Yellow-Cedar, Callitropsis (Chamaecyparis) nootkatensis, Secondary Metabolites, Biological Activities, and Chemical Ecology

  • Joseph J. Karchesy
  • Rick G. Kelsey
  • M. P. González-Hernández
Review Article
  • 16 Downloads

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, mosquitoes, 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 

References

  1. Adams RP, Thomas P, Rushforth K (2007) The leaf essential oils of the new conifer genus, Xanthocyparis: Xanthocyparis vietnamensis and X. nootkatensis. J Essent Oil Res 19:30–33.  https://doi.org/10.1080/10412905.2007.9699223 CrossRefGoogle Scholar
  2. Addesso KM, Oliver JB, O’Neal PA, Youssef N (2017) Efficacy of nootka oil as a biopesticide for management of imported fire ants (Hymenoptera: Formicidae). J Econ Entomol 110:1547–1555.  https://doi.org/10.1093/jee/tox114 CrossRefPubMedGoogle Scholar
  3. Andersen NH (1970) Biogenetic implications of the antipodal sesquiterpenes of vetiver oil. Phytochemistry 9:145–151.  https://doi.org/10.1016/S0031-9422(00)86626-1 CrossRefGoogle Scholar
  4. Andersen NH, Syrdal D (1970) Terpenes and sesquiterpenes of Chamaecyparis nootkatensis leaf oil. Phytochemistry 9:1325–1340.  https://doi.org/10.1016/S0031-9422(00)85326-1 CrossRefGoogle Scholar
  5. Barton GM (1976) A review of yellow cedar (Chamaecyparis nootkatensis [D. Don] Spach) extractives and their importance to utilization. Wood Fiber 8:172–176Google Scholar
  6. Baser KHC (2008) Biological and pharmacological activities of carvacrol and carvacrol bearing essential oils. Curr Pharm Des 14:3106–3120.  https://doi.org/10.2174/138161208786404227 CrossRefPubMedGoogle Scholar
  7. Beekwilder J, van Houwelingen A, Cankar K, van Dijk ADJ, de Jong RM, Stoopen G, Bouwmeester H, Achkar J, Sonke T, Bosch D (2014) Valencene synthase from the heartwood of Nootka cypress (Callitropsis nootkatensis) for biotechnological production of valencene. Plant Biotechnol J 12:174–182.  https://doi.org/10.1111/pbi.12124 CrossRefPubMedGoogle Scholar
  8. Behle RW, Flor-Weiler LB, Bharadwaj A, Stafford KC III (2011) A formulation to encapsulate nootkatone for tick control. J Med Entomol 48:1120–1127.  https://doi.org/10.1603/ME10282 CrossRefPubMedGoogle Scholar
  9. Belt T, Keplinger T, Hänninen T, Rautkari L (2017) Cellular level distributions of scots pine heartwood and knot heartwood extractives revealed by Raman spectroscopy imaging. Ind Crop Prod 108:327–335.  https://doi.org/10.1016/j.indcrop.2017.06.056 CrossRefGoogle Scholar
  10. Bharadwaj A, Stafford KC III, Behle RW (2012) Efficacy and environmental persistence of nootkatone for the control of the blacklegged tick (Acari: Ixodidae) in residential landscapes. J Med Entomol 49:1035–1044.  https://doi.org/10.1603/ME11251 CrossRefPubMedGoogle Scholar
  11. Bicho JG, Zavarin E, Bhacca NS (1963) On the occurrence of hydronootkatinol in the heartwood of Cupressus lindleyi Klotsch. J Org Chem 28:2927–2929.  https://doi.org/10.1021/jo01045a538 CrossRefGoogle Scholar
  12. Buma B, Hennon PE, Harrington CA, Popkin JR, Krapek J, Lamb MS, Oakes LE, Saunders S, Zeglen S (2017) Emerging climate-driven disturbance processes: widespread mortality associated with snow-to-rain transitions across 10° of latitude and half the range of a climate-threatened conifer. Glob Chang Biol 23:2903–2914.  https://doi.org/10.1111/gcb.13555 CrossRefPubMedGoogle Scholar
