Dual biotic stressors shape volatile organic compound emission patterns in pome fruit trees

Plants release volatile organic compounds (VOCs) as part of their defense mechanisms when attacked by phytopathogens and herbivores. These specific volatile emissions can help plants avoid damage. In this study, we investigated the effects of the brown marmorated stink bug (BMSB), Halyomorpha halys, and the phytopathogens "Candidatus phytoplasma mali", causing apple proliferation (AP) or "Ca. P. pyri", causing pear decline (PD) on the volatile emissions from apple (Malus domestica) or pear (Pyrus communis) trees. We analyzed VOCs emitted by uninfected and infected trees exposed to male and female BMSB. Using random forest analysis, the profiles of uninfected trees and those singly infected with PD- or AP-phytoplasma were clearly distinguishable from those infested with BMSB and double-infections with both phytoplasma and BMSB. BMSB-infested apple and pear trees emitted higher levels of linalool and 4,8-dimethyl-1(E)-3,7-nonatriene (DMNT) compared to uninfested trees. In addition, dual infections with phytoplasma and BMSB showed an induction in the content of these VOCs. Phytoplasma-infected apple trees significantly increased emissions of methyl salicylate (MeSA), whereas MeSA content was significantly increased in pear trees exposed to BMSB and also dual infections with phytoplasma and BMSB. In apple trees, α-farnesene was emitted at a higher amount only from phytoplasma-infected trees exposed to BMSB males, whereas in pear trees this VOC was significantly induced in response to female BMSB and dual infections with phytoplasma and female BMSB. Furthermore, we found three acids in healthy pear trees, n-hexadecanoic acid, octadecanoic acid, and oleic acid, which were not detected in phytoplasma-infected or BMSB-infested trees. It was demonstrated that this information can help to identify specific chemical signatures and specific VOCs, which may be used as biomarkers for detecting and monitoring these pests.