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

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

Research output: Contribution to journalArticle

68 Citations (Scopus)

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.

Original languageEnglish (US)
Article numbere38146
JournalPloS one
Volume7
Issue number6
DOIs
StatePublished - Jun 27 2012

Fingerprint

Herbivory
Citrus
entomopathogenic nematodes
Ecosystem
biological control
herbivores
Nematoda
Mortality
Diaprepes abbreviatus
pests
habitats
Orchards
Larva
Biological Pest Control
natural enemies
Blueberry Plants
Weevils
Pachnaeus litus
rhizosphere
Anomala orientalis

All Science Journal Classification (ASJC) codes

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)
  • General

Cite this

Ali, Jared G. ; Alborn, Hans T. ; Campos-Herrera, Raquel ; Kaplan, Fatma ; Duncan, Larry W. ; Rodriguez-Saona, Cesar ; Koppenhöfer, Albrecht M. ; Stelinski, Lukasz L. / Subterranean, herbivore-induced plant volatile increases biological control activity of multiple beneficial nematode species in distinct habitats. In: PloS one. 2012 ; Vol. 7, No. 6.
@article{20640af15c9641568a21c92f1ebc41dd,
title = "Subterranean, herbivore-induced plant volatile increases biological control activity of multiple beneficial nematode species in distinct habitats",
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.",
author = "Ali, {Jared G.} and Alborn, {Hans T.} and Raquel Campos-Herrera and Fatma Kaplan and Duncan, {Larry W.} and Cesar Rodriguez-Saona and Koppenh{\"o}fer, {Albrecht M.} and Stelinski, {Lukasz L.}",
year = "2012",
month = "6",
day = "27",
doi = "10.1371/journal.pone.0038146",
language = "English (US)",
volume = "7",
journal = "PLoS One",
issn = "1932-6203",
publisher = "Public Library of Science",
number = "6",

}

Subterranean, herbivore-induced plant volatile increases biological control activity of multiple beneficial nematode species in distinct habitats. / Ali, Jared G.; Alborn, Hans T.; Campos-Herrera, Raquel; Kaplan, Fatma; Duncan, Larry W.; Rodriguez-Saona, Cesar; Koppenhöfer, Albrecht M.; Stelinski, Lukasz L.

In: PloS one, Vol. 7, No. 6, e38146, 27.06.2012.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Subterranean, herbivore-induced plant volatile increases biological control activity of multiple beneficial nematode species in distinct habitats

AU - Ali, Jared G.

AU - Alborn, Hans T.

AU - Campos-Herrera, Raquel

AU - Kaplan, Fatma

AU - Duncan, Larry W.

AU - Rodriguez-Saona, Cesar

AU - Koppenhöfer, Albrecht M.

AU - Stelinski, Lukasz L.

PY - 2012/6/27

Y1 - 2012/6/27

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=84863002872&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84863002872&partnerID=8YFLogxK

U2 - 10.1371/journal.pone.0038146

DO - 10.1371/journal.pone.0038146

M3 - Article

C2 - 22761668

AN - SCOPUS:84863002872

VL - 7

JO - PLoS One

JF - PLoS One

SN - 1932-6203

IS - 6

M1 - e38146

ER -