Modification of chrysanthemum odour and taste with chrysanthemol synthase induces strong dual resistance against cotton aphids

Jinjin Li, Thierry Delatte, Jacques Vervoort, Liping Gao, Francel Verstappen, Wei Xiong, Jianping Gan, Maarten A. Jongsma, Caiyun Wang

Research output: Contribution to journalArticleAcademicpeer-review

6 Citations (Scopus)

Abstract

Aphids are pests of chrysanthemum that employ plant volatiles to select host plants and ingest cell contents to probe host quality before engaging in prolonged feeding and reproduction. Changes in volatile and nonvolatile metabolite profiles can disrupt aphid-plant interactions and provide new methods of pest control. Chrysanthemol synthase (CHS) from Tanacetum cinerariifolium represents the first committed step in the biosynthesis of pyrethrin ester insecticides, but no biological role for the chrysanthemol product alone has yet been documented. In this study, the TcCHS gene was over-expressed in Chrysanthemum morifolium and resulted in both the emission of volatile chrysanthemol (ca. 47 pmol/h/gFW) and accumulation of a chrysanthemol glycoside derivative, identified by NMR as chrysanthemyl-6-O-malonyl-β-D-glucopyranoside (ca. 1.1 mM), with no detrimental phenotypic effects. Dual-choice assays separately assaying these compounds in pure form and as part of the headspace and extract demonstrated independent bioactivity of both components against the cotton aphid (Aphis gossypii). Performance assays showed that the TcCHS plants significantly reduced aphid reproduction, consistent with disturbance of aphid probing activities on these plants as revealed by electropenetrogram (EPG) studies. In open-field trials, aphid population development was very strongly impaired demonstrating the robustness and high impact of the trait. The results suggest that expression of the TcCHS gene induces a dual defence system, with both repellence by chrysanthemol odour and deterrence by its nonvolatile glycoside, introducing a promising new option for engineering aphid control into plants.
Original languageEnglish
Pages (from-to)1434-1445
JournalPlant Biotechnology Journal
Volume16
Issue number8
Early online date1 Jan 2018
DOIs
Publication statusPublished - Aug 2018

Fingerprint

Chrysanthemum
Aphids
Aphis gossypii
Aphidoidea
odors
Glycosides
glycosides
Tanacetum cinerariifolium
Reproduction
Chrysanthemum cinerariifolium
Chrysanthemum morifolium
Pyrethrins
assays
Pest Control
pyrethrins
pest control
headspace analysis
Plant Cells
probes (equipment)
Insecticides

Keywords

  • Aphid resistance
  • Chrysanthemol synthase
  • Chrysanthemum
  • Double bioactivity
  • Glycoside
  • Terpene volatile

Cite this

@article{857866e9ac26485cbaf025a9983eb811,
title = "Modification of chrysanthemum odour and taste with chrysanthemol synthase induces strong dual resistance against cotton aphids",
abstract = "Aphids are pests of chrysanthemum that employ plant volatiles to select host plants and ingest cell contents to probe host quality before engaging in prolonged feeding and reproduction. Changes in volatile and nonvolatile metabolite profiles can disrupt aphid-plant interactions and provide new methods of pest control. Chrysanthemol synthase (CHS) from Tanacetum cinerariifolium represents the first committed step in the biosynthesis of pyrethrin ester insecticides, but no biological role for the chrysanthemol product alone has yet been documented. In this study, the TcCHS gene was over-expressed in Chrysanthemum morifolium and resulted in both the emission of volatile chrysanthemol (ca. 47 pmol/h/gFW) and accumulation of a chrysanthemol glycoside derivative, identified by NMR as chrysanthemyl-6-O-malonyl-β-D-glucopyranoside (ca. 1.1 mM), with no detrimental phenotypic effects. Dual-choice assays separately assaying these compounds in pure form and as part of the headspace and extract demonstrated independent bioactivity of both components against the cotton aphid (Aphis gossypii). Performance assays showed that the TcCHS plants significantly reduced aphid reproduction, consistent with disturbance of aphid probing activities on these plants as revealed by electropenetrogram (EPG) studies. In open-field trials, aphid population development was very strongly impaired demonstrating the robustness and high impact of the trait. The results suggest that expression of the TcCHS gene induces a dual defence system, with both repellence by chrysanthemol odour and deterrence by its nonvolatile glycoside, introducing a promising new option for engineering aphid control into plants.",
keywords = "Aphid resistance, Chrysanthemol synthase, Chrysanthemum, Double bioactivity, Glycoside, Terpene volatile",
author = "Jinjin Li and Thierry Delatte and Jacques Vervoort and Liping Gao and Francel Verstappen and Wei Xiong and Jianping Gan and Jongsma, {Maarten A.} and Caiyun Wang",
year = "2018",
month = "8",
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language = "English",
volume = "16",
pages = "1434--1445",
journal = "Plant Biotechnology Journal",
issn = "1467-7644",
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Modification of chrysanthemum odour and taste with chrysanthemol synthase induces strong dual resistance against cotton aphids. / Li, Jinjin; Delatte, Thierry; Vervoort, Jacques; Gao, Liping; Verstappen, Francel; Xiong, Wei; Gan, Jianping; Jongsma, Maarten A.; Wang, Caiyun.