  13. Cankar K, van Houwelingen A, Goedbloed M, Renirie R, de Jong RM, Bouwmeester H, Bosch D, Sonke T, Beekwilder J (2014) Valencene oxidase CYP706M1 from Alaska cedar (Callitropsis nootkatensis). FEBS Lett 588:1001–1007.  https://doi.org/10.1016/j.febslet.2014.01.061 CrossRefPubMedGoogle Scholar
  14. Carlsson B, Erdtman H, Frank A, Harvey WE (1952) The chemistry of the order Cupressales VIII. Heartwood constituents of Chamaecyparis nootkatensis. Carvacrol, nootkatin and chamic acid. Acta Chem Scand 6:690–696.  https://doi.org/10.3891/acta.chem.scand.06-0690 CrossRefGoogle Scholar
  15. Chavan PS, Tupe SG (2014) Antifungal activity and mechanism of action of carvacrol and thymol against vineyard and wine spoilage yeasts. Food Control 46:115–120.  https://doi.org/10.1016/j.foodcont.2014.05.007 CrossRefGoogle Scholar
  16. Cheng YS, von Rudloff E (1970a) The volatile oil of the leaves of Chamaecyparis nootkatensis. Phytochemistry 9:2517–2527.  https://doi.org/10.1016/S0031-9422(00)85772-6 CrossRefGoogle Scholar
  17. Cheng YS, von Rudloff E (1970b) Two new diterpenoid oxides from the leaf oil of Chamaecyparis nootkatensis. Tetrahedron Lett 11(14):1131–1132.  https://doi.org/10.1016/S0040-4039(01)97927-4 CrossRefGoogle Scholar
  18. Clark RH, Lucas CC (1926) The essential oil content of Chamaecyparis nootkatensis. Trans Roy Soc Can Sec III 20:423–428Google Scholar
  19. Constantine GH, Karchesy JJ, Franzblau SG, LaFleur LE (2001) (+)-Totarol from Chamaecyparis nootkatensis and activity against Mycobacterium tuberculosis. Fitoterapia 72:572–574.  https://doi.org/10.1016/S0367-326X(01)00272-6 CrossRefPubMedGoogle Scholar
  20. Cornelius ML, Bland JM, Daigle DJ, Williams KS, Lovisa MP, Connick WJ Jr, Lax AR (2004) Effect of a lignin-degrading fungus on feeding preferences of Formosan subterranean termite (Isoptera: Rhinotermitidae) for different commercial lumber. J Econ Entomol 97:1025–1035.  https://doi.org/10.1093/jee/97.3.1025 CrossRefPubMedGoogle Scholar
  21. DeGroot RC, Woodward B, Hennon PE (2000) Natural decay resistance of heartwood from dead, standing yellow-cedar trees: laboratory evaluations. For Prod J 50:53–59Google Scholar
  22. Dietrich G, Dolan MC, Peralta-Cruz J, Schmidt J, Piessman J, Eisen RJ, Karchesy JJ (2006) Repellent activity of fractioned compounds from Chamaecyparis nootkatensis essential oil against nymphal Ixodes scapularis (Acari: Ixodidae). J Med Entomol 43:957–961.  https://doi.org/10.1093/jmedent/43.5.957 CrossRefPubMedGoogle Scholar
  23. Dixon RA, Xie DY, Sharma SB (2005) Proanthocyanidins – a final frontier in flavonoid research? New Phytol 165:9–28.  https://doi.org/10.1111/j.1469-8137.2004.01217.x CrossRefPubMedGoogle Scholar
  24. Dolan MC, Jordan RA, Schulze TL, Schulze CJ, Manning MC, Ruffalo D, Schmidt JP, Piesman J, Karchesy JJ (2009) Ability of two natural products, nootkatone and carvacrol, to suppress Ixodes scapularis and Amblyomma americanum (Acari: Ixodidae) in a Lyme disease endemic area of New Jersey. J Econ Entomol 102:2316–2324.  https://doi.org/10.1603/029.102.0638 CrossRefPubMedGoogle Scholar
