Biosynthesis of monoterpene scent compounds in roses

Magnard, Jean‐Louis; Roccia, Aymeric; Caissard, Jean‐Claude; Vergne, Philippe; Sun, Pulu; Hecquet, Romain; Dubois, Annick; Oyant, Laurence Hibrand‐Saint; Jullien, Frédéric; Nicolè, Florence; Raymond, Olivier; Huguet, Stéphanie; Baltenweck, Raymonde; Meyer, Sophie; Claudel, Patricia; Jeauffre, Julien; Rohmer, Michel; Foucher, Fabrice; Hugueney, Philippe; Bendahmane, Mohammed; Baudino, Sylvie

doi:10.1126/science.aab0696

Cited by 191 publications

(210 citation statements)

References 44 publications

(32 reference statements)

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“…The conversion of CDP to trans-chrysanthemol could be catalyzed by a member of the terpene synthase family similar to those terpene synthases catalyzing the conversion of geranyl diphosphate to the alcohol monoterpenes geraniol and linalool in many species (Chen et al, 2011), or CDP could be hydrolyzed by phosphatases to give trans-chrysanthemol, similar to the conversion of geranyl diphosphate to geraniol in rose (Rosa spp.) flowers (Magnard et al, 2015). However, no such enzymatic activities were reported thus far in T. cinerariifolium.…”

mentioning

confidence: 93%

Coexpression Analysis Identifies Two Oxidoreductases Involved in the Biosynthesis of the Monoterpene Acid Moiety of Natural Pyrethrin Insecticides in Tanacetum cinerariifolium

Moghe

Schilmiller

et al. 2017

Plant Physiol.

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Flowers of Tanacetum cinerariifolium produce a set of compounds known collectively as pyrethrins, which are commercially important pesticides that are strongly toxic to flying insects but not to most vertebrates. A pyrethrin molecule is an ester consisting of either trans-chrysanthemic acid or its modified form, pyrethric acid, and one of three alcohols, jasmolone, pyrethrolone, and cinerolone, that appear to be derived from jasmonic acid. Chrysanthemyl diphosphate synthase (CDS), the first enzyme involved in the synthesis of trans-chrysanthemic acid, was characterized previously and its gene isolated. TcCDS produces free trans-chrysanthemol in addition to trans-chrysanthemyl diphosphate, but the enzymes responsible for the conversion of trans-chrysanthemol to the corresponding aldehyde and then to the acid have not been reported. We used an RNA sequencingbased approach and coexpression correlation analysis to identify several candidate genes encoding putative trans-chrysanthemol and trans-chrysanthemal dehydrogenases. We functionally characterized the proteins encoded by these genes using a combination of in vitro biochemical assays and heterologous expression in planta to demonstrate that TcADH2 encodes an enzyme that oxidizes trans-chrysanthemol to trans-chrysanthemal, while TcALDH1 encodes an enzyme that oxidizes trans-chrysanthemal into transchrysanthemic acid. Transient coexpression of TcADH2 and TcALDH1 together with TcCDS in Nicotiana benthamiana leaves results in the production of trans-chrysanthemic acid as well as several other side products. The majority (58%) of trans-chrysanthemic acid was glycosylated or otherwise modified. Overall, these data identify key steps in the biosynthesis of pyrethrins and demonstrate the feasibility of metabolic engineering to produce components of these defense compounds in a heterologous host.

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mentioning

confidence: 93%

Coexpression Analysis Identifies Two Oxidoreductases Involved in the Biosynthesis of the Monoterpene Acid Moiety of Natural Pyrethrin Insecticides in Tanacetum cinerariifolium

Moghe

Schilmiller

et al. 2017

Plant Physiol.

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“…The corresponding probe belongs to cluster 4, which also harbors several monoterpenes (Table 2, Supplementary Tables S8, S9). Recently, a rose nudix hydrolase was reported to convert geranyl diphosphate to geranyl monophosphate, which in turn is hydrolyzed to geraniol by a phosphatase activity (Magnard et al, 2015). This alternative and completely new terpene synthase-independent route for monoterpene production might play a role also in other plants, including grapevine.…”

Section: Resultsmentioning

confidence: 99%

Drawing Links from Transcriptome to Metabolites: The Evolution of Aroma in the Ripening Berry of Moscato Bianco (Vitis vinifera L.)

