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Differential Metabolic Specialization of Foliar Oil Glands in Eucalyptus

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Differential Metabolic Specialization of Foliar Oil Glands in Eucalyptus Tree Physiology 38, 1451–1460 doi:10.1093/treephys/tpy077 Research paper Differential metabolic specialization of foliar oil glands in Eucalyptus brevistylis Brooker (Myrtaceae) Downloaded from https://academic.oup.com/treephys/article/38/10/1451/5055867 by guest on 27 September 2021 † † Jason Q.D. Goodger 1,4, , Samiddhi L. Senaratne1, , Dean Nicolle2 and Ian E. Woodrow3 1School of BioSciences, The University of Melbourne, Melbourne, Victoria 3010, Australia; 2Currency Creek Arboretum, PO Box 808 Melrose Park, Currency Creek, SA 5039, Australia; 3School of Ecosystem and Forest Sciences, The University of Melbourne, Melbourne, Victoria 3010, Australia; 4Corresponding author ([email protected]) orcid.org/0000- 0001-7392-3891 Received January 7, 2018; accepted June 6, 2018; published online July 19, 2018; handling Editor Ülo Niinemets Trees and shrubs from the genus Eucalyptus are characterized by the presence of numerous foliar oil glands that generally house mono- and sesquiterpenes. In some species, glands are also known to house substantial quantities of unrelated secondary meta- bolites such as volatile, aromatic β-triketones. It is not known if these compounds are co-housed with terpenes or if they are pro- duced in distinct, metabolically specialized glands. We showed that Eucalyptus brevistylis—a species with appreciable foliar quantities of both β-triketones and terpenes—contains two visually distinct gland types in leaves, one that is translucent and the other golden-brown. Gas chromatographic analyses of solvent extracts of the two gland types showed that the translucent glands contain sesquiterpene alcohol cubenols and cubebols (termed ‘sesquiterpene glands’), whereas the golden-brown glands contain predominantly the β-triketone conglomerone with lesser amounts of sesquiterpene hydrocarbon caryophyllenes (termed ‘trike- tone glands’). Analysis of leaves from trees of different ages, from young saplings through to advanced age trees, showed a grad- ual increase in the abundance of sesquiterpene glands relative to triketone glands as plants aged. Such ontogenetic regulation of foliar secondary metabolite concentration appears to be a common feature of Eucalyptus species, albeit at different temporal scales. A similar ontogenetic pattern was observed in ageing leaves, with mature leaves having a higher proportion of sesquiter- pene glands than young leaf tips. It is concluded that regulation of the relative abundances of the two gland types with ontogeny likely reflects the different herbivores present at the different life stages of leaves and whole plants. In particular, leaf tips and young plants may be advantaged by deploying higher amounts of insecticidal β-triketones. The concurrent deployment of two metabolically distinct gland types in leaves is a rare phenomenon and a novel finding for myrtaceous trees. Keywords: caryophyllene, conglomerone, cubebol, eucalypt, metabolomics, secretory cavity, sesquiterpene, terpene, terpen- oid, triketone. Introduction − between species with gland densities as high as 3400 cm 2 in Trees and shrubs from the genus Eucalyptus are characterized Eucalyptus protensa (Brooker and Nicolle 2013) and mean by the presence of numerous oil glands embedded within their gland volumes as large as 10 nl in Eucalyptus apiculata leaves. Each sub-dermal gland is a spherical, multi-cellular com- (Goodger et al. 2016). Consequently, terpenic oils can comprise plex composed of outer secretory cell layers surrounding a large over 6% leaf fresh weight in high oil-yielding species such as extra-cellular lumen (Carr and Carr 1970). The secretory cells Eucalyptus polybractea (Goodger et al. 2008). The constituent produce a range of mono- and sesquiterpene oils that are then terpenes housed in glands can also differ between Eucalyptus stored within the lumen. The number and size of glands vary species (Brophy et al. 1991, Brophy and Southwell 2002), and † These authors contributed equally to this work. © The Author(s) 2018. Published by Oxford University Press. All rights reserved. For Permissions, please email: [email protected] 1452 Goodger et al. impart distinctive aromas, some of which are valued for pharma- results were not consistent between all species, but did suggest ceutical, industrial and perfumery uses (Doran 1991). that at least in some species there is a level of metabolic special- Moreover, the different terpene profiles produced are thought to ization between the two embedded gland types. For example, serve important ecological roles, particularly as herbivore deter- the flavonoid rutin was detected only in dark glands of Hypericum rents (Harborne 1991, 2001) or as reducers of ozone