  25. Donlin MJ, Zunica A, Lipnicky A, Garimallaprabhakaran AK, Berkowitz AJ, Grigoryan A, Meyers MJ, Tavis JE, Murelli RP (2017) Troponoids can inhibit growth of the human fungal pathogen Cryptococcus neoformans. Antimicrob Agents Chemother 61:e02574-16.  https://doi.org/10.1128/AAC.02574-16 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Du T, Shupe TF, Hse CY (2011) Antifungal activities of three supercritical fluid extracted cedar oils. Holzforschung 65:277–284.  https://doi.org/10.1515/hf.2011.005 CrossRefGoogle Scholar
  27. Duff SR, Erdtman H (1953) Occurrence of carvacrol methyl ether in the heartwood of Chamaecyparis nootkatensis (lamb.) Spach. Chem Ind 747–748Google Scholar
  28. Duff SR, Erdtman H, Harvey WE (1954) The chemistry of the order Cupressales. XI. Heartwood constituents of Chamaecyparis nootkatensis (lamb.) Spach. Nootkatin. Acta Chem Scand 8:1073–1082CrossRefGoogle Scholar
  29. Erdtman H, Hirose Y (1962) Chemistry of natural order Cupressales 46. The structure of nootkatone. Acta Chem Scand 16:1311–1314.  https://doi.org/10.3891/acta.chem.scand.16-1311 CrossRefGoogle Scholar
  30. Erdtman H, Topliss JG (1957) The chemistry of the natural-order Cupressales XVIII. Nootkatene, a new sesquiterpene type hydrocarbon from the heartwood of Chamaecyparis nootkatensis (lamb.) Spach. Acta Chem Scand 11:1157–1161.  https://doi.org/10.3891/acta.chem.scand.11-1157 CrossRefGoogle Scholar
  31. Erdtman H, Harvey WE, Topliss JG (1956) The chemistry of the natural order Cupressales XVI. Heartwood constituents of Chamaecyparis nootkatensis (lamb.) Spach. The structure of chamic and chaminic acids. Acta Chem Scand 10:1381–1392.  https://doi.org/10.3891/acta.chem.scand.10-1381 CrossRefGoogle Scholar
  32. European and Mediterranean Plant Protection Organization (2017) WebCite® 2017–11-06. https://www.eppo.int/QUARANTINE/Alert_List/fungi/PHYTRA.htm. Accessed 6 Nov 2017. (Archived by WebCite®at http://www.webcitation.org/6umGfe1P4)
  33. Federal Laboratory Consortium for Technology Transfer (FLC) (2018) Formulation of nootkatone as repellent and pesticide products against mosquitoes and ticks. https://www.federallabs.org/successes/success-stories/formulation-of-nootkatone-as-repellent-and-pesticide-products-against. Accessed 5 Feb 2018
  34. Flor-Weiler LB, Behle RW, Stafford KC III (2011) Susceptibility of four tick species, Amblyomma americanum, Dermacentor variabilis, Ixodes scapularis, and Rhipicephalus sanguineus (Acari: Ixodidae), to nootkatone from essential oil of grapefruit. J Med Entomol 48:322–326.  https://doi.org/10.1603/ME10148 CrossRefPubMedGoogle Scholar
  35. Foster AJ, Aloni R, Fidanza M, Gries R, Gries G, Mattsson J (2016) Foliar phase changes are coupled with changes in storage and biochemistry of monoterpenoids in western redcedar (Thuja plicata). Trees 30:1361–1375.  https://doi.org/10.1007/s00468-016-1373-x CrossRefGoogle Scholar
  36. Fraatz MA, Berger RG, Zorn H (2009) Nootkatone-a biotechnological challenge. Appl Microbiol Biotechnol 83:35–41.  https://doi.org/10.1007/s00253-009-1968-x CrossRefPubMedGoogle Scholar
  37. Franceschi VR, Krokene P, Christiansen E, Krekling T (2005) Anatomical and chemical defenses of conifer bark against bark beetles and other pests. New Phytol 167:353–375.  https://doi.org/10.1111/j.1469-8137.2005.01436.x CrossRefPubMedGoogle Scholar
  38. Frankel SJ, Palmieri KM (2014) Sudden oak death, Phytophthora ramorum: A persistent threat to oaks and other tree species Internat Oaks No 25:43–56Google Scholar
