Silencing the alarm an insect salivary enzyme closes plant stomata and inhibits volatile release

• Herbivore-induced plant volatiles (HIPVs) are widely recognized as an ecologically important defensive response of plants against herbivory. Although the induction of this ‘cry for help’ has been well documented, only a few studies have investigated the inhibition of HIPVs by herbivores and little...

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Published inThe New phytologist Vol. 230; no. 2; pp. 793 - 803
Main Authors Lin, Po-An, Chen, Yintong, Chaverra-Rodriguez, Duverney, Heu, Chan Chin, Zainuddin, Nursyafiqi Bin, Sidhu, Jagdeep Singh, Peiffer, Michelle, Tan, Ching-Wen, Helms, Anjel, Kim, Donghun, Ali, Jared, Rasgon, Jason L., Lynch, Jonathan, Anderson, Charles T., Felton, Gary W.
Format Journal Article
LanguageEnglish
Published England Wiley 01.04.2021
Wiley Subscription Services, Inc
John Wiley and Sons Inc
Subjects
Acetates
Acetic acid
Allelochemicals
Animals
CRISPR
CRISPR-Cas systems
Defensive behavior
Dynamics
effector
Emission
Emissions
Enzymes
Gene editing
Glucose oxidase
Glycine (amino acid)
Glycine max
Helicoverpa zea
Herbivores
Herbivory
HIPV
insect herbivore
Insecta
Insects
Moths
phytophagous insects
plant defense
Plant Stomata
Solanum lycopersicum
Soybeans
Stomata
stomatal movement
Tomatoes
Volatile compounds
Volatile Organic Compounds
Volatiles
stomata
effector
plant defense
insect herbivore
HIPV
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Abstract • Herbivore-induced plant volatiles (HIPVs) are widely recognized as an ecologically important defensive response of plants against herbivory. Although the induction of this ‘cry for help’ has been well documented, only a few studies have investigated the inhibition of HIPVs by herbivores and little is known about whether herbivores have evolved mechanisms to inhibit the release of HIPVs. • To examine the role of herbivore effectors in modulating HIPVs and stomatal dynamics, we conducted series of experiments combining pharmacological, surgical, genetic (CRISPR-Cas9) and chemical (GC-MS analysis) approaches. • We show that the salivary enzyme, glucose oxidase (GOX), secreted by the caterpillar Helicoverpa zea on leaves, causes stomatal closure in tomato (Solanum lycopersicum) within 5 min, and in both tomato and soybean (Glycine max) for at least 48 h. GOX also inhibits the emission of several HIPVs during feeding by H. zea, including (Z)-3-hexenol, (Z)-jasmone and (Z)-3-hexenyl acetate, which are important airborne signals in plant defenses. • Our findings highlight a potential adaptive strategy where an insect herbivore inhibits plant airborne defenses during feeding by exploiting the association between stomatal dynamics and HIPV emission.
AbstractList Herbivore‐induced plant volatiles (HIPVs) are widely recognized as an ecologically important defensive response of plants against herbivory. Although the induction of this ‘cry for help’ has been well documented, only a few studies have investigated the inhibition of HIPVs by herbivores and little is known about whether herbivores have evolved mechanisms to inhibit the release of HIPVs. To examine the role of herbivore effectors in modulating HIPVs and stomatal dynamics, we conducted series of experiments combining pharmacological, surgical, genetic (CRISPR‐Cas9) and chemical (GC‐MS analysis) approaches. We show that the salivary enzyme, glucose oxidase (GOX), secreted by the caterpillar Helicoverpa zea on leaves, causes stomatal closure in tomato ( Solanum lycopersicum ) within 5 min, and in both tomato and soybean ( Glycine max ) for at least 48 h. GOX also inhibits the emission of several HIPVs during feeding by H. zea , including ( Z )‐3‐hexenol, ( Z )‐jasmone and ( Z )‐3‐hexenyl acetate, which are important airborne signals in plant defenses. Our findings highlight a potential adaptive strategy where an insect herbivore inhibits plant airborne defenses during feeding by exploiting the association between stomatal dynamics and HIPV emission.
Herbivore‐induced plant volatiles (HIPVs) are widely recognized as an ecologically important defensive response of plants against herbivory. Although the induction of this ‘cry for help’ has been well documented, only a few studies have investigated the inhibition of HIPVs by herbivores and little is known about whether herbivores have evolved mechanisms to inhibit the release of HIPVs. To examine the role of herbivore effectors in modulating HIPVs and stomatal dynamics, we conducted series of experiments combining pharmacological, surgical, genetic (CRISPR‐Cas9) and chemical (GC‐MS analysis) approaches. We show that the salivary enzyme, glucose oxidase (GOX), secreted by the caterpillar Helicoverpa zea on leaves, causes stomatal closure in tomato (Solanum lycopersicum) within 5 min, and in both tomato and soybean (Glycine max) for at least 48 h. GOX also inhibits the emission of several HIPVs during feeding by H. zea, including (Z)‐3‐hexenol, (Z)‐jasmone and (Z)‐3‐hexenyl acetate, which are important airborne signals in plant defenses. Our findings highlight a potential adaptive strategy where an insect herbivore inhibits plant airborne defenses during feeding by exploiting the association between stomatal dynamics and HIPV emission.
