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An Indirect Defence Trait Mediated through Egg-Induced Maize Volatiles from Neighbouring Plants

Attack of plants by herbivorous arthropods may result in considerable changes to the plant’s chemical phenotype with respect to emission of herbivore-induced plant volatiles (HIPVs). These HIPVs have been shown to act as repellents to the attacking insects as well as attractants for the insects anta...

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Autores principales: Mutyambai, Daniel M., Bruce, Toby J. A., van den Berg, Johnnie, Midega, Charles A. O., Pickett, John A., Khan, Zeyaur R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4938388/
https://www.ncbi.nlm.nih.gov/pubmed/27392034
http://dx.doi.org/10.1371/journal.pone.0158744
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author Mutyambai, Daniel M.
Bruce, Toby J. A.
van den Berg, Johnnie
Midega, Charles A. O.
Pickett, John A.
Khan, Zeyaur R.
author_facet Mutyambai, Daniel M.
Bruce, Toby J. A.
van den Berg, Johnnie
Midega, Charles A. O.
Pickett, John A.
Khan, Zeyaur R.
author_sort Mutyambai, Daniel M.
collection PubMed
description Attack of plants by herbivorous arthropods may result in considerable changes to the plant’s chemical phenotype with respect to emission of herbivore-induced plant volatiles (HIPVs). These HIPVs have been shown to act as repellents to the attacking insects as well as attractants for the insects antagonistic to these herbivores. Plants can also respond to HIPV signals from other plants that warn them of impending attack. Recent investigations have shown that certain maize varieties are able to emit volatiles following stemborer egg deposition. These volatiles attract the herbivore’s parasitoids and directly deter further oviposition. However, it was not known whether these oviposition-induced maize (Zea mays, L.) volatiles can mediate chemical phenotypic changes in neighbouring unattacked maize plants. Therefore, this study sought to investigate the effect of oviposition-induced maize volatiles on intact neighbouring maize plants in ‘Nyamula’, a landrace known to respond to oviposition, and a standard commercial hybrid, HB515, that did not. Headspace volatile samples were collected from maize plants exposed to Chilo partellus (Swinhoe) (Lepidoptera: Crambidae) egg deposition and unoviposited neighbouring plants as well as from control plants kept away from the volatile emitting ones. Behavioural bioassays were carried out in a four-arm olfactometer using egg (Trichogramma bournieri Pintureau & Babault (Hymenoptera: Trichogrammatidae)) and larval (Cotesia sesamiae Cameron (Hymenoptera: Braconidae)) parasitoids. Coupled Gas Chromatography-Mass Spectrometry (GC-MS) was used for volatile analysis. For the ‘Nyamula’ landrace, GC-MS analysis revealed HIPV production not only in the oviposited plants but also in neighbouring plants not exposed to insect eggs. Higher amounts of EAG-active biogenic volatiles such as (E)-4,8-dimethyl-1,3,7-nonatriene were emitted from these plants compared to control plants. Subsequent behavioural assays with female T. bournieri and C. sesamiae parasitic wasps indicated that these parasitoids preferred volatiles from oviposited and neighbouring landrace plants compared to those from the control plants. This effect was absent in the standard commercial hybrid we tested. There was no HIPV induction and no difference in parasitoid attraction in neighbouring and control hybrid maize plants. These results show plant-plant signalling: ‘Nyamula’ maize plants emitting oviposition-induced volatiles attractive to the herbivore’s natural enemies can induce this indirect defence trait in conspecific neighbouring undamaged maize plants. Maize plants growing in a field may thus benefit from this indirect defence through airborne signalling which may enhance the fitness of the volatile-emitting plant by increasing predation pressure on herbivores.