  39. Grace JK, Yamamoto RT (1994) Natural resistance of Alaska-cedar, redwood, and teak to Formosan subterranean termites. For Prod J 44:41–45Google Scholar
  40. Harris AS (1990) Chamaecyparis nootkatensis (D. Don) Spach Alaska-cedar. In: Burns RM, Honkala BH (tech Coord) silvics of North America: 1. Conifers.; USDA for Serv, Washington DC, pp 97–102Google Scholar
  41. Hennon PE (1991) Diseases, insects, and animal damage of yellow cypress. In: Lousier JD (ed) Yellow cypress: can we grow it? Can we sell it? Forestry Canada, British Columbia Ministry of Forests, FRDA report 171, pp 36–43Google Scholar
  42. Hennon PE, Shaw CGIII, Hansen EM (1990) Dating decline and mortality of Chamaecyparis nootkatensis in Southeast Alaska. For Sci 36:502–515Google Scholar
  43. Hennon P, Woodward B, Lebow P (2007) Deterioration of wood from live and dead Alaska yellow-cedar in contact with soil. For Prod J 57:23–30Google Scholar
  44. Hennon PE, McKenzie CM, D’Amore DV, Wittwer DT, Mulvey RL, Lamb MS, Biles FE, Cronn RC (2016) A climate adaptation strategy for conservation and management of yellow-cedar in Alaska. Gen Tech Rep PNW-GTR-917. Portland, OR: U.S. Department of Agriculture, Forest Service, Pacific Northwest Research StationGoogle Scholar
  45. Imai T, Tanabe K, Kato T, Fukushima K (2005) Localization of ferruginol, a diterpene phenol, in Cryptomeria japonica heartwood by time-of-flight secondary ion mass spectrometry. Planta 221:549–556.  https://doi.org/10.1007/s00425-004-1476-2 CrossRefPubMedGoogle Scholar
  46. Johnston WH, Karchesy JJ, Constantine GH, Craig AM (2001) Antimicrobial activity of some Pacific northwest woods against anaerobic bacteria and yeast. Phytother Res 15:586–588.  https://doi.org/10.1002/ptr.765 CrossRefPubMedGoogle Scholar
  47. Jordan RA, Dolan MC, Piesman J, Schulze TL (2011) Suppression of host-seeking Ixodes scapularis and Amblyomma americanum (Acari: Ixodidae) nymphs after dual applications of plant-derived acaricides in New Jersey. J Econ Entomol 104:659–664.  https://doi.org/10.1603/EC10340 CrossRefPubMedGoogle Scholar
  48. Jordan RA, Schulze TL, Dolan MC (2012) Efficacy of plant-derived and synthetic compounds on clothing as repellents against Ixodes scapularis and Amblyomma americanum (Acari: Ixodidae). J Med Entomol 49:101–106.  https://doi.org/10.1603/ME10241 CrossRefPubMedGoogle Scholar
  49. Jozsa LA (1991) Yellow cypress trivia. In: Lousier JD (ed) Yellow cypress: can we grow it? Can we sell it? Forestry Canada, British Columbia Ministry of Forests, FRDA report 171, pp 13–15Google Scholar
  50. Karchesy YM, Kelsey RG, Constantine G, Karchesy JJ (2016) Biological screening of selected Pacific northwest forest plants using the brine shrimp (Artemia salina) toxicity bioassay. Springer Plus 5:510.  https://doi.org/10.1186/s40064-016-2145-1 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Kelsey RG, Hennon PE, Huso M, Karchesy JJ (2005) Changes in heartwood chemistry of dead yellow-cedar trees that remain standing for 80 years or more in Southeast Alaska. J Chem Ecol 31:2653–2670.  https://doi.org/10.1007/s10886-005-7618-6 CrossRefPubMedGoogle Scholar