Summary Herbivore‐induced plant volatiles (HIPVs) are widely recognized as an ecologically important defensive response of plants against herbivory. Although the induction of this ‘cry for help’ has been well documented, only a few studies have investigated the inhibition of HIPVs by herbivores and little is known about whether herbivores have evolved mechanisms to inhibit the release of HIPVs. To examine the role of herbivore effectors in modulating HIPVs and stomatal dynamics, we conducted series of experiments combining pharmacological, surgical, genetic (CRISPR‐Cas9) and chemical (GC‐MS analysis) approaches. We show that the salivary enzyme, glucose oxidase (GOX), secreted by the caterpillar Helicoverpa zea on leaves, causes stomatal closure in tomato (Solanum lycopersicum) within 5 min, and in both tomato and soybean (Glycine max) for at least 48 h. GOX also inhibits the emission of several HIPVs during feeding by H. zea, including (Z)‐3‐hexenol, (Z)‐jasmone and (Z)‐3‐hexenyl acetate, which are important airborne signals in plant defenses. Our findings highlight a potential adaptive strategy where an insect herbivore inhibits plant airborne defenses during feeding by exploiting the association between stomatal dynamics and HIPV emission.
Herbivore-induced plant volatiles (HIPVs) are widely recognized as an ecologically important defensive response of plants against herbivory. Although the induction of this 'cry for help' has been well documented, only a few studies have investigated the inhibition of HIPVs by herbivores and little is known about whether herbivores have evolved mechanisms to inhibit the release of HIPVs. To examine the role of herbivore effectors in modulating HIPVs and stomatal dynamics, we conducted series of experiments combining pharmacological, surgical, genetic (CRISPR-Cas9) and chemical (GC-MS analysis) approaches. We show that the salivary enzyme, glucose oxidase (GOX), secreted by the caterpillar Helicoverpa zea on leaves, causes stomatal closure in tomato (Solanum lycopersicum) within 5 min, and in both tomato and soybean (Glycine max) for at least 48 h. GOX also inhibits the emission of several HIPVs during feeding by H. zea, including (Z)-3-hexenol, (Z)-jasmone and (Z)-3-hexenyl acetate, which are important airborne signals in plant defenses. Our findings highlight a potential adaptive strategy where an insect herbivore inhibits plant airborne defenses during feeding by exploiting the association between stomatal dynamics and HIPV emission.
• Herbivore-induced plant volatiles (HIPVs) are widely recognized as an ecologically important defensive response of plants against herbivory. Although the induction of this ‘cry for help’ has been well documented, only a few studies have investigated the inhibition of HIPVs by herbivores and little is known about whether herbivores have evolved mechanisms to inhibit the release of HIPVs. • To examine the role of herbivore effectors in modulating HIPVs and stomatal dynamics, we conducted series of experiments combining pharmacological, surgical, genetic (CRISPR-Cas9) and chemical (GC-MS analysis) approaches. • We show that the salivary enzyme, glucose oxidase (GOX), secreted by the caterpillar Helicoverpa zea on leaves, causes stomatal closure in tomato (Solanum lycopersicum) within 5 min, and in both tomato and soybean (Glycine max) for at least 48 h. GOX also inhibits the emission of several HIPVs during feeding by H. zea, including (Z)-3-hexenol, (Z)-jasmone and (Z)-3-hexenyl acetate, which are important airborne signals in plant defenses. • Our findings highlight a potential adaptive strategy where an insect herbivore inhibits plant airborne defenses during feeding by exploiting the association between stomatal dynamics and HIPV emission.
Herbivore-induced plant volatiles (HIPVs) are widely recognized as an ecologically important defensive response of plants against herbivory. Although the induction of this 'cry for help' has been well documented, only a few studies have investigated the inhibition of HIPVs by herbivores and little is known about whether herbivores have evolved mechanisms to inhibit the release of HIPVs. To examine the role of herbivore effectors in modulating HIPVs and stomatal dynamics, we conducted series of experiments combining pharmacological, surgical, genetic (CRISPR-Cas9) and chemical (GC-MS analysis) approaches. We show that the salivary enzyme, glucose oxidase (GOX), secreted by the caterpillar Helicoverpa zea on leaves, causes stomatal closure in tomato (Solanum lycopersicum) within 5 min, and in both tomato and soybean (Glycine max) for at least 48 h. GOX also inhibits the emission of several HIPVs during feeding by H. zea, including (Z)-3-hexenol, (Z)-jasmone and (Z)-3-hexenyl acetate, which are important airborne signals in plant defenses. Our findings highlight a potential adaptive strategy where an insect herbivore inhibits plant airborne defenses during feeding by exploiting the association between stomatal dynamics and HIPV emission.Herbivore-induced plant volatiles (HIPVs) are widely recognized as an ecologically important defensive response of plants against herbivory. Although the induction of this 'cry for help' has been well documented, only a few studies have investigated the inhibition of HIPVs by herbivores and little is known about whether herbivores have evolved mechanisms to inhibit the release of HIPVs. To examine the role of herbivore effectors in modulating HIPVs and stomatal dynamics, we conducted series of experiments combining pharmacological, surgical, genetic (CRISPR-Cas9) and chemical (GC-MS analysis) approaches. We show that the salivary enzyme, glucose oxidase (GOX), secreted by the caterpillar Helicoverpa zea on leaves, causes stomatal closure in tomato (Solanum lycopersicum) within 5 min, and in both tomato and soybean (Glycine max) for at least 48 h. GOX also inhibits the emission of several HIPVs during feeding by H. zea, including (Z)-3-hexenol, (Z)-jasmone and (Z)-3-hexenyl acetate, which are important airborne signals in plant defenses. Our findings highlight a potential adaptive strategy where an insect herbivore inhibits plant airborne defenses during feeding by exploiting the association between stomatal dynamics and HIPV emission.
