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The Diversity of Volatile Compounds in Australia's Semi-Desert

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plants Article The Diversity of Volatile Compounds in Australia’s Semi-Desert Genus Eremophila (Scrophulariaceae) Nicholas J. Sadgrove 1,* , Guillermo F. Padilla-González 1 , Alison Green 1, Moses K. Langat 1 , Eduard Mas-Claret 1, Dane Lyddiard 2 , Julian Klepp 2 , Sarah V. A.-M. Legendre 2, Ben W. Greatrex 2, Graham L. Jones 2, Iskandar M. Ramli 2, Olga Leuner 3 and Eloy Fernandez-Cusimamani 3,* 1 Jodrell Science Laboratory, Royal Botanic Gardens Kew, Richmond TW9 3DS, UK; [email protected] (G.F.P.-G.); [email protected] (A.G.); [email protected] (M.K.L.); [email protected] (E.M.-C.) 2 School of Science and Technology and School of Rural Medicine, University of New England, Armidale, NSW 2351, Australia; [email protected] (D.L.); [email protected] (J.K.); [email protected] (S.V.A.-M.L.); [email protected] (B.W.G.); [email protected] (G.L.J.); [email protected] (I.M.R.) 3 Department of Crop Sciences and Agroforestry, Faculty of Tropical AgriSciences, Czech University of Life Sciences Prague, Kamýcká 129, 16500 Prague, Czech Republic; [email protected] * Correspondence: [email protected] (N.J.S.); [email protected] (E.F.-C.); Tel.: +44-785-756-9823 (N.J.S.); +420-224-382-183 (E.F.-C.) Abstract: Australia’s endemic desert shrubs are commonly aromatic, with chemically diverse ter- penes and phenylpropanoids in their headspace profiles. Species from the genus Eremophila (Scro- Citation: Sadgrove, N.J.; phulariaceae ex. Myoporaceae) are the most common, with 215 recognised taxa and many more that Padilla-González, G.F.; Green, A.; Langat, M.K.; Mas-Claret, E.; have not yet been described, widely spread across the arid parts of the Australian continent. Over Lyddiard, D.; Klepp, J.; Legendre, the years, our research team has collected multiple specimens as part of a survey to investigate the S.V.A.-M.; Greatrex, B.W.; Jones, G.L.; chemical diversity of the genus and create leads for further scientific enquiry. In the current study, et al. The Diversity of Volatile the diversity of volatile compounds is studied using hydrodistilled essential oils and leaf solvent Compounds in Australia’s extracts from 30 taxa. Several rare terpenes and iridoids were detected in chemical profiles widely Semi-Desert Genus Eremophila across the genus, and three previously undescribed sesquiterpenes were isolated and are assigned by (Scrophulariaceae). Plants 2021, 10, 2D NMR—E-11(12)-dehydroisodendrolasin, Z-11-hydroxyisodendrolasin and 10-hydroxydihydro- 785. https://doi.org/10.3390/ α-humulene acetate. Multiple sampling from Eremophila longifolia, Eremophila arbuscular, Eremophila plants10040785 latrobei, Eremophila deserti, Eremophila sturtii, Eremophila oppositifolia and Eremophila alternifolia coneys that species in Eremophila are highly chemovariable. However, taxa are generally grouped according Academic Editor: Jésus Palá-Pául to the expression of (1) furanosesquiterpenes, (2) iridoids or oxides, (3) mixtures of 1 and 2, (4) phenyl- Received: 30 March 2021 propanoids, (5) non-furanoid terpenes, (6) mixtures of 4 and 5, and less commonly (7) mixtures of 1 Accepted: 13 April 2021 and 5. Furthermore, GC–MS analysis of solvent-extracted leaves taken from cultivated specimens Published: 16 April 2021 conveys that many heavier ‘volatiles’ with lower vapour pressure are not detected in hydrodistilled essential oils and have therefore been neglected in past chemical studies. Hence, our data reiterate Publisher’s Note: MDPI stays neutral that chemical studies of the genus Eremophila will continue to describe new metabolites and that with regard to jurisdictional claims in taxon determination has limited predictive value for the chemical composition. published maps and institutional affil- iations. Keywords: phenylpropanoid; terpene; furanosesquiterpene; Eremophila; essential oil Copyright: © 2021 by the authors. 1. Introduction Licensee MDPI, Basel, Switzerland. The semi-desert ‘grassland’ region of Australia’s inner perimeter is in a transition This article is an open access article zone between the sandy central Australian deserts and the tropical, subtropical, or tem- distributed under the terms and perate regions (Figure1). In these semi-deserts, several species of Eremophila are found in conditions of the Creative Commons dwindling populations [1] adjacent to sandstone or shale ranges that, on rare occasions, Attribution (CC BY) license (https:// channel rainwater to near exhausted water pans underlain by red or grey cracking clay, creativecommons.org/licenses/by/ which is where some of the highest essential oil-yielding aromatic species can be found. 