  52. Kelsey RG, González-Hernández MP, Karchesy J, Veluthoor S (2015) Volatile terpenoids and tropolones in heartwood extracts of yellow-cedar, Monterey cypress, and their hybrid Leyland cypress. Ann For Sci 72:349–355.  https://doi.org/10.1007/s13595-014-0429-6 CrossRefGoogle Scholar
  53. Khasawneh MA, Karchesy JJ (2011) Terpenoids of the heartwood of Chamaecyparis nootkatensis. Am J Org Chem 1:1–5.  https://doi.org/10.5923/j.ajoc.20110101.01 CrossRefGoogle Scholar
  54. Khasawneh MA, Xiong Y, Peralta-Cruz J, Karchesy JJ (2011) Biologically important eremophilane sesquiterpenes from Alaska cedar heartwood essential oil and their semi-synthetic derivatives. Molecules 16:4775–4785.  https://doi.org/10.3390/molecules16064775 CrossRefPubMedGoogle Scholar
  55. Kimball BA, Russell JH, Ott PK (2012) Phytochemical variation within a single plant species influences foraging behavior of deer. Oikos 121:743–751.  https://doi.org/10.1111/j.1600-0706.2011.19515.x CrossRefGoogle Scholar
  56. Kirker GT, Bishell AB, Lebow PK (2016) Laboratory evaluations of durability of southern pine pressure treated with extractives from durable wood species. J Econ Entomol 109:259–266.  https://doi.org/10.1093/jee/tov286 CrossRefPubMedGoogle Scholar
  57. Kirker GT, Blodgett AB, Arango RA, Lebow PK, Clausen CA (2013) The role of extractives in naturally durable wood species. Int Biodeter Biodegrad 82:53–58.  https://doi.org/10.1016/j.ibiod.2013.03.007 CrossRefGoogle Scholar
  58. Kuroda K, Fujiwara T, Hashida K, Imai T, Kushi M, Saito K, Fukushima K (2014) The accumulation pattern of ferruginol in the heartwood-forming Cryptomeria japonica xylem as determined by time-of-flight secondary ion mass spectrometry and quantity analysis. Ann Bot 113:1029–1036.  https://doi.org/10.1093/aob/mcu028 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Leonhardt RH, Berger RG (2015) Nootkatone. Adv Biochem Eng Biotechnol 148:391–404.  https://doi.org/10.1007/10_2014_279 PubMedGoogle Scholar
  60. Liang B, Zheng C (1992) Studies on chemical constituents of volatile oil from the fruits and shells of Alpinia oxyphylia Miq. Nat Prod Res Dev 4:18–26.  https://doi.org/10.16333/j.1001-6880.1992.03.004 Google Scholar
  61. Lima IO, Pereira FO, de Oliveira WA, Lima EO, Menezes EA, Cunha FA, Diniz MFFM (2013) Antifungal activity and mode of action of carvacrol against Candida albicans strains. J Essent Oil Res 25:138–142.  https://doi.org/10.1080/10412905.2012.754728 CrossRefGoogle Scholar
  62. MacLeod WD Jr (1965) The constitution of nootkatone, nootkatene, and valencene. Tetrahedron Lett 6(52):4779–4783.  https://doi.org/10.1016/S0040-4039(01)89034-1 CrossRefGoogle Scholar
  63. MacLeod WD Jr, Buigues NM (1964) Sesquiterpenes. I. Nootkatone, a new grapefruit flavor constituent. J Food Sci 29:565–568.  https://doi.org/10.1111/j.1365-2621.1964.tb00411.x CrossRefGoogle Scholar
  64. Manter DK, Karchesy JJ, Kelsey RG (2006) The sporicidal activity of yellow-cedar heartwood, essential oil and wood constituents toward Phytophthora ramorum in culture. For Pathol 36:297–308.  https://doi.org/10.1111/j.1439-0329.2006.00461.x CrossRefGoogle Scholar
  65. Manter DK, Kelsey RG, Karchesy JJ (2007) Antimicrobial activity of extractable conifer heartwood compounds toward Phytophthora ramorum. J Chem Ecol 33:2133–2147.  https://doi.org/10.1007/s10886-007-9368-0 CrossRefPubMedGoogle Scholar