Author Sidhu, Jagdeep Singh
Ali, Jared
Peiffer, Michelle
Lynch, Jonathan
Kim, Donghun
Anderson, Charles T.
Rasgon, Jason L.
Chen, Yintong
Zainuddin, Nursyafiqi Bin
Helms, Anjel
Felton, Gary W.
Heu, Chan Chin
Chaverra-Rodriguez, Duverney
Lin, Po-An
Tan, Ching-Wen
AuthorAffiliation 2 Department of Biology Pennsylvania State University 415 Life Sciences Building University Park PA 16802 USA
4 Department of Plant Protection Faculty of Agriculture Universiti Putra Malaysia Serdang Selangor 43400 UPM Malaysia
1 Department of Entomology Pennsylvania State University 501 ASI Building University Park PA 16802 USA
5 Department of Plant Science Pennsylvania State University 310 Tyson Building University Park PA 16802 USA
6 Department of Entomology 103DA Entomology Research Laboratory Texas A&M University College Station TX 77843 USA
3 Department of Cell and Developmental Biology University of California San Diego 9500 Gilman Drive #0335 La Jolla CA 92093 USA
7 Department of Applied Biology Kyungpook National University 80 Daehakro Bukgu, Daegu 41566 Korea
AuthorAffiliation_xml – name: 3 Department of Cell and Developmental Biology University of California San Diego 9500 Gilman Drive #0335 La Jolla CA 92093 USA
– name: 5 Department of Plant Science Pennsylvania State University 310 Tyson Building University Park PA 16802 USA
– name: 4 Department of Plant Protection Faculty of Agriculture Universiti Putra Malaysia Serdang Selangor 43400 UPM Malaysia
– name: 7 Department of Applied Biology Kyungpook National University 80 Daehakro Bukgu, Daegu 41566 Korea
– name: 2 Department of Biology Pennsylvania State University 415 Life Sciences Building University Park PA 16802 USA
– name: 6 Department of Entomology 103DA Entomology Research Laboratory Texas A&M University College Station TX 77843 USA
– name: 1 Department of Entomology Pennsylvania State University 501 ASI Building University Park PA 16802 USA
Author_xml – sequence: 1
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  surname: Lin
  fullname: Lin, Po-An
– sequence: 2
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  surname: Chen
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  fullname: Heu, Chan Chin
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/33459359$$D View this record in MEDLINE/PubMed
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Issue 2
Keywords stomata
effector
plant defense
insect herbivore
HIPV
Language English
License Attribution-NonCommercial-NoDerivs
2021 The Authors. New Phytologist © 2021 New Phytologist Foundation.
This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.
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2020; 14
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Snippet • Herbivore-induced plant volatiles (HIPVs) are widely recognized as an ecologically important defensive response of plants against herbivory. Although the...
Summary Herbivore‐induced plant volatiles (HIPVs) are widely recognized as an ecologically important defensive response of plants against herbivory. Although...
Herbivore‐induced plant volatiles (HIPVs) are widely recognized as an ecologically important defensive response of plants against herbivory. Although the...
Herbivore-induced plant volatiles (HIPVs) are widely recognized as an ecologically important defensive response of plants against herbivory. Although the...
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StartPage 793
SubjectTerms Acetates
Acetic acid
Allelochemicals
Animals
CRISPR
CRISPR-Cas systems
Defensive behavior
Dynamics
effector
Emission
Emissions
Enzymes
Gene editing
Glucose oxidase
Glycine (amino acid)
Glycine max
Helicoverpa zea
Herbivores
Herbivory
HIPV
insect herbivore
Insecta
Insects
Moths
phytophagous insects
plant defense
Plant Stomata
Solanum lycopersicum
Soybeans
Stomata
stomatal movement
Tomatoes
Volatile compounds
Volatile Organic Compounds
Volatiles
Subtitle an insect salivary enzyme closes plant stomata and inhibits volatile release
Title Silencing the alarm
URI https://www.jstor.org/stable/27013913
https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fnph.17214
https://www.ncbi.nlm.nih.gov/pubmed/33459359
https://www.proquest.com/docview/2501884392
https://www.proquest.com/docview/2478778824
https://www.proquest.com/docview/2540482408
https://pubmed.ncbi.nlm.nih.gov/PMC8048682
Volume 230
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