Subterranean Herbivore-induced Volatiles Released by Citrus Roots upon Feeding by Diaprepes abbreviatus Recruit Entomopathogenic Nematodes

Abstract

Herbivore-induced volatile emissions benefit plant hosts by recruiting natural enemies of herbivorous insects. Such tritrophic interactions have been examined thoroughly in the above-ground terrestrial environment. Recently, similar signals have also been described in the subterranean environment, which may be of equal importance for indirect plant defense. The larvae of the root weevil, Diaprepes abbreviates, are a serious pest of citrus. Infestations can be controlled by the use of entomopathogenic nematodes, yet the interactions between the plant, insect and nematode are poorly understood and remain unpredictable. In bioassays that used a root zone six-arm olfactometer, citrus roots ('Swingle citrumelo' rootstock) recruited significantly more entomopathogenic nematodes (Steinernema diaprepesi) when infested with root weevil larvae than non-infested roots. Infested plants were more attractive to nematodes than larvae alone. Roots damaged by weevil larvae attracted more nematodes than mechanically damaged roots and sand controls. By dynamic in situ collection and GC-MS analysis of volatiles from soil, we determined that four major terpene compounds were produced by infested plant roots that were not found in samples from non-infested roots or soil that contained only larvae. Solvent extracts of weevil-infested roots attracted more nematodes than extracts of non-infested roots in a two choice sand-column bioassay. These findings suggest that Swingle citrus roots release induced volatiles as an indirect defense in response to herbivore feeding, and that some of these induced volatiles function as attractants for entomopathogenic nematodes.

The Role of Root-Produced Volatile Secondary Metabolites in Mediating Soil Interactions

“…To date, few additional tritrophic interactions implying belowground VOCs signaling have been described both in agricultural systems Stelinski 2010, 2011;Rasmann et al 2005) and in wild environment (Rasmann et al 2011). Ali, Alborn, andStelinski (2010) have demonstrated that citrus roots upon feeding by the root weevil Diaprepes abbreviates emit several terpenes in the surrounding soil. Using belowground olfactometers Ali et al (2010) could show that the entomopathogenic nematode Steinernema diaprepesi was significantly more attracted by citrus roots induced by the insect pest larvae than by roots mechanically damaged or by control empty pots.…”

“…Ali, Alborn, andStelinski (2010) have demonstrated that citrus roots upon feeding by the root weevil Diaprepes abbreviates emit several terpenes in the surrounding soil. Using belowground olfactometers Ali et al (2010) could show that the entomopathogenic nematode Steinernema diaprepesi was significantly more attracted by citrus roots induced by the insect pest larvae than by roots mechanically damaged or by control empty pots. However, Ali et al (2011) recently pointed out that insect induced roots of citrus tree could also attract the phytopathogenic nematode Tylenchulus semipenetrans (see above section).…”

Host-seeking behavior of the Heterorhabditis amazonensis nematode in response to stimulant sources1

“…Van Tol et al (2001) reported that the nematode Heterorhabditis megidis Poinar, Jackson and Klein 1987 (Rhabditida: Heterorhabditidae) was attracted considerably more strongly to exudates released from roots of the Thuja occidentalis L. conifer when it was attacked by larvae of the Otiorhynchus sulcatus (Fabricius, 1775) (Coleoptera: Curculionidae) beetle. Ali et al (2010 and demonstrated that multiple species of entomopathogenic nematodes are highly attracted to the roots of citrus plants damaged by the feeding of Diaprepes abbreviatus (Linnaeus) (Coleoptera: Curculionidae) larvae. Roots infested and damaged by insects were more attractive to nematodes than those that were mechanically damaged or by the larvae alone.…”

Selective breeding of entomopathogenic nematodes for enhanced attraction to a root signal did not reduce their establishment or persistence after field release

“…9 Root-produced volatiles appear to play an important role in the recruitment of EPN [10][11][12][13] and one such volatile, (E)-β-caryophyllene (EβC), has recently been identified for maize roots 14 and was found to be an ideal belowground alarm signal. 15 EPN efficacy can be improved by exploiting the ability of WCR-damaged maize roots to emit the attractant.…”