  66. McAllister JC, Adams MF (2010) Mode of action for natural products isolated from essential oils of two trees is different from available mosquito adulticides. J Med Entomol 47:1123–1126.  https://doi.org/10.1603/ME10098 CrossRefPubMedGoogle Scholar
  67. Meck C, D’Erasmo MP, Hirsch DR, Murelli RP (2014) The biology and synthesis of α-hydroxytropolones. Med Chem Commun 5:842–852.  https://doi.org/10.1039/C4MD00055B CrossRefGoogle Scholar
  68. Michener DC (1993) Chamaecyparis. In: Flora of North America editorial committee (eds) Flora of North America. North of Mexico, vol 2. Pterodphytes and gymnsperms, Oxford University Press, New York and Oxford, pp 408–410Google Scholar
  69. Morales-Ramos JA, Rojas MG (2001) Nutritional ecology of the Formosan subterranean termite (Isoptera: Rhinotermitidae): feeding response to commercial wood species. J Econ Entomol 94:516–523.  https://doi.org/10.1603/0022-0493-94.2.516 CrossRefPubMedGoogle Scholar
  70. Morales-Ramos JA, Rojas MG, Hennon PE (2003) Black-staining fungus effects on the natural resistance properties of Alaskan yellow cedar to the Formosan subterranean termite (Isoptera: Rhinotermitidae). Environ Entomol 32:1234–1241.  https://doi.org/10.1603/0046-225X-32.5.1234 CrossRefGoogle Scholar
  71. Norin T (1964a) The absolute configuration of chamic, chaminic, and isochamic acids. Arkiv för Kemi, Stockholm 22:123–128Google Scholar
  72. Norin T (1964b) Chanootin, a bicyclic C15 tropolone from the heartwood of Chamaecyparis nootkatensis (lamb.) Spach. Arkiv för Kemi, Stockholm 22:129–135Google Scholar
  73. Palá-Paúl J, Usano-Alemany J, Granda E, Soria AC (2009) Chemical composition, antifungal and antibacterial activity of the essential oil of Chamaecyparis nootkatensis from Spain. Nat Prod Commun 4:1007–1010PubMedGoogle Scholar
  74. Panella NA, Karchesy J, Maupin GO, Malan JCS, Piesman J (1997) Susceptibility of immature Ixodes scapularis (Acari: Ixodidae) to plant-derived acaricides. J Med Entomol 34:340–345.  https://doi.org/10.1093/jmedent/34.3.340 CrossRefPubMedGoogle Scholar
  75. Panella NA, Dolan MC, Karchesy JJ, Xiong Y, Peralta-Cruz J, Khasawneh M, Montenieri JA, Maupin GO (2005) Use of novel compounds for pest control: insecticidal and acaricidal activity of essential oil components from heartwood of Alaska yellow cedar. J Med Entomol 42:352–358.  https://doi.org/10.1093/jmedent/42.3.352 CrossRefPubMedGoogle Scholar
  76. Pettit GR, Tan R, Northen JS, Herald DL, Chapuis JC, Pettit RK (2004) Antineoplastic agents. 529. Isolation and structure of nootkastatins 1 and 2 from the Alaskan yellow cedar Chamaecyparis nootkatensis. J Nat Prod 67:1476–1482.  https://doi.org/10.1021/np0304161 CrossRefPubMedGoogle Scholar
  77. Piesman J (2006) Response of nymphal Ixodes scapularis, the primary tick vector of Lyme disease spirochetes in North America, to barriers derived from wood products or related home and garden items. J Vector Ecol 31:412–417.  https://doi.org/10.3376/1081-1710(2006)31%5B412:RONIST%5D2.0.CO;2 CrossRefPubMedGoogle Scholar
  78. Rennerfelt E, Nacht G (1955) The fungicidal activity of some constituents from heartwood of conifers. Sven Bot Tidskr 49:419–432Google Scholar
