Chrysanthemum expressing a linalool synthase gene ‘smells good’, but ‘tastes bad’ to western flower thrips

Abstract

Summary Herbivore‐induced plant volatiles are often involved in direct and indirect plant defence against herbivores. Linalool is a common floral scent and found to be released from leaves by many plants after herbivore attack. In this study, a linalool/nerolidol synthase, FaNES1, was overexpressed in the plastids of chrysanthemum plants (Chrysanthemum morifolium). The volatiles of FaNES1 chrysanthemum leaves were strongly dominated by linalool, but they also emitted small amount of the C11‐homoterpene, (3E)‐4,8‐dimethyl‐1,3,7‐nonatriene, a derivative of nerolidol. Four nonvolatile linalool glycosides in methanolic extracts were found to be significantly increased in the leaves of FaNES1 plants compared to wild‐type plants. They were putatively identified by LC‐MS‐MS as two linalool–malonyl–hexoses, a linalool–pentose–hexose and a glycoside of hydroxy–linalool. A leaf‐disc dual‐choice assay with western flower thrips (WFT, Frankliniella occidentalis) showed, initially during the first 15 min of WFT release, that FaNES1 plants were significantly preferred. This gradually reversed into significant preference for the control, however, at 20–28 h after WFT release. The initial preference was shown to be based on the linalool odour of FaNES1 plants by olfactory dual‐choice assays using paper discs emitting pure linalool at similar rates as leaf discs. The reversal of preference into deterrence could be explained by the initial nonvolatile composition of the FaNES1 plants, as methanolic extracts were less preferred by WFT. Considering the common occurrence of linalool and its glycosides in plant tissues, it suggests that plants may balance attractive fragrance with ‘poor taste’ using the same precursor compound.

CYP76C1 (Cytochrome P450)-Mediated Linalool Metabolism and the Formation of Volatile and Soluble Linalool Oxides in Arabidopsis Flowers: A Strategy for Defense against Floral Antagonists

“…The linalool conjugates were exclusively detected as putative linalyl-hexose and linalyl-malonyl hexoses, as previously observed Yang et al, 2013). They accumulated at up to 5 times higher concentrations in the cyp76c1 lines, and their levels were significantly reduced in the complemented/35S:CYP76C1 line compared with the wild type ( Figure 6; Supplemental Figure 10A).…”

“…Thus, it seems that the roles of linalool differ depending on the plant-insect interactions. Interestingly, Yang et al (2013) reported that thrips were first attracted by linalool emitted by engineered chrysanthemum expressing linalool/nerolidol synthase from strawberry (Fa-NES1) but were ultimately repelled by linalool conjugates. The role of linalool conjugates and linalool oxides in ecological interactions is still a matter of debate (Raguso and Pichersky, 1999).…”

“…Linalool and its oxides have been reported to accumulate as free or conjugated compounds in flower tissues from various plant species including Arabidopsis (Aharoni et al, 2003;Ginglinger et al, 2013;Yang et al, 2013). Soluble linalool derivatives were thus quantified by targeted UPLC-MS/MS in the inflorescence of wild-type, cyp76c1, and complemented/35S:CYP76C1 lines ( Figure 6; Supplemental Figure 10).…”

“…Dual-choice tests performed on thrips demonstrated that they preferred to visit the flowers of the cyp76c1 mutants over the wild type ( Figure 8A; Supplemental Figure 12). Thrips are antagonistic flower visitors described as being attracted by pure linalool (Koschier et al, 2000) and by linalool-emitting engineered chrysanthemum (Chrysanthemum morifolium) plants transformed with Fa-NES1, but repelled by linalool conjugates (Yang et al, 2013). To distinguish the role of volatiles from the influence of compounds stored in flowers the thrips could feed on, we conducted dual-choice tests in a Y-shaped olfactometer giving thrips the choice between volatiles from the flowers of the wild-type, cyp76c1, or complemented/ 35S:CYP76C1 lines using different combinations ( Figure 8B).…”

Transgenics in Ornamental Crops:Creating Novelties in Economically Important Cut Flowers

“…Expression of this gene in the plastids of chrysanthemum plants resulted in linalool emissions and accumulation of several forms of linalool glycosides. During the first 15 min, WFT significantly preferred these FaNES1 plants, but in the next 24 h gradually changed their preference to the wild type 52 . Recently, Shinoyama et al 53 developed genetically modified chrysanthemums by introducing a modified cry1Ab gene of Bacillus thuringiensis var.…”