Bacterial phytopathogen infection disrupts belowground plant indirect defense mediated by tritrophic cascade.

Plants can defend themselves against herbivores through activation of defensive pathways and attraction of third-trophic-level predators and parasites. Trophic cascades that mediate interactions in the phytobiome are part of a larger dynamic including the pathogens of the plant itself, which are known to greatly influence plant defenses. As such, we investigated the impact of a phloem-limited bacterial pathogen, Liberibacter asiaticus (Las), in cultivated citrus rootstock on a well-studied belowground tritrophic interaction involving the attraction of an entomopathogenic nematode (EPN), , to their root-feeding insect hosts, larvae. Using belowground olfactometers, we show how Las infection interferes with this belowground interaction by similarly inducing the release of a C12 terpene, pregeijerene, and disconnecting the association of the terpene with insect presence. larvae that were not feeding but in the presence of a Las-infected plant were more likely to be infected by EPN than those near uninfected plants. Furthermore, nonfeeding larvae associated with Las-infected plants were just as likely to be infected by EPN as those near noninfected plants with larval damage. Larvae of two weevil species, and , were also more attracted to plants with infection than to uninfected plants. larvae were most active when exposed to pregeijerene at a concentration of 0.1 μg/μl. We attribute this attraction to Las-infected plants to the same signal previously thought to be a herbivore-induced plant volatile specifically induced by root-feeding insects, pregeijerene, by assessing volatiles collected from the roots of infected plants and uninfected plants with and without feeding . . Phytopathogens can influence the structuring of soil communities extending to the third trophic level. Field populations of EPN may be less effective at host-finding using pregeijerene as a cue in citrus grove agroecosystems with high presence of Las infection.