et al. 2017

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Monoterpenes confer typical floral notes to “Muscat” grapevine varieties and, to a lesser extent, to other aromatic non-Muscat varieties. Previous studies have led to the identification and functional characterization of some enzymes and genes in this pathway. However, the underlying genetic map is still far from being complete. For example, the specific steps of monoterpene metabolism and its regulation are largely unknown. With the aim of identifying new candidates for the missing links, we applied an integrative functional genomics approach based on the targeted metabolic and genome-wide transcript profiling of Moscato Bianco ripening berries. In particular, gas chromatography-mass spectrometry analysis of free and bound terpenoid compounds was combined with microarray analysis in the skins of berries collected at five developmental stages from pre-veraison to over-ripening. Differentially expressed metabolites and probes were identified in the pairwise comparison between time points by using the early stage as a reference. Metabolic and transcriptomic data were integrated through pairwise correlation and clustering approaches to discover genes linked with particular metabolites or groups of metabolites. These candidate transcripts were further checked for co-localization with quantitative trait loci (QTLs) affecting aromatic compounds. Our findings provide insights into the biological networks of grapevine secondary metabolism, both at the catalytic and regulatory levels. Examples include a nudix hydrolase as component of a terpene synthase-independent pathway for monoterpene biosynthesis, genes potentially involved in monoterpene metabolism (cytochrome P450 hydroxylases, epoxide hydrolases, glucosyltransferases), transport (vesicle-associated proteins, ABCG transporters, glutathione S-transferases, amino acid permeases), and transcriptional control (transcription factors of the ERF, MYB and NAC families, intermediates in light- and circadian cycle-mediated regulation with supporting evidence from the literature and additional regulatory genes with a previously unreported association to monoterpene accumulation).

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“…The length of time required for effective silencing of flowers with graft‐accelerated VIGS (approximately 30–35 d) is also much shorter compared with the conventional method (approximately 90–270 d; Figure ). Using the grafting method, genes related to floral color ( RhDFR1 (Suzuki et al ; Katsumoto et al )), development ( RhAG (Ma et al )), and fragrance ( RhNUDX1 (Magnard et al )) were successfully silenced. We found that 44.4% of RhDFR1 ‐silenced rose flowers exhibited bleached petals.…”

Section: Discussionmentioning

confidence: 99%

Graft-accelerated virus-induced gene silencing facilitates functional genomics in rose flowers

Yan

Shi

et al. 2017

J. Integr. Plant Biol.

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Rose has emerged as a model ornamental plant for studies of flower development, senescence, and morphology, as well as the metabolism of floral fragrances and colors. Virus-induced gene silencing (VIGS) has long been used in functional genomics studies of rose by vacuum infiltration of cuttings or seedlings with an Agrobacterium suspension carrying TRV-derived vectors. However, VIGS in rose flowers remains a challenge because of its low efficiency and long time to establish silencing. Here we present a novel and rapid VIGS method that can be used to analyze gene function in rose, called 'graft-accelerated VIGS', where axillary sprouts are cut from the rose plant and vacuum infiltrated with Agrobacterium. The inoculated scions are then grafted back onto the plants to flower and silencing phenotypes can be observed within 5 weeks, post-infiltration. Using this new method, we successfully silenced expression of the RhDFR1, RhAG, and RhNUDX1 in rose flowers, and affected their color, petal number, as well as fragrance, respectively. This grafting method will facilitate high-throughput functional analysis of genes in rose flowers. Importantly, it may also be applied to other woody species that are not currently amenable to VIGS by conventional leaf or plantlet/seedling infiltration methods.

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Biosynthesis of monoterpene scent compounds in roses

Cited by 191 publications

References 44 publications

Coexpression Analysis Identifies Two Oxidoreductases Involved in the Biosynthesis of the Monoterpene Acid Moiety of Natural Pyrethrin Insecticides in Tanacetum cinerariifolium

Coexpression Analysis Identifies Two Oxidoreductases Involved in the Biosynthesis of the Monoterpene Acid Moiety of Natural Pyrethrin Insecticides in Tanacetum cinerariifolium

Drawing Links from Transcriptome to Metabolites: The Evolution of Aroma in the Ripening Berry of Moscato Bianco (Vitis vinifera L.)

Graft-accelerated virus-induced gene silencing facilitates functional genomics in rose flowers

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