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Nootkatensis, Secondary Metabolites, Biological Activities, and Chemical Ecology

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Nootkatensis, Secondary Metabolites, Biological Activities, and Chemical Ecology Journal of Chemical Ecology (2018) 44:510–524 https://doi.org/10.1007/s10886-018-0956-y REVIEW ARTICLE Yellow-Cedar, Callitropsis (Chamaecyparis) nootkatensis, Secondary Metabolites, Biological Activities, and Chemical Ecology Joseph J. Karchesy1 & Rick G. Kelsey2 & M. P. González-Hernández3 Received: 22 December 2017 /Revised: 26 March 2018 /Accepted: 28 March 2018 /Published online: 14 April 2018 # This is a U.S. government work and its text is not subject to copyright protection in the United States; however, its text may be subject to foreign copyright protection 2018 Abstract Yellow-cedar, Callitropsis nootkatensis, is prevalent in coastal forests of southeast Alaska, western Canada, and inland forests along the Cascades to northern California, USA. These trees have few microbial or animal pests, attributable in part to the distinct groups of biologically active secondary metabolites their tissues store for chemical defense. Here we summarize the new yellow-cedar compounds identified and their biological activities, plus new or expanded activities for tissues, extracts, essential oils and previously known compounds since the last review more than 40 years ago. Monoterpene hydrocarbons are the most abundant compounds in foliage, while heartwood contains substantial quantities of oxygenated monoterpenes and oxygenated sesquiterpenes, with one or more tropolones. Diterpenes occur in foliage and bark, whereas condensed tannins have been isolated from inner bark. Biological activities expressed by one or more compounds in these groups include fungicide, bactericide, sporicide, acaricide, insecticide, general cytotoxicity, antioxidant and human anticancer. The diversity of organisms impacted by whole tissues, essential oils, extracts, or individual compounds now encompasses ticks, fleas, termites, ants, mos- quitoes, bacteria, a water mold, fungi and browsing animals. Nootkatone, is a heartwood component with sufficient activity against arthropods to warrant research focused toward potential development as a commercial repellent and biopesticide for ticks, mosquitoes and possibly other arthropods that vector human and animal pathogens. Keywords Nootkatone . Chemical defense . Repellents . Biopesticides . Monoterpenes . Sesquiterpenes . Tropolones . Tannins Introduction coastal forests of southeast Alaska and British Columbia, with a southern extension primarily in the Cascade Range through Yellow-cedar, Callitropsis nootkatensis (D.Don)Oerst.exD.P. WashingtonandOregontonorthernCalifornia,whereittypi- Little, also known as Alaska cedar, Alaska yellow-cedar or cally grows above 600 m (Harris 1990;Hennonetal.2016). Nootka cypress, is an ecologically and economically important Investigations of yellow-cedar secondary metabolites have conifer in the Cupressaceae family that indigenous people have been ongoing for nearly a century, beginning with the isolation valued and used for centuries as a material resource (Hennon of α-andβ-pinene (Fig. 1) from foliage essential oil with other et al. 2016;Stewart1984). It is naturally most abundant in the monoterpenes not fully characterized (Clark and Lucas 1926). Subsequent investigations of the leaf essential oil by gas-liquid chromatography (GC) found (−)-α-pinene, (+)-δ-3-carene and * Rick G. Kelsey (+)-limonene to be the major components (Fig. 1) with several [email protected] additional monoterpenes in lower quantities (Andersen and Syrdal 1970; Cheng and von Rudloff 1970a). Sesquiterpenes, 1 Wood Science and Engineering, Oregon State University, diterpenes, n-alkanes, alkanals, and esters of short chain (C4, Corvallis, OR 97331, USA C5) acids also occur in foliage oil, but usually in low abundance 2 USDA Forest Service, Pacific Northwest Research Station, (trace-0.5%, Cheng and von Rudloff 1970a, b). Initial studies of Corvallis, OR 97331, USA heartwood essential oils identified five monoterpenes (Fig. 1,), 3 Department of Crop Production and Projects of Engineering, carvacrol, methyl carvacrol, chamic acid, isochamic acid and Santiago de Compostela University, 27002 Lugo, Spain chaminic acid (Carlsson et al. 1952; Duff and Erdtman 1953; J Chem Ecol (2018) 44:510–524 511 Fig. 1 Monoterpenes in tissues of yellow-cedar. Compounds in the top two rows occur only in foliage, except α-terpineol and terpinen-4-ol that sometimes are found in heartwood. Compounds in the last two rows have been reported only in heartwood Erdtman et al. 1956;Norin1964a), two tropolones (Fig. 2), Fungal bioassays with some of these compounds began as nootkatin and chanootin (Carlsson et al. 1952; Duff et al. sufficient quantities were isolated and purified. Nootkatin con- 1954,Norin1964b), and