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RESEARCH ARTICLE (Open Access)

Floral constituents of the Australian tar tree, Semecarpus australiensis

Soo Jean Park https://orcid.org/0000-0002-5414-6772 A B * , Jodie Cheesman C , Donald N. S. Cameron A B , Stefano G. De Faveri C and Phillip W. Taylor A B
+ Author Affiliations
- Author Affiliations

A Applied BioSciences, Macquarie University, Sydney, 2109, Australia.

B Australian Research Council Centre for Fruit Fly Biosecurity Innovation, Macquarie University, North Ryde, NSW 2109, Australia.

C Horticulture and Forestry Science, Queensland Department of Agriculture and Fisheries, Mareeba, Qld, Australia.

* Correspondence to: soojean.park@mq.edu.au

Handling Editor: Charlotte Williams

Australian Journal of Chemistry 75(12) 945-952 https://doi.org/10.1071/CH22097
Submitted: 27 April 2022  Accepted: 22 September 2022   Published: 23 November 2022

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

Floral constituents of the Australian tar tree, Semecarpus australiensis, distributed in Melanesia and Northern Australia, were extracted with solvent, and analyzed by gas chromatography-mass spectrometry. The main constituents were 16- and 18-carbon fatty acids and their ethyl esters. Amongst the 67 identified compounds, zingerone was detected in minute quantity, providing the chemical basis for previous observations of fruit fly attraction to the flowers. The present study is the first to report the chemical profile of tar tree flowers.

Keywords: fatty acids, floral volatiles, fruit fly, GC-MS, isoeugenol, native cashew, salicylates, Tephritidae.

Introduction

The flowers of many orchid species of the genus Bulbophyllum contain phenylpropanoids or phenylbutanoids that attract male Bactrocera and Zeugodacus fruit flies (Diptera, Tephritidae).[1] Their most common responses are to raspberry ketone and methyl eugenol, although many species do not respond to either of these compounds or respond only weakly.[2] More recent studies have found that some Bactrocera and Zeugodacus species respond to zingerone,[1a,1d,3] which occurs as a floral scent in Bu. patens and Bu. baileyi.[1a,1b,1d] In addition, isoeugenol and methyl isoeugenol have been found to attract some species that are non-responsive or weakly responsive to raspberry ketone and methyl eugenol.[3c,3d,4] Isoeugenol and methyl isoeugenol occur in the essential oils of various plant taxa, including different species of Citrus, Clusia, Pimenta, and Etlingera.[5] Reasons for the attraction of male fruit flies to phenylpropanoids and phenylbutanoids are incompletely understood,[6] and vary across compounds and fruit fly species. For example, males of some species of Bactrocera acquire methyl eugenol as a pheromone precursor[7] or as a metabolic enhancer to increase mating competitiveness. [8] In return, Bulbophyllum orchids benefit through pollination,[1a,1b,1f] hence the interaction between the orchids and fruit flies is mutually beneficial.

In an evolutionarily unrelated interaction, the flowers of Passiflora maliformis release zingerone from their filaments and attract Bactrocera jarvisi.[9] Earlier records report that B. jarvisi is also attracted to flowers of the tar tree, also known as native cashew, Semecarpus australiensis, as well as to Bu. baileyi.[10] Zingerone in Bu. baileyi is responsible for attraction of B. jarvisi.[10b]

The tar tree grows naturally in rainforests, including the northeast part of Queensland and Northern Territory in Australia, and across a wide range in Melanesia including Torres Strait Islands, New Guinea, New Britain, and Aru Islands.[11] The tar tree produces cream-colored flowers in spring. Staminate (male) flowers, about 1.5 mm long, are sessile, while pistillate (female) flowers, about 4 mm long, are on pedicels. To date, the chemistry of tar tree flowers is unknown. The present study aims to (1) characterize the compounds in the tar tree flowers and (2) confirm the chemical basis of previous observations on the attraction of B. jarvisi males. The present study describes constituents in the solvent extracts of both staminate and pistillate tar tree flowers analyzed by gas chromatography-mass spectrometry (GC-MS) and identifies the chemical basis for the attraction of fruit flies to these flowers.


