Diaphorina citri Induces Huanglongbing-Infected Citrus Plant Volatiles to Repel and Reduce the Performance of Propylaea japonica

Abstract

Transmission of plant pathogens through insect vectors is a complex biological process involving interactions between the host plants, insects, and pathogens. Simultaneous impact of the insect damage and pathogenic bacteria in infected host plants induce volatiles that modify not only the behavior of its insect vector but also of their natural enemies, such as parasitoid wasps. Therefore, it is essential to understand how insects such as the predator ladybird beetle responds to volatiles emitted from a host plant and how the disease transmission alters the interactions between predators, vector, pathogens, and plants. In this study, we investigated the response of Propylaea japonica to volatiles from citrus plants damaged by Diaphorina citri and Candidatus Liberibacter asiaticus through olfactometer bioassays. Synthetic chemical blends were also used to determine the active compounds in the plant volatile. The results showed that volatiles emitted by healthy plants attracted more P. japonica than other treatments, due to the presence of high quantities of D-limonene and beta-ocimene, and the lack of methyl salicylate. When using synthetic chemicals in the olfactory tests, we found that D-limonene attracted P. japonica while methyl salicylate repelled the predator. However, beta-ocimene attracted the insects at lower concentrations but repelled them at higher concentrations. These results indicate that P. japonica could not efficiently search for its host by using volatile cues emitted from psyllids- and Las bacteria-infected citrus plants.

Genomic Analysis of Terpene Synthase Family and Functional Characterization of Seven Sesquiterpene Synthases from Citrus sinensis

“…Linalool/nerolidol synthase gene expression was induced in mandarin leaves by wounding and Xhantomonas citri infection (Shimada et al, 2014 ). Some mono and sesquiterpene compounds have been proposed to be important in the relation of citrus hosts with D. citri , vector of Candidatus Liberibacters (Patt and Sétamou, 2010 ; Coutinho-Abreu et al, 2014 ; Lin et al, 2016 ; dos Santos Andrade et al, 2016 ; Alquézar et al, 2017 ). However, in spite of their importance, just five citrus SesquiTPSs have been characterized up to date (Maruyama et al, 2001 ; Sharon-Asa et al, 2003 ; Shimada et al, 2012 , 2014 ; Uji et al, 2015 ).…”

Thrips as the Transmission Bottleneck for Mixed Infection of Two Orthotospoviruses

“…On the contrary, methyl salicylate, a well-known SA-derived volatile that attracts the aphid predator Coccinella septempunctata [45] and the beneficial insect Chrysopa nigricornis [46], but is repellant to predators of Diaphorina citri [43], was only present in TSWV-infected plants (two out of four TSWV-infected plants).…”

“…Among them, (Z)-3-hexen-1-ol acetate, already shown to attract the parasitic wasp Cotesia glomerata [41], was seen only in mixed-infected plants (two out of four mixed-infected plants), while undecanal (aldehydes) and d-limonene (monoterpenes) were not present in TSWV-infected plants but were present in the other treatments (in three healthy, two mixed-infected, and one INSV-infected plants out of four plants for each treatment; and in three healthy, one mixed-infected, and one INSV-infected plants out of four plants for each treatment). d-Limonene is a known attractant of some insects such as Diaphorina citri (also known as Asian citrus psyllid, the vector of citrus greening) and of their predators [42,43]. Propylaea japonica is more attracted to healthy sour orange (Citrus aurantium) because of the high level of the combination of d-limonene and beta-ocimene, and lack of methyl salicylate emitted by those plants [43].…”

“…d-Limonene is a known attractant of some insects such as Diaphorina citri (also known as Asian citrus psyllid, the vector of citrus greening) and of their predators [42,43]. Propylaea japonica is more attracted to healthy sour orange (Citrus aurantium) because of the high level of the combination of d-limonene and beta-ocimene, and lack of methyl salicylate emitted by those plants [43]. Finally, citrus varieties that are tolerant to Candidatus Liberibacter asiaticus (the causal agent of citrus greening) emitted more aldehydes (undecanal, geranial, citronella, and neral) and monoterpenes including d-limonene [44].…”

Susceptibilities of Candidatus Liberibacter asiaticus‐infected and noninfected Diaphorina citri to entomopathogenic fungi and their detoxification enzyme activities under different temperatures

“…The infection was determined and confirmed using PCR as described by Tatineni et al (2008). Infected and uninfected orange jasmine were used in this rearing of the psyllids, which were also tested by real-time PCR for the presence or absence of Las infection before the bioassays (Lin et al, 2016). Before each experiment, the purity of cultures HLB-free or HLB-infected established colonies was further checked regularly by the random amplified polymorphic DNA polymerase chain reaction (RAPD-PCR) technique and further tested with mtCOI sequencing as described by Tatineni et al (2008) for infection (established colony).…”