Infochemicals mediate communication within and between different trophic levels. In this study, we identified a new type of plant allomone induced by a plant pathogen and perceived by its vector insect Cacopsylla picta. This phloem-feeding psyllid is the main vector of Candidatus Phytoplasma mali, a cell wall-lacking bacterium that causes the so-called apple proliferation disease. In a previous study, we showed that newly emerged females of C. picta were attracted by the odor of phytoplasma-infected apple plants (Malus domestica), which release ss-caryophyllene in contrast to uninfected plants. Here, the attractiveness of this sesquiterpene for C. picta was confirmed in both olfactometer bioassays and field studies. Synthetic ss-caryophyllene was highly attractive to newly emerged adults of C. picta both when offered simultaneously with healthy apple odor and without. The psyllid's response was independent of its odor experience and infection status. These results confirm our previously established hypothesis that this phytoplasma manipulates the behavior of its vector insect by changing the odor blend of its host plant. Deployed in apple orchards, sticky traps baited with ss-caryophyllene dispensers caught both males and females of C. picta. Consequently, this new type of infochemical, i.e., a phytopathogen-induced plant allomone, represents a promising compound to develop innovative techniques for monitoring or maybe even mass trapping of C. picta.

Many phytopathogens that cause worldwide losses of agricultural yield are vectored by herbivorous insects. Limited information is available about the interactions among phytopathogens, host plants, and insect vectors. In this paper, we report that the cell wall-lacking bacterium Candidatus Phytoplasma mali can alter both the odor of its host plant (apple) and behavior of its vector, the univoltine psyllid Cacopsylla picta. Apple trees infected by this phytoplasma emitted higher amounts of beta-caryophyllene when compared to uninfected ones. Psyllids that had no previous contact with Ca. P. mali, as well as infected pyllids, are more attracted by volatiles emitted from phytoplasma-infected apple plants than from uninfected ones. Psyllids that had developed on infected plants without getting infected showed the opposite behavior. These results suggest that the pathogen modifies host plant odor that lures its vector to infected plants. This may result in higher numbers of transmitting vector insects within the population.

We elucidated the life cycles of two jumping plant lice species (Hemiptera: Psyllidae): Cacopsylla picta, a vector of the apple proliferation phytoplasma (Candidatus Phytoplasma mali), and Cacopsylla melanoneura, a nonvectoring species in Germany and some neighbouring countries, which may transmit the phytoplasma in one region in Italy. The adults of C. picta reproduce exclusively on apple and migrate soon after emergence (emigrants) to conifers in mountainous regions, and return to apple plants in early spring (remigrants). Cacopsylla melanoneura also uses conifers as overwintering host plants but prefers to reproduce on hawthorn, despite its ability to reproduce on apple. Both psyllid species used chemical cues for the identification of their alternate host plants during migration. Remigrants of C. melanoneura preferred the odour of their main reproduction host plant hawthorn to apple but preferred the odour of apple when experienced by feeding and oviposition. Although emigrants of C. picta reportedly prefer the odour of apple trees infected by Ca. P. mali, the remigrants of both species did not distinguish between the odours of infected or uninfected apple plants. Investigating the distribution of Ca. P. mali in plant species involved in psyllid life cycle revealed that the phytoplasma is specialized on apple. Infection of apple by Ca. P. mali increased mortality and resulted in decreased body size of C. picta offspring. Gravid females of C. picta preferred to oviposit on non-infected plants. It is concluded that Ca. P. mali indirectly promotes its acquisition from infected plants and transmission to non-infected plants by behavioural manipulation of its vector C. picta