Results and discussion

Extracts of tar tree flowers contained a diverse suite of 67 compounds, including 11 aliphatic acids, 13 aliphatic esters, 2 aliphatic alcohols, 2 monoterpenes, 4 aldehydes, 15 aromatic compounds, and 20 hydrocarbons (Table 1). The proportions of the classes of the detected compounds in pistillate and staminate flowers are illustrated in Fig. 1. The aliphatic esters had the highest proportions in both sexes (51.9% in pistillate flowers and 35.2% in staminate flowers), followed by the aliphatic acids (21.8% in pistillate and 21.3% in staminate flowers). While many hydrocarbons were detected, their proportions were small (2.7% in pistillate flowers and 5.4% in staminate flowers). The proportions of aromatic compounds were 4.7 and 4.5% in pistillate flowers and staminate flowers, respectively. The remainder consisted of monoterpenes (2.6% in pistillate flowers and 9.6% in staminate flowers), aliphatic aldehydes (0.6% in pistillate flowers and 0.4% in staminate flowers), and aliphatic alcohols (0.3% in pistillate flowers and 0.9% in staminate flowers). D-limonene is noticeably higher in staminate flowers than in pistillate flowers (Table 1). Principal component analysis identified notable differences in the compositions of pistillate and staminate flowers (Fig. 2). Further detailed investigation will be required to identify the functional or physiological role of such compositional differences in these flowers.


Table 1.  Identified compounds in Smecarpus australiensis.
Click to zoom


Fig. 1.  Proportions of the compound classes in female and male flowers of S. australiensis.
F1


Fig. 2.  Principal component analysis of the individual compounds in pistillate and staminate flowers; Biplot of the first and second principal components.
F2

Flowers release a more diverse suite of volatiles at higher levels than other plant parts.[46] The floral volatiles are by-products of plant secondary metabolism, and some volatiles function to attract pollinators or as a defence against florivores and pathogens.[46] The fatty acids, 16- and 18-carbon species, i.e. C16:1 (palmitoleic acid), C16:0 (palmitic acid), C18:1 (oleic acid) and C18:2 (linoleic), and their ethyl esters are the predominant constituents in the tar tree flower samples. The fatty acids are important compounds in plants. For example, most cutin monomers are derived from the 16- and 18-carbon fatty acids to form the macromolecules that are the framework of the plant cuticles. [47] The 18-carbon unsaturated fatty acids can be nitrated to act as signalling mediators in the plant-defence system in oxidative stress situations.[48] It is also known that linoleic acid serves as a hydroperoxyl intermediate for the biosynthesis of green leaf volatiles.[49] The other detected compounds are also commonly found in plants. For example, D-limonene inhibits spore germination of the rice blast fungus (Magnaporthe oryzae) and is expressed at higher levels in response to the up-regulation of a terpene synthase gene when rice plants have the fungal infection.[50] Methyl salicylate is widespread as a herbivore-induced volatile to communicate herbivore attacts in plants. For example, barley exposed to deuterated methyl salicylate showed significant qualitative and quantitative changes in the chemical profile of the headspace.[51] Methyl salicylate is also known as a mobile signal to induce systemic acquired resistance against biotrophic pathogens in the tobacco plant.[52]

Ethyl and methyl salicylates are the major aromatic constituents in solvent extracts of the tar tree flowers, while phenylpropanoids and phenylbutanoids are present only in minute amounts. Although the amount of zingerone is minute (Table 1), the presence of this compound explains the attraction of B. jarvisi.[3a,53] The attraction of B. jarvisi is specific to zingerone and has been confirmed by systematic modification of zingerone and testing the synthesized analogs in the field.[54] In the study, >99% of flies captured by traps containing zingerone and its analogs were B. jarvisi. Hence, it is likely that zingerone is responsible for the observed interaction between the plant and fruit fly species. There appears to be no record of other fruit fly species being attracted to tar tree flowers. Along the tar tree natural distribution range, it is likely that different local fruit fly species are attracted to one or more of the phenylpropanoids and phenylbutanoids. For example, tar tree flowers contain trans-isoeugenol which is attractive to males of a New Caledonian fruit fly, B. curvipennis.[3d]