  79. Rosales-Castro M, González-Laredo RF, Bae YS, Kim JK, Morre J, Karchesy JJ (2014) Characterization and antioxidant properties of the condensed tannins from Alaska cedar inner bark. Rec Nat Prod 8:217–227Google Scholar
  80. Russell JH, Ferguson DC (2010) Western redcedar browse resistance breeding and deployment material. In: Harrington CA (tech coord), a tale of two cedars – international symposium on western redcedar and yellow-cedar, USDA for Serv, PNW Res Sta gen tech rep PNW-GTR-828. Portland, Oregon, pp 160–162Google Scholar
  81. Russell J, Kimball B (2010) Summary of western redcedar browse resistance research. In: Harrington CA (tech coord), a tale of two cedars – international symposium on western redcedar and yellow-cedar, USDA for Serv, PNW Res Sta gen tech rep PNW-GTR-828. Portland, Oregon, pp 163–165Google Scholar
  82. Saniewska M, Saniewska A, Kanlayanarat S (2007) Biological activities of tropolone and hinokitiol: the tools in plant physiology and their practical use. Acta Hort 755:133–142CrossRefGoogle Scholar
  83. Saniewska M, Horbowicz M, Kanlayanarat S (2014) The biological activities of troponoids and their use in agriculture. J Hort Res 22:5–19.  https://doi.org/10.2478/johr-2014-0001 Google Scholar
  84. Scheffer TC, Cowling EB (1966) Natural resistance of wood to microbial deterioration. Annu Rev Phytopathol 4:147–170.  https://doi.org/10.1146/annurev.py.04.090166.001051 CrossRefGoogle Scholar
  85. Scheffer TC, Morrell JJ (1998) Natural durability of wood: a worldwide checklist of species. Oregon State Univ, For Res Lab, Res Contrib 22Google Scholar
  86. Schulze TL, Jordan RA, Dolan MC (2011) Experimental use of two standard tick collection methods to evaluate the relative effectiveness of several plant-derived and synthetic repellents against Ixodes scapularis and Amblyomma americanum (Acari: Ixodidae). J Econ Entomol 104:2062–2067.  https://doi.org/10.1603/EC10421 CrossRefPubMedGoogle Scholar
  87. Smith RS (1970) Black stain in yellow cedar heartwood. Can J Bot 48:1731–1739.  https://doi.org/10.1139/b70-256 CrossRefGoogle Scholar
  88. Smith RS, Cserjesi AJ (1970) Degradation of nootkatin by fungi causing black heartwood stain in yellow cedar. Can J Bot 48:1727–1729.  https://doi.org/10.1139/b70-255 CrossRefGoogle Scholar
  89. Stewart H (1984) Cedar: tree of life to the northwest coast Indians. Douglas & McIntyre, VancouverGoogle Scholar
  90. Taylor AM, Gartner BL, Morrell JJ, Tsunoda K (2006) Effects of heartwood extractive fractions of Thuja plicata and Chamaecyparis nootkatensis on wood degradation by termites or fungi. J Wood Sci 52:147–153.  https://doi.org/10.1007/s10086-005-0743-6 CrossRefGoogle Scholar
  91. Tsoyi K, Jang HJ, Lee YS, Kim YM, Kim HJ, Seo HG, Lee JH, Kwak JH, Lee DU, Chang KC (2011) (+)-Nootkatone and (+)-valencene from rhizomes of Cyperus rotundus increase survival rates in septic mice due to heme oxygenase-1 induction. J Ethnopharmacol 137:1311–1317.  https://doi.org/10.1016/j.jep.2011.07.062 CrossRefPubMedGoogle Scholar
  92. Turner NC, Bell MAM (1973) The ethnobotany of the southern Kwakiutl Indians of British Columbia. Econ Bot 27:257–310.  https://doi.org/10.1007/BF02907532 CrossRefGoogle Scholar
  93. Ultee A, Bennik MHJ, Moezelaar R (2002) The phenolic hydroxyl group of carvacrol is essential for action against the food-borne pathogen Bacillus cereus. Appl Environ Microbiol 68:1561–1568.  https://doi.org/10.1128/AEM.68.4.1561-1568.2002 CrossRefPubMedPubMedCentralGoogle Scholar