4.0/). Plants 2021, 10, 785. https://doi.org/10.3390/plants10040785 https://www.mdpi.com/journal/plants Plants 2021, 10, 785 2 of 41 Plants 2021, 10, x FOR PEER REVIEW 3 of 33 Such species include the diploid specimens of Eremophila longifolia (R.Br) F.Muell from Mutawintji National Park [2] and the myodesert-1-ene-yielding species Eremophila dalyana F.Muell of the ‘grey ranges’ in south-west Queensland [3]. Figure 1. Australian climate map; image taken from https://en.wikipedia.org/wiki/Deserts_of_ FigureAustralia 1. Australian(accessed on 15climate January map; 2021). image taken from https://en.wikipedia.org/wiki/De- serts_of_Australia (accessed on 15 January 2021). In contrast, other moderately aromatic species are sparsely distributed across the 2.undulating Results and slopes Discussion and plains of western New South Wales, the sand-to-clay dermosols on the flat plains of central west Queensland and north-west Western Australia. Human habi- tationIt ofis thesecommon arid parts for isstudies sparse, of particularly new essential outside oils of the from lake regionsfamiliar (i.e., genera Menindee to be comprised ofLakes), a diversity where farmingof known practices volat includeile organic cattle compounds. and sheep grazing. Hence, Due routine to populous gaswild chromatography andgoats, mass the nativespectrometry flora is under (GC–MS), considerable together pressure, with with a commercial some common mass species spectral in rapid library (NIST) decline as grazing continues to denude the landscape. The so called ‘goat weed’ is a classic andexample; retentionEremophila indices latrobei areF.Muell usually is oftenall that found are with necessary only a few to remaining chemically leaves. characterize In new wholecontrast, essential with the oils. disappearance of indigenous foliage, opportunistic native species are rapidlyHowever, finding avolatiles niche. Both fromEremophila the genus sturtii EremophilaR.Br and Eremophila are different mitchellii fromBenth. those are familiar to the speciesbecoming of sothe common northern that hemisphere they are regarded and by mass some fragmentation as a weed [4]. spectrums are not present in Previous phytochemical studies on the volatile organic compounds in species of commercial libraries. Identification of compounds is therefore strongly dependent on nu- Eremophila demonstrate considerable intraspecific variability, particularly in E. longifolia [2, clear5,6]. magnetic Furthermore, resonance aromatic spectroscopy timbers express and completely authentic different standards. chemical The profiles current as study chem- icallycompared assigned to their 19 leaves. rare albeit To illustrate known this, sesq theuiterpenes, aromatic timbers and ofanotherE. mitchellii threewere previously un- described.once regarded In asmany a suitable cases, alternative only single to the leaf Australian specimens sandalwood, were Santalumstudied, spicatum so many unknown compounds(R.Br) A.DC., are producing highlighted a termite to repellent convey essential the full oil comprisedchemical ofdiversity eremophilones of the and genus and the other derivatives [7]. As a substitute, it came to be regarded with distaste and earned the potentialcolloquial to name identify ‘bastard previously sandalwood’ undescribed and was discontinued metabolites. [8]. Furthermore, the chemical profiles within species, and even within populations, can often be entirely different from specimen to specimen. This is illustrated in the current study. Out of the 30 taxa that we studied (Tables 1 and 2), several replicates were collected for Eremophila arbuscular, Eremophila latrobei, Eremophila alternifolia, Eremophila longifolia, Er- emophila deserti, Eremophila oppositifolia subsp. rubra, Eremophila mitchellii and Eremophila sturtii. In some cases, only hydrodistilled essential oils were studied but in other cases small leaf samples were taken, extracted in dichloromethane, and analysed by GC–MS. The distinction is explained through the text. Some species of Eremophila demonstrate a strong chemical overlap into species from Myoporum. This is particularly true of specimens that express furanosesquiterpenes in their metabolome. Furanosesquiterpenes are expressed in several species of Eremophila and most species of Myoporum. Over the years, the synonymity of these two genera has been debated and species are sometimes removed from one genus and placed in the other. Plants 2021, 10, 785 3 of 41 The etymology of the name Eremophila is related to its persistence in arid regions. The name is an amalgamation of the Greek words ‘eremos’, which means desert, and ‘philos’, which means friend (or platonic love); hence, Eremophila translates to ‘desert loving’. It is also believed that the ephemeral nature of the arid landscapes is important in persuading the expression of secondary metabolites. Preliminary observations of the effects of persistent drought and the opposite,
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