In summary, the present study addressed the chemical basis of the interaction between B. jarvisi and the native tar tree. Solvent extracts from tar tree flowers were dominated by unsaturated fatty acids and their ethyl esters. Amongst the 67 identified compounds, zingerone, a fruit fly attractant, was detected in minute amounts, providing a likely explanation for reported attraction of B. jarvisi fruit flies. Co-evolutionary interactions between plants and their insect pollinators mediated by plant secondary metabolites are known.[55] The commonly used fruit fly attractants are plant secondary metabolites or derivatives, which have been deployed for decades to monitor and control horticultural pest fruit flies.[56] There are many unexplored plant species, but future investigations will greatly benefit from a targeted approach, for example, studies on species with previous observations and records will increase the chances of new attractant discovery and address the chemistry of a species of interest.


Experimental

Chemicals

3-Methylbutanoic acid, n-nonane, 2-heptenal, benzaldehyde, β-myrcene, 1-decene, n-decane, D-limonene, benzyl alcohol, 3-methylbenzaldehyde, n-heptanoic acid, n-nonanal, phenethyl alcohol, n-octanoic acid, methyl 2-hydroxybenzoate, 1-dodecene, n-dodecane, n-decanal, benzothiazole, n-nonanoic acid, ethyl 2-hydroxybenzoate, n-tridecane, 3-alyl-6-methoxyphenol, n-decanoic acid, 4-hydroxy-3-methoxybenzaldehyde, 1-tetradecene, n-tetradecane, 3-allyl-6-methoxyphenol, 1-tetradecene, tetradecane, (E)-2-methoxy-4-(1-propenyl)phenol, n-dodecanoic acid, n-hexadecane, n-tetradecanal, benzophenone, 4-(4-hydroxy-3-methoxyphenyl)-2-butanone, n-heptadecane, n-tetradecanoic acid, ethyl tetradecanoate, n-octadecane, 1-hexadecanol, ethyl pentadecanoate, (Z)-9-hexadecenoic acid, n-hexadecanoic acid, ethyl (Z)-9-hexadecenoate, ethyl (E)-9-hexadecenoate, ethyl hexadecanoate, (Z,Z)-9,12-octadecadienoic acid, ethyl (Z,Z)-9,12-octadecadienoate, ethyl (Z,Z,Z)-9,12,15-octadecatrienoate, 1-octadecanol, (Z,Z)-9,12-octadecadienoic acid, (Z)-9-octadecenloic acid, ethyl (Z)-9-octadecenoate, and ethyl octadecanoate were purchased from Sigma-Aldrich. 3-Ethylhexyl acetate was purchased from Tokyo Chemical Industry. All compounds were analytical grade with 98% purity or higher.

Collection of flowers

The flowers (Queensland Herbarium voucher number: AQ952605) were collected from male and female tar trees located in Silver Crescent Park, Palm Cove, Queensland, Australia (−16.758420, 154.669235) in October 2018. Branches with staminte or pistillate flowers were cut from the trees. Ten flowers of each sex were separately cut into fine pieces in a ceramic bowl using microscissors. The fine flower pieces were transferred to a 2.0 mL clear vial containing 1.0 mL of absolute ethanol (six replicates for each sex). The samples were transported to Macquarie University, Australia, and stored at 4°C for 2–3 weeks until extracted.

Extraction of flowers

Milli-Q water (1.0 mL) (Millipore) was added to each sample vial, vortexed for 30 s, and then ultrasonicated for 30 min. The aqueous extract was transferred to a 10 mL separating funnel. The aqueous phase was extracted with the organic solvents (3 × 2.0 mL, 10% ethyl acetate in hexane). The organic layers were combined, washed with Milli-Q water (6.0 mL), and dried over Na2SO4. The solvents were evaporated using a Rotary evaporator (Buchi), and the residue was re-dissolved in 200 µL of 10% ethyl acetate (v/v) in hexane. The extracted samples were stored at −30°C until analyzed. An aliquot (5 μL) of the three internal standards, 1-octanol, methyl n-dodecanoate, and methyl n-hexadecanoate, were incorporated to give 2.6, 2.5, and 2.6 µg/mL, respectively.

