diseases are characterized by frequency-dependent transmission, transmission in the adult stage, and by virulence effects involving sterility rather than mortality. These characteristics serve to differentiate the dynamics and evolution of sexually transmitted diseases from that of other diseases and are features that are also shared by many pollinator-transmitted diseases. However, the majority of plant diseases that involve the reproductive structures show a rich biology that defies easy categorization. The experimental convenience of plants and their pathogens is likely to play an important role in understanding the evolution of disease traits, irrespective of what descriptive terms are applied to the natural history of the transmission process.

Host Manipulation by Parasites: Cases, Patterns, and Remaining Doubts

“…The fungus M. violaceum causes the abortion of ovaries, replaces the pollen with fungal spores, and uses insect pollinators for their transmission (Wennström et al, 2003;Antonovics, 2005;Sloan et al, 2008), whereas, quite remarkably, the rust fungus Puccinia monoica forms flowerimitating pseudoflowers on Arabis holboellii (Brassicaceae), which attract insects aiding the sexual reproduction of the fungus (Roy, 1993). Recently, many other manipulations have been reported for plant pathogens, including alterations in plant odor or in the quality and quantity of nutrients that move in the phloem.…”

The incidence and selection of multiple mating in plants

“…What might the costs and benefits of polyandry be for the female function of plants? Almost certainly, one of the costs faced by animals will also apply to plants: the increased risk of becoming infected by disease as a result of mating with more than one male [54,55]. Work on the dioecious perennial herb Silene latifolia has shown that increased pollinator visits to female flowers is positively associated with the probability of infection by the anther-smut fungus, Microbotryum violaceum, which causes both males and females to produce sterile staminate (male) flowers that disperse only fungal spores [56,57].…”

Silene as a model system in ecology and evolution

“…This fungus invades the plant and produces spores in the anthers, which replace the normal pollen. The disease sterilizes its host and is transmitted when insects carry spores from infected to healthy flowers during pollination (Antonovics, 2005). In females of dioecious host species, anther development is induced by the pathogen, and this remarkable symptom caught the attention of early researchers including Darwin (1863) to be followed by a series of studies using the pathogen to understand the host's sexual development (for example, Strasburger, Silene as a model system in ecology and evolution G Bernasconi et al 1900; Shull, 1910).…”