two sesquiterpenes, nootkatene and centrations of 0.001–0.002% inhibited eight out of 12 fungal nootkatone (Erdtman and Topliss 1957; Erdtman and Hirose species growing on agar, and it was fungicidal to seven of the 1962;MacLeod1965). taxa at 0.001–0.005% (Rennerfelt and Nacht 1955). In the 512 J Chem Ecol (2018) 44:510–524 1993), however further details about their biochemistry and storage of monoterpenes relative to leaf morphology, age, etc. as observed in western redcedar (Foster et al. 2016)remainto be determined. Foliage Monoterpenes dominating yellow-cedar foliage have been studied further. Leaf essential oil from trees growing in their native range contain primarily limonene (35.4–42.2%), and lesser quantities of δ-3-carene (11.5–23.4%), α-pinene (8.7–16.3%), and sabinene (0.2–10.5%), with 0.4–0.9% ses- quiterpenes and 5.0–7.4% diterpenes (Adams et al. 2007). Outside its native environment in Spain the essential oil from young stems and leaves contain higher quantities of limonene (53.2%), similar proportions of δ-3-carene (21.0%), α-pinene (12.2%), and myrcene (6.1%), but considerably lower levels of sesquiterpenes (0.1%) and diterpenes (0.3%, Palá-Paúl et al. 2009). None of the major foliage components occur in other tissues, but there are five less abundant foliage com- pounds also in heartwood, two monoterpenes (terpinen-4-ol, and α-terpineol) and three sesquiterpenes (α-cadinol, δ- cadinene, and β-bisabolene). When present in foliage their ≤ Fig. 2 Tropolones that may occur in yellow-cedar heartwood concentrations are typically 0.7% (Adams et al. 2007; Andersen and Syrdal 1970; Cheng and von Rudloff 1970a; Palá-Paúl et al. 2009), and when present in heartwood oils or same study, chamic acid inhibited growth for six fungal spe- extracts they are usually ≥1.0% (Addesso et al. 2017; Kelsey cies at 0.01–0.02% and was fungicidal for two species at the et al. 2015; Khasawneh et al. 2011;Manteretal.2007). same concentrations. Wood infused with 1.1–1.2% nootkatin or carvacrol, or 1.0% carvacrol was protected from decay with Heartwood Several new compounds have been isolated from varying levels of efficacy, depending on the fungal species yellow-cedar heartwood since Barton’s(1976) review, includ- (Scheffer and Cowling 1966). In addition, yellow-cedar heart- ing two new oxygenated monoterpenes (1S)-2-oxo-3-p- wood blocks containing a natural mix of these compounds at menthenol and (4R)-4-hydroxy-4-isopropylcyclohex-1- their constitutive concentrations resisted decay from several enecarboxylic acid (Fig. 1) obtained from a methanol extract fungal species (Smith 1970; Smith and Cserjesi 1970). (Khasawneh et al. 2011). Four new sesquiterpenes have been The focus of this synthesis is on biological activities of new identified, although all were previously known in the litera- yellow-cedar compounds, and new or expanded activities for ture. Nootkatol, and valencene-13-ol were isolated from steam nootkatone and other previously known compounds, extracts, distilled essential oil (Khasawneh et al. 2011), while essential oils, and tissues reported since Barton’s(1976)re- valencene-11, 12-diol (syn tedonodiol) and kudtdiol (Fig. 3) view. Emphasis is placed on chemical studies linked closely to were isolated from a methanol extract (Khasawneh and yellow-cedar. It is not an exhaustive assessment of all biolog- Karchesy 2011). The absolute stereochemistry for nootkatol ical activities tested for each compound, since many occur in was resolved (Khasawneh et al. 2011), and both nootkatol and other plant species, are commercially available, or synthesized epi-nootkatol were detected in heartwood ethyl acetate ex- by the investigators. tracts by GC analysis (Kelsey et al. 2015). Heartwood essential oil analyzed by GC contained carva- crol (35.4%) as the major component, followed by four ses- Tissue Chemical Composition quiterpenes (Fig. 3), nootkatene (20.1%), nootkatone (17.4%), valencene-13-ol (6.4%) and nootkatol (5.2%) and the Conifer tissues often store constitutive defense chemicals in tropolone, nootkatin (3.5%, Khasawneh et al. 2011). specialized ducts or glands to limit their interference with life Heartwood ethyl acetate extracts analyzed by GC contained sustaining metabolic functions (Foster et al. 2016; Franceschi valencene-11, 12-diol (16.8%), nootkatol (10.6%), et al. 2005; Zulak and Bohlmann 2010). Yellow-cedar outer nootkatone (8.2%), valencene-13-ol (7.3%), carvacrol bark and phloem have resin ducts (Hennon et al. 2016), but the (7.1%) and nootkatin (6.4%, Kelsey et al. 2015). The same sapwood and heartwood do not (Wheeler and Arnette 1994). study reported additional tropolones, procerin (5.7%), a pos- The scale-like leaves are occasionally glandular (Michener sible procerin isomer (0.7%), and hinokitiol (β-thujaplicin, J Chem Ecol (2018) 44:510–524 513 Fig. 3 Sesquiterpenes in yellow-cedar heartwood. The bottom
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