toxicity maculatum and Hypericum erectum. Nonetheless, very low quan- (Li et al. 2018). tities of rutin were found in both dark and translucent glands of Individual foliar glands of Eucalyptus are known to contain Hypericum perforatum. The authors suggested the apparent lack mixtures of both monoterpenes and sesquiterpenes (King et al. of metabolic specialization in some species may have been arte- 2006), and analysis of extracts of bulk glands have also shown factual given the difficulty they had in imaging through the thick they can house substantial quantities of other chemicals such as leaf cuticles of those species (Kucharíková et al. 2016b). volatile, aromatic β-triketones, non-volatile flavanones or non- In this study, we determine if β-triketones and terpenes are Downloaded from https://academic.oup.com/treephys/article/38/10/1451/5055867 by guest on 27 September 2021 volatile monoterpene acid glucose esters (Heskes et al. 2012a, biosynthesized and stored in the same glands of a chosen Goodger et al. 2016). The monoterpene acid glucose esters Eucalyptus species or if there is metabolic specialization of gland have been better studied and are known to co-occur with terpe- types for the different compound classes. Volatile β-triketones nic oils in individual glands where they are localized to the outer have long been found in steam distillates of leaves from particu- region of lumena, with the terpenes more centrally located lar Eucalyptus species (Hellyer 1968, Brophy et al. 1991), but (Heskes et al. 2012a, 2012b). This unique extra-cellular spatial their specific localization to oil glands was only recently shown arrangement is thought to be mediated by the ampipathic nature (Goodger et al. 2016). The research by Goodger et al. (2016) of the compounds, being comprised of glucose centres and ter- used an enzymatic leaf digestion protocol to isolate glands and pene acid side groups, and may protect glandular secretory cells show the presence of the β-triketones conglomerone, agglomer- from the potentially auto-toxic terpenes stored within lumena one and iso-baeckeol methyl ether in Eucalyptus suberea glands (Goodger and Woodrow 2011). It is not known if flavanones or and conglomerone in Eucalyptus brevistylis glands. Similarly, the β-triketones are similarly housed together with oils in Eucalyptus use of Raman microscopy recently localized the β-triketone glands or if they are produced in distinct, metabolically specia- grandiflorone to the foliar glands of the myrtaceous shrub spe- lized glands. cies Leptospermum scoparium and Leptospermum morrisonii Such differential metabolic specialization of foliar oil glands (Killeen et al. 2015). Nevertheless, neither of those studies has not previously been observed in myrtaceous trees, but has showed if triketones co-occurred with oils in glands or if there been reported from a few herbaceous plants. The most definitive were two distinct types of glands responsible for the storage example comes from Salvia sclarea (clary sage; Lamiaceae), of triketones and terpenes, respectively. We chose to address which possess morphologically distinct peltate and capitate glan- this question using E. brevistylis as its glands are amenable to dular secreting trichomes (GSTs) protruding from epidermal isolation with the aforementioned enzymatic protocol and layers of above-ground organs. Gas chromatographic analysis of because extracts from bulk glands contained moderate individual GSTs collected from petal surfaces found capitate amounts of both triketones and terpenes, whereas those from glands mainly produce the monoterpene linalool together with E. suberea glands were almost exclusively comprised of trike- the diterpene sclareol, whereas peltate glands largely store the tones, with only very low amounts of sesquiterpenes detected sesquiterpene germacrene D (Schmiderer et al. 2008). Another (Goodger et al. 2016). Lamiaceae plant, Pogostemon cablin, possesses glandular tri- chomes on the surfaces of leaves and stems as well as internally Materials and methods embedded glands within the same tissues. Non-quantitative, histochemical characterization of the glandular constituents of Plant material both gland types similarly suggested metabolic specialization of Eucalyptus brevistylis Brooker (Rate’s tingle) is a large tree spe- gland types as staining was consistent with internal glands con- cies in the family Myrtaceae that is capable of growing up to taining lipids, flavones and terpenes and external GSTs housing 40 m tall (Brooker 1974). The species is endemic to the state of polysaccharides and terpenes (Guo et al. 2013). Western Australia (WA) where it holds the conservation status of Further evidence of metabolic specialization of gland types Priority 4: Rare, Near Threatened (Department of Parks and comes from Hypericum species (Hyperaceae) that contain two Wildlife 2015,
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