Volatile Signals From Guava Plants Prime Defense Signaling and Increase Jasmonate-Dependent Herbivore Resistance in Neighboring Citrus Plants

Intercropping can reduce agricultural pest incidence and represents an important sustainable alternative to conventional pest control methods. Citrus intercropped with guava (Psidium guajava L.) has a lower incidence of Asian citrus psyllid (ACP, Diaphorina citri Kuwayama) and huanglongbing disease (HLB), but the mechanisms are still unknown. In this study, we tested whether volatile organic compounds (VOCs) emitted by guava plants play a role in plant–plant communications and trigger defense responses in sweet orange (Citrus sinensis L. Osbeck) in the laboratory. The results showed that the behavioral preference and developmental performance of ACP on citrus plants that were exposed to guava VOCs were suppressed. The expression of defense-related pathways involved in early signaling, jasmonate (JA) biosynthesis, protease inhibitor (PI), terpenoid, phenylpropanoid, and flavonoid biosynthesis was induced in guava VOC-exposed citrus plants. Headspace analysis revealed that guava plants constitutively emit high levels of (E)-β-caryophyllene and (E)-4,8-dimethyl-1,3,7-nonatriene (DMNT), which can induce the accumulation of JA and promote stronger defense responses of citrus to ACP feeding. In addition, exposure to guava VOCs also increased the indirect defense of citrus by attracting the parasitic wasp Tamarixia radiata. Together, our findings indicate that citrus plants can eavesdrop on the VOC cues emitted by neighboring intact guava plants to boost their JA-dependent anti-herbivore activities. The knowledge gained from this study will provide mechanisms underlying citrus-guava intercropping for the ecological management of insect pests.