Dynamic changes in virus-induced volatiles in cotton modulate the orientation and oviposition behavior of the whitefly Bemisia tabaci

Manipulation of insect vector behavior by virus-induced plant volatiles is well known. But how the viral disease progression alters the plant volatiles and its effect on vector behavior remains less explored. Our studies tracked changes in volatile profile in progressive infection stages of cotton l...

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Main Authors: Suresh M. Nebapure, Karuppan Shankarganesh, Salim Rajna, Kailash Chandra Naga, Dheerendra Pandey, Shubham Gambhir, Koovalamkadu Velayudhan Praveen, Sabtharishi Subramanian
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-10-01
Series:Frontiers in Physiology
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Online Access:https://www.frontiersin.org/articles/10.3389/fphys.2022.1017948/full
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author Suresh M. Nebapure
Karuppan Shankarganesh
Karuppan Shankarganesh
Salim Rajna
Kailash Chandra Naga
Dheerendra Pandey
Shubham Gambhir
Koovalamkadu Velayudhan Praveen
Sabtharishi Subramanian
author_facet Suresh M. Nebapure
Karuppan Shankarganesh
Karuppan Shankarganesh
Salim Rajna
Kailash Chandra Naga
Dheerendra Pandey
Shubham Gambhir
Koovalamkadu Velayudhan Praveen
Sabtharishi Subramanian
author_sort Suresh M. Nebapure
collection DOAJ
description Manipulation of insect vector behavior by virus-induced plant volatiles is well known. But how the viral disease progression alters the plant volatiles and its effect on vector behavior remains less explored. Our studies tracked changes in volatile profile in progressive infection stages of cotton leaf curl virus (CLCuV) infected plants and their effect on B. tabaci behavior. Significant differences in virus titers were noticed between progressive infection stages showing distinct symptoms. Whiteflies initially settled on CLCuV infected plants, but their preference was shifted to healthy plants over time. GC-MS analysis revealed subtle quantitative/qualitative changes in volatile organic compounds (VOCs) between the healthy and selected CLCuV infection stages. VOCs such as hexanal, (E)-2-hexen-1-ol, (+)-α-pinene, (−)-β-pinene, (Z)-3-hexen-1-ol, (+)-sylvestrene, and (1S,2E,6E, 10R)-3,7,11,11-tetramethylbicycloundeca-2,6-diene (Bicyclogermacrene) were associated with the infection stage showing upward curling of leaves; (E)-2-hexen-1-ol, β-myrcene, β-ocimene, and copaene were associated with the infection stage showing downward curling. Validation studies with eight synthetic VOCs indicated that γ-terpinene elicited attraction to B. tabaci (Olfactometric Preference Index (OPI) = 1.65), while β-ocimene exhibited strong repellence (OPI = 0.64) and oviposition reduction (66.01%–92.55%). Our studies have demonstrated that progression of CLCuV disease in cotton was associated with dynamic changes in volatile profile which influences the behavioural responses of whitefly, B.tabaci. Results have shown that VOCs such as (+)-α-pinene, (−)-β-pinene γ-Terpinene, α-guaiene; 4- hydroxy- 4 methyl-2- pentanone and β-ocimene emitted from Begomovirus infected plants could be the driving force for early attraction and later repellence/oviposition deterrence of B. tabaci on virus-infected plants. The findings of this study offer scope for the management of whitefly, B. tabaci through semiochemicals.