In: Plant Biotechnology Journal, Vol. 16, No. 8, 08.2018, p. 1434-1445.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Modification of chrysanthemum odour and taste with chrysanthemol synthase induces strong dual resistance against cotton aphids

AU - Li, Jinjin

AU - Delatte, Thierry

AU - Vervoort, Jacques

AU - Gao, Liping

AU - Verstappen, Francel

AU - Xiong, Wei

AU - Gan, Jianping

AU - Jongsma, Maarten A.

AU - Wang, Caiyun

PY - 2018/8

Y1 - 2018/8

N2 - Aphids are pests of chrysanthemum that employ plant volatiles to select host plants and ingest cell contents to probe host quality before engaging in prolonged feeding and reproduction. Changes in volatile and nonvolatile metabolite profiles can disrupt aphid-plant interactions and provide new methods of pest control. Chrysanthemol synthase (CHS) from Tanacetum cinerariifolium represents the first committed step in the biosynthesis of pyrethrin ester insecticides, but no biological role for the chrysanthemol product alone has yet been documented. In this study, the TcCHS gene was over-expressed in Chrysanthemum morifolium and resulted in both the emission of volatile chrysanthemol (ca. 47 pmol/h/gFW) and accumulation of a chrysanthemol glycoside derivative, identified by NMR as chrysanthemyl-6-O-malonyl-β-D-glucopyranoside (ca. 1.1 mM), with no detrimental phenotypic effects. Dual-choice assays separately assaying these compounds in pure form and as part of the headspace and extract demonstrated independent bioactivity of both components against the cotton aphid (Aphis gossypii). Performance assays showed that the TcCHS plants significantly reduced aphid reproduction, consistent with disturbance of aphid probing activities on these plants as revealed by electropenetrogram (EPG) studies. In open-field trials, aphid population development was very strongly impaired demonstrating the robustness and high impact of the trait. The results suggest that expression of the TcCHS gene induces a dual defence system, with both repellence by chrysanthemol odour and deterrence by its nonvolatile glycoside, introducing a promising new option for engineering aphid control into plants.

AB - Aphids are pests of chrysanthemum that employ plant volatiles to select host plants and ingest cell contents to probe host quality before engaging in prolonged feeding and reproduction. Changes in volatile and nonvolatile metabolite profiles can disrupt aphid-plant interactions and provide new methods of pest control. Chrysanthemol synthase (CHS) from Tanacetum cinerariifolium represents the first committed step in the biosynthesis of pyrethrin ester insecticides, but no biological role for the chrysanthemol product alone has yet been documented. In this study, the TcCHS gene was over-expressed in Chrysanthemum morifolium and resulted in both the emission of volatile chrysanthemol (ca. 47 pmol/h/gFW) and accumulation of a chrysanthemol glycoside derivative, identified by NMR as chrysanthemyl-6-O-malonyl-β-D-glucopyranoside (ca. 1.1 mM), with no detrimental phenotypic effects. Dual-choice assays separately assaying these compounds in pure form and as part of the headspace and extract demonstrated independent bioactivity of both components against the cotton aphid (Aphis gossypii). Performance assays showed that the TcCHS plants significantly reduced aphid reproduction, consistent with disturbance of aphid probing activities on these plants as revealed by electropenetrogram (EPG) studies. In open-field trials, aphid population development was very strongly impaired demonstrating the robustness and high impact of the trait. The results suggest that expression of the TcCHS gene induces a dual defence system, with both repellence by chrysanthemol odour and deterrence by its nonvolatile glycoside, introducing a promising new option for engineering aphid control into plants.

KW - Aphid resistance

KW - Chrysanthemol synthase

KW - Chrysanthemum

KW - Double bioactivity

KW - Glycoside

KW - Terpene volatile

U2 - 10.1111/pbi.12885

DO - 10.1111/pbi.12885

M3 - Article

VL - 16

SP - 1434

EP - 1445

JO - Plant Biotechnology Journal

JF - Plant Biotechnology Journal

SN - 1467-7644

IS - 8

ER -