Subterranean, herbivore-induced plant volatile increases biological control activity of multiple beneficial nematode species in distinct habitats.

Jared G Ali,Hans T Alborn,Albrecht M Koppenhöfer,Lukasz L Stelinski,Fatma Kaplan,Raquel Campos-Herrera,Cesar Rodriguez-Saona,Larry W Duncan,Martin Heil

doi:10.1371/journal.pone.0038146

Abstract

While the role of herbivore-induced volatiles in plant-herbivore-natural enemy interactions is well documented aboveground, new evidence suggests that belowground volatile emissions can protect plants by attracting entomopathogenic nematodes (EPNs). However, due to methodological limitations, no study has previously detected belowground herbivore-induced volatiles in the field or quantified their impact on attraction of diverse EPN species. Here we show how a belowground herbivore-induced volatile can enhance mortality of agriculturally significant root pests. First, in real time, we identified pregeijerene (1,5-dimethylcyclodeca-1,5,7-triene) from citrus roots 9–12 hours after initiation of larval Diaprepes abbreviatus feeding. This compound was also detected in the root zone of mature citrus trees in the field. Application of collected volatiles from weevil-damaged citrus roots attracted native EPNs and increased mortality of beetle larvae (D. abbreviatus) compared to controls in a citrus orchard. In addition, field applications of isolated pregeijerene caused similar results. Quantitative real-time PCR revealed that pregeijerene increased pest mortality by attracting four species of naturally occurring EPNs in the field. Finally, we tested the generality of this root-zone signal by application of pregeijerene in blueberry fields; mortality of larvae (Galleria mellonella and Anomala orientalis) again increased by attracting naturally occurring populations of an EPN. Thus, this specific belowground signal attracts natural enemies of widespread root pests in distinct agricultural systems and may have broad potential in biological control of root pests.

Highlights

Natural enemies of herbivorous pests use flexible foraging strategies that often incorporate environmental cues emitted by the herbivore’s host plant
Nematode Attraction in the Field using herbivore-induced plant volatiles (HIPVs) We conducted field tests to determine whether application of volatiles collected from infested roots would impact EPNinflicted mortality of sentinel D. abbreviatus larvae
Available entomopathogenic nematodes (EPNs) had been applied to the test orchard at numerous occasions; their persistence was not monitored

Summary

Introduction

Natural enemies of herbivorous pests use flexible foraging strategies that often incorporate environmental cues emitted by the herbivore’s host plant. To date, only one root-induced attractant has been described and shown to enhance the effectiveness of EPNs in the field: (E)-bcaryophyllene from the roots of maize (Zea Mays L.) [11,13]. No previous studies have detected a belowground herbivore-induced volatile from intact plants in the field or measured the effectiveness of belowground attractants for recruiting populations of naturally occurring EPNs in the soil. Depending on the specificity of interactions, the identification and manipulation of a root signal in the field could well enhance biological control of diverse root pests in agroecosystems

Methods

Results

Conclusion