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spelling doaj.art-078604e39c0d4d31a10d5e4484ab28002022-12-22T04:13:03ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2022-10-011310.3389/fphys.2022.10179481017948Dynamic changes in virus-induced volatiles in cotton modulate the orientation and oviposition behavior of the whitefly Bemisia tabaciSuresh M. Nebapure0Karuppan Shankarganesh1Karuppan Shankarganesh2Salim Rajna3Kailash Chandra Naga4Dheerendra Pandey5Shubham Gambhir6Koovalamkadu Velayudhan Praveen7Sabtharishi Subramanian8ICAR-Indian Agricultural Research Institute, New Delhi, IndiaICAR-Indian Agricultural Research Institute, New Delhi, IndiaICAR-Central Institute for Cotton Research, Regional Station, Coimbatore, IndiaICAR-Indian Agricultural Research Institute, New Delhi, IndiaICAR-Central Potato Research Institute, Shimla, IndiaICAR-Indian Agricultural Research Institute, New Delhi, IndiaICAR-Indian Agricultural Research Institute, New Delhi, IndiaICAR-Indian Agricultural Research Institute, New Delhi, IndiaICAR-Indian Agricultural Research Institute, New Delhi, IndiaManipulation of insect vector behavior by virus-induced plant volatiles is well known. But how the viral disease progression alters the plant volatiles and its effect on vector behavior remains less explored. Our studies tracked changes in volatile profile in progressive infection stages of cotton leaf curl virus (CLCuV) infected plants and their effect on B. tabaci behavior. Significant differences in virus titers were noticed between progressive infection stages showing distinct symptoms. Whiteflies initially settled on CLCuV infected plants, but their preference was shifted to healthy plants over time. GC-MS analysis revealed subtle quantitative/qualitative changes in volatile organic compounds (VOCs) between the healthy and selected CLCuV infection stages. VOCs such as hexanal, (E)-2-hexen-1-ol, (+)-α-pinene, (−)-β-pinene, (Z)-3-hexen-1-ol, (+)-sylvestrene, and (1S,2E,6E, 10R)-3,7,11,11-tetramethylbicycloundeca-2,6-diene (Bicyclogermacrene) were associated with the infection stage showing upward curling of leaves; (E)-2-hexen-1-ol, β-myrcene, β-ocimene, and copaene were associated with the infection stage showing downward curling. Validation studies with eight synthetic VOCs indicated that γ-terpinene elicited attraction to B. tabaci (Olfactometric Preference Index (OPI) = 1.65), while β-ocimene exhibited strong repellence (OPI = 0.64) and oviposition reduction (66.01%–92.55%). Our studies have demonstrated that progression of CLCuV disease in cotton was associated with dynamic changes in volatile profile which influences the behavioural responses of whitefly, B.tabaci. Results have shown that VOCs such as (+)-α-pinene, (−)-β-pinene γ-Terpinene, α-guaiene; 4- hydroxy- 4 methyl-2- pentanone and β-ocimene emitted from Begomovirus infected plants could be the driving force for early attraction and later repellence/oviposition deterrence of B. tabaci on virus-infected plants. The findings of this study offer scope for the management of whitefly, B. tabaci through semiochemicals.https://www.frontiersin.org/articles/10.3389/fphys.2022.1017948/fullwhiteflycotton leaf curl virusinteractionsvolatile organic compoundsovipositionorientation
spellingShingle Suresh M. Nebapure
Karuppan Shankarganesh
Karuppan Shankarganesh
Salim Rajna
Kailash Chandra Naga
Dheerendra Pandey
Shubham Gambhir
Koovalamkadu Velayudhan Praveen
Sabtharishi Subramanian
Dynamic changes in virus-induced volatiles in cotton modulate the orientation and oviposition behavior of the whitefly Bemisia tabaci
Frontiers in Physiology
whitefly
cotton leaf curl virus
interactions
volatile organic compounds
oviposition
orientation
title Dynamic changes in virus-induced volatiles in cotton modulate the orientation and oviposition behavior of the whitefly Bemisia tabaci
title_full Dynamic changes in virus-induced volatiles in cotton modulate the orientation and oviposition behavior of the whitefly Bemisia tabaci
title_fullStr Dynamic changes in virus-induced volatiles in cotton modulate the orientation and oviposition behavior of the whitefly Bemisia tabaci
title_full_unstemmed Dynamic changes in virus-induced volatiles in cotton modulate the orientation and oviposition behavior of the whitefly Bemisia tabaci
title_short Dynamic changes in virus-induced volatiles in cotton modulate the orientation and oviposition behavior of the whitefly Bemisia tabaci
title_sort dynamic changes in virus induced volatiles in cotton modulate the orientation and oviposition behavior of the whitefly bemisia tabaci
topic whitefly
cotton leaf curl virus
interactions
volatile organic compounds
oviposition
orientation
url https://www.frontiersin.org/articles/10.3389/fphys.2022.1017948/full
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