Gas chromatography-mass spectrometry (GC-MS) analysis

GC-MS analysis was performed on a Shimadzu GCMS TQ8040 spectrometer equipped with a split/splitless injector, fused silica capillary column (SH-Rtx-5MS, 30 m × 0.25 mm I.D. × 0.25 μm film thickness) with cross-bond 5% diphenyl/95% dimethyl polysiloxane as the stationary phase and integrated mass spectrometry (MS). Helium gas (BOC, North Ryde, NSW, Australia) (99.999%) was used as a carrier gas with a constant flow of 1.5 mL/min. An aliquot of 1 μL of a sample was injected in splitless mode, and the injection port temperature was 270°C. The initial column temperature was set at 60°C and held for 4 min, increased to 220°C at a rate of 2°C/min, then increased to 320°C at a rate of 30°C/min and held for 3 min. The interface and ion source box temperatures were set at 250 and 200°C, respectively. The ionization method was electron impact at a voltage of 70 eV. The spectra were obtained over a mass range of m/z 41–600. The data were processed by Shimadzu GCMS Post-run software. The retention indices were obtained by analyzing a run of a standard mixture of C8 to C40 alkane with a sample. For identifications, mass spectra were compared with the NIST library (NIST17-1, NIST17-2, NIST17s) to identify related molecules. Fragmentation patterns and retention indices published in the literature were used to determine candidate molecules. The identity of a candidate molecule was confirmed by comparing retention time and fragmentations of the authentic molecule. The solvents used, including absolute ethanol, hexane, and ethyl acetate, were routinely analyzed by GC-MS to identify any impurities. The percentage of each compound was calculated from the quantification or semi-quantification of the constituents.

Standard solutions of five known concentrations of the individual compounds were prepared to quantify individual compounds. These contained three internal standards with the same concentration used in the extracted samples, in 5 mL volumetric flasks. The standard solutions were analyzed by GC-MS along with the flower samples. The standard curves of the authentic samples were generated by linear regression of peak area ratios of a compound to the internal standard against concentration ratios of a compound to that of the internal standard. Equations obtained by linear regression were used to calculate the concentrations of the compounds in a sample, and the amount of a compound per flower was subsequently estimated by taking account of the final sample volume of a sample prepared from ten flowers.

Several compounds that are not commercially available were estimated by the use of a surrogate.[57] The response factor of 1,2,4-trimethyl cyclohexane was used to estimate the quantities of 1-ethyl-4-methylcyclohexane and 1-ethyl-3-methylcyclohexane. The response factor of benzaldehyde was used to estimate the quantity of benzeneacetaldehyde. The response factor of methyl hexadecanoate was used to estimate the quantities of 3-methyl pentadecane, undecyl cyclopentane, 2-methyl hexadecane, 2-methyl heptadecane. The response factor of ethyl (Z)-9-hexadecenoate was used to estimate the quantity of ethyl (E)-9-hexadecenoate. The response factor of ethyl (Z)-9-octadecenoate was used to estimate the quantity of ethyl (E)-9-octadecenoate.

Data analysis

Principal component analysis was carried out to compare the compositions of pistillate and staminate flowers.


Data availability

Not applicable.


Conflicts of interest

The authors declare no conflicts of interest.


Declaration of funding

This research was supported by the Australian Research Council Industrial Transformation Training Centre (ITTC) for Fruit Fly Biosecurity Innovation (Project IC50100026), funded by the Australian Government.


Supplementary material

Supplementary material is available online.



Acknowledgements

The authors thank Prof Darren Crayn and Mr Stuart Worboys for helping the identification of the Australian tar trees and locating them.


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