Electroantennogram and machine learning reveal a volatile blend mediating avoidance behavior by Tuta absoluta females to a wild tomato plant

Abstract Tomato cultivation is threatened by the infestation of the nocturnal invasive tomato pinworm, Tuta absoluta. This study was based on field observations that a wild tomato plant, Solanum lycopersicum var. cerasiforme, grown in the Mount Kenya region, Kenya, is less attacked by T. absoluta, u...

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Main Authors: Raphael Njurai Miano, Pascal Mahukpe Ayelo, Richard Musau, Ahmed Hassanali, Samira A. Mohamed
Format: Article
Language:English
Published: Nature Portfolio 2022-05-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-022-13125-0
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author Raphael Njurai Miano
Pascal Mahukpe Ayelo
Richard Musau
Ahmed Hassanali
Samira A. Mohamed
author_facet Raphael Njurai Miano
Pascal Mahukpe Ayelo
Richard Musau
Ahmed Hassanali
Samira A. Mohamed
author_sort Raphael Njurai Miano
collection DOAJ
description Abstract Tomato cultivation is threatened by the infestation of the nocturnal invasive tomato pinworm, Tuta absoluta. This study was based on field observations that a wild tomato plant, Solanum lycopersicum var. cerasiforme, grown in the Mount Kenya region, Kenya, is less attacked by T. absoluta, unlike the cultivated tomato plants like S. lycopersicum (var. Rambo F1). We hypothesized that the wild tomato plant may be actively avoided by gravid T. absoluta females because of the emission of repellent allelochemical constituents. Therefore, we compared infestation levels by the pest in field monocrops and intercrops of the two tomato genotypes, characterized the headspace volatiles, then determined the compounds detectable by the insect through gas chromatography-linked electroantennography (GC-EAG), and finally performed bioassays using a blend of four EAG-active compounds unique to the wild tomato. We found significant reductions in infestation levels in the monocrop of the wild tomato, and intercrops of wild and cultivated tomato plants compared to the monocrop of the cultivated tomato plant. Quantitative and qualitative differences were noted between volatiles of the wild and cultivated tomato plants, and between day and night volatile collections. The most discriminating compounds between the volatile treatments varied with the variable selection or machine learning methods used. In GC-EAG recordings, 16 compounds including hexanal, (Z)-3-hexenol, α-pinene, β-myrcene, α-phellandrene, β-phellandrene, (E)-β-ocimene, terpinolene, limonene oxide, camphor, citronellal, methyl salicylate, (E)-β-caryophyllene, and others tentatively identified as 3,7,7-Trimethyl-1,3,5-cycloheptatriene, germacrene D and cis-carvenone oxide were detected by antennae of T. absoluta females. Among these EAG-active compounds, (Z)-3-hexenol, α-pinene, α-phellandrene, limonene oxide, camphor, citronellal, (E)-β-caryophyllene and β-phellandrene are in the top 5 discriminating compounds highlighted by the machine learning methods. A blend of (Z)-3-hexenol, camphor, citronellal and limonene oxide detected only in the wild tomato showed dose-dependent repellence to T. absoluta females in wind tunnel. This study provides some groundwork for exploiting the allelochemicals of the wild tomato in the development of novel integrated pest management approaches against T. absoluta.
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spelling doaj.art-e23b8211c73f424f8ae0babfa247ba622022-12-22T02:21:49ZengNature PortfolioScientific Reports2045-23222022-05-0112111610.1038/s41598-022-13125-0Electroantennogram and machine learning reveal a volatile blend mediating avoidance behavior by Tuta absoluta females to a wild tomato plantRaphael Njurai Miano0Pascal Mahukpe Ayelo1Richard Musau2Ahmed Hassanali3Samira A. Mohamed4International Centre of Insect Physiology and Ecology (icipe)International Centre of Insect Physiology and Ecology (icipe)Department of Chemistry, Kenyatta UniversityDepartment of Chemistry, Kenyatta UniversityInternational Centre of Insect Physiology and Ecology (icipe)Abstract Tomato cultivation is threatened by the infestation of the nocturnal invasive tomato pinworm, Tuta absoluta. This study was based on field observations that a wild tomato plant, Solanum lycopersicum var. cerasiforme, grown in the Mount Kenya region, Kenya, is less attacked by T. absoluta, unlike the cultivated tomato plants like S. lycopersicum (var. Rambo F1). We hypothesized that the wild tomato plant may be actively avoided by gravid T. absoluta females because of the emission of repellent allelochemical constituents. Therefore, we compared infestation levels by the pest in field monocrops and intercrops of the two tomato genotypes, characterized the headspace volatiles, then determined the compounds detectable by the insect through gas chromatography-linked electroantennography (GC-EAG), and finally performed bioassays using a blend of four EAG-active compounds unique to the wild tomato. We found significant reductions in infestation levels in the monocrop of the wild tomato, and intercrops of wild and cultivated tomato plants compared to the monocrop of the cultivated tomato plant. Quantitative and qualitative differences were noted between volatiles of the wild and cultivated tomato plants, and between day and night volatile collections. The most discriminating compounds between the volatile treatments varied with the variable selection or machine learning methods used. In GC-EAG recordings, 16 compounds including hexanal, (Z)-3-hexenol, α-pinene, β-myrcene, α-phellandrene, β-phellandrene, (E)-β-ocimene, terpinolene, limonene oxide, camphor, citronellal, methyl salicylate, (E)-β-caryophyllene, and others tentatively identified as 3,7,7-Trimethyl-1,3,5-cycloheptatriene, germacrene D and cis-carvenone oxide were detected by antennae of T. absoluta females. Among these EAG-active compounds, (Z)-3-hexenol, α-pinene, α-phellandrene, limonene oxide, camphor, citronellal, (E)-β-caryophyllene and β-phellandrene are in the top 5 discriminating compounds highlighted by the machine learning methods. A blend of (Z)-3-hexenol, camphor, citronellal and limonene oxide detected only in the wild tomato showed dose-dependent repellence to T. absoluta females in wind tunnel. This study provides some groundwork for exploiting the allelochemicals of the wild tomato in the development of novel integrated pest management approaches against T. absoluta.https://doi.org/10.1038/s41598-022-13125-0
spellingShingle Raphael Njurai Miano
Pascal Mahukpe Ayelo
Richard Musau
Ahmed Hassanali
Samira A. Mohamed
Electroantennogram and machine learning reveal a volatile blend mediating avoidance behavior by Tuta absoluta females to a wild tomato plant
Scientific Reports
title Electroantennogram and machine learning reveal a volatile blend mediating avoidance behavior by Tuta absoluta females to a wild tomato plant
title_full Electroantennogram and machine learning reveal a volatile blend mediating avoidance behavior by Tuta absoluta females to a wild tomato plant
title_fullStr Electroantennogram and machine learning reveal a volatile blend mediating avoidance behavior by Tuta absoluta females to a wild tomato plant
title_full_unstemmed Electroantennogram and machine learning reveal a volatile blend mediating avoidance behavior by Tuta absoluta females to a wild tomato plant
title_short Electroantennogram and machine learning reveal a volatile blend mediating avoidance behavior by Tuta absoluta females to a wild tomato plant
title_sort electroantennogram and machine learning reveal a volatile blend mediating avoidance behavior by tuta absoluta females to a wild tomato plant
url https://doi.org/10.1038/s41598-022-13125-0
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