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spelling pubmed-49383882016-07-22 An Indirect Defence Trait Mediated through Egg-Induced Maize Volatiles from Neighbouring Plants Mutyambai, Daniel M. Bruce, Toby J. A. van den Berg, Johnnie Midega, Charles A. O. Pickett, John A. Khan, Zeyaur R. PLoS One Research Article Attack of plants by herbivorous arthropods may result in considerable changes to the plant’s chemical phenotype with respect to emission of herbivore-induced plant volatiles (HIPVs). These HIPVs have been shown to act as repellents to the attacking insects as well as attractants for the insects antagonistic to these herbivores. Plants can also respond to HIPV signals from other plants that warn them of impending attack. Recent investigations have shown that certain maize varieties are able to emit volatiles following stemborer egg deposition. These volatiles attract the herbivore’s parasitoids and directly deter further oviposition. However, it was not known whether these oviposition-induced maize (Zea mays, L.) volatiles can mediate chemical phenotypic changes in neighbouring unattacked maize plants. Therefore, this study sought to investigate the effect of oviposition-induced maize volatiles on intact neighbouring maize plants in ‘Nyamula’, a landrace known to respond to oviposition, and a standard commercial hybrid, HB515, that did not. Headspace volatile samples were collected from maize plants exposed to Chilo partellus (Swinhoe) (Lepidoptera: Crambidae) egg deposition and unoviposited neighbouring plants as well as from control plants kept away from the volatile emitting ones. Behavioural bioassays were carried out in a four-arm olfactometer using egg (Trichogramma bournieri Pintureau & Babault (Hymenoptera: Trichogrammatidae)) and larval (Cotesia sesamiae Cameron (Hymenoptera: Braconidae)) parasitoids. Coupled Gas Chromatography-Mass Spectrometry (GC-MS) was used for volatile analysis. For the ‘Nyamula’ landrace, GC-MS analysis revealed HIPV production not only in the oviposited plants but also in neighbouring plants not exposed to insect eggs. Higher amounts of EAG-active biogenic volatiles such as (E)-4,8-dimethyl-1,3,7-nonatriene were emitted from these plants compared to control plants. Subsequent behavioural assays with female T. bournieri and C. sesamiae parasitic wasps indicated that these parasitoids preferred volatiles from oviposited and neighbouring landrace plants compared to those from the control plants. This effect was absent in the standard commercial hybrid we tested. There was no HIPV induction and no difference in parasitoid attraction in neighbouring and control hybrid maize plants. These results show plant-plant signalling: ‘Nyamula’ maize plants emitting oviposition-induced volatiles attractive to the herbivore’s natural enemies can induce this indirect defence trait in conspecific neighbouring undamaged maize plants. Maize plants growing in a field may thus benefit from this indirect defence through airborne signalling which may enhance the fitness of the volatile-emitting plant by increasing predation pressure on herbivores. Public Library of Science 2016-07-08 /pmc/articles/PMC4938388/ /pubmed/27392034 http://dx.doi.org/10.1371/journal.pone.0158744 Text en © 2016 Mutyambai et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Mutyambai, Daniel M.
Bruce, Toby J. A.
van den Berg, Johnnie
Midega, Charles A. O.
Pickett, John A.
Khan, Zeyaur R.
An Indirect Defence Trait Mediated through Egg-Induced Maize Volatiles from Neighbouring Plants
title An Indirect Defence Trait Mediated through Egg-Induced Maize Volatiles from Neighbouring Plants
title_full An Indirect Defence Trait Mediated through Egg-Induced Maize Volatiles from Neighbouring Plants
title_fullStr An Indirect Defence Trait Mediated through Egg-Induced Maize Volatiles from Neighbouring Plants
title_full_unstemmed An Indirect Defence Trait Mediated through Egg-Induced Maize Volatiles from Neighbouring Plants
title_short An Indirect Defence Trait Mediated through Egg-Induced Maize Volatiles from Neighbouring Plants
title_sort indirect defence trait mediated through egg-induced maize volatiles from neighbouring plants
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4938388/
https://www.ncbi.nlm.nih.gov/pubmed/27392034
http://dx.doi.org/10.1371/journal.pone.0158744
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