  94. Urzúa A, Rezende MC, Mascayano C, Vásquez L (2008) A structure-activity study of antibacterial diterpenoids. Molecules 13:882–891.  https://doi.org/10.3390/molecules13040822 CrossRefPubMedGoogle Scholar
  95. Velasco-Negueruela A, Pérez-Alonso MJ (1990) The volatiles of six Teucrium species from the Iberian peninsula and the Balearic Islands. Phytochemistry 29:1165–1169.  https://doi.org/10.1016/0031-9422(90)85421-B CrossRefGoogle Scholar
  96. Veldhuizen EJA, Tjeerdsma-van Bokhoven JLM, Zweijtzer C, Burt SA, Haagsman HP (2006) Structural requirements for the antimicrobial activity of carvacrol. J Agric Food Chem 54:1874–1879.  https://doi.org/10.1021/jf052564y CrossRefPubMedGoogle Scholar
  97. Vourc’h G, Russell J, Martin JL (2002) Linking deer browsing and terpene production among genetic identities in Chamaecyparis nootkatensis and Thuja plicata (Cupressaceae). J Hered 93:370–373.  https://doi.org/10.1093/jhered/93.5.370 CrossRefGoogle Scholar
  98. Wheeler EA, Arnette CG Jr (1994) Identification of Neogene woods from Alaska-Yukon. Quat Int 22/23:91–102.  https://doi.org/10.1016/1040-6182(94)90008-6 CrossRefGoogle Scholar
  99. Wriessnegger T, Augustin P, Engleder M, Leitner E, Müller M, Kaluzna I, Schürmann M, Mink D, Zellnig G, Schwab H, Pichler H (2014) Production of the sesquiterpenoid (+)-nootkatone by metabolic engineering of Pichia pastoris. Metab Eng 24:18–29.  https://doi.org/10.1016/j.ymben.2014.04.001 CrossRefPubMedGoogle Scholar
  100. Zavarin E, Smith LV, Bicho JG (1967) Tropolones of Cupressaceae-III. Phytochemistry 6:1387–1394.  https://doi.org/10.1016/S0031-9422(00)82881-2 CrossRefGoogle Scholar
  101. Zhao J (2007) Plant troponoids: chemistry, biological activity, and biosynthesis. Curr Med Chem 14:2597–2621.  https://doi.org/10.2174/092986707782023253 CrossRefPubMedGoogle Scholar
  102. Zhu BCR, Henderson G, Chen F, Maistrello L, Laine RA (2001) Nootkatone is a repellent for formosan subterranean termite (Coptotermes formosanus). J Chem Ecol 27:523–531.  https://doi.org/10.1023/A:1010301308649 CrossRefPubMedGoogle Scholar
  103. Zhu BCR, Henderson G, Sauer AM, Crowe W, Laine RA (2010) Structural requirements for repellency: norsesquiterpenes and sesquiterpenoid derivatives of nootkatone against the Formosan subterranean termite (Isoptera:Rhinotermitidae). Pest Manag Sci 66:875–878.  https://doi.org/10.1002/ps.1956 PubMedGoogle Scholar
  104. Zulak KG, Bohlmann J (2010) Terpenoid biosynthesis and specialized vascular cells of conifer defense. J Integr Plant Biol 52:86–97.  https://doi.org/10.1111/j.1744-7909.2010.00910.x CrossRefPubMedGoogle Scholar
  105. Zviely M (2009) Molecule of the month: Nootkatone. Perf Flav 34:20–22Google Scholar

Copyright information

© 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

Authors and Affiliations

  • Joseph J. Karchesy
    • 1
  • Rick G. Kelsey
    • 2
  • M. P. González-Hernández
    • 3
  1. 1.Wood Science and EngineeringOregon State UniversityCorvallisUSA
  2. 2.USDA Forest ServicePacific Northwest Research StationCorvallisUSA
  3. 3.Department of Crop Production and Projects of EngineeringSantiago de Compostela UniversityLugoSpain

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