Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE

A molecular perspective on terpene variation in Australian Myrtaceae

Andras Keszei A , Curt L. Brubaker B C and William J. Foley D
+ Author Affiliations
- Author Affiliations

A School of Botany and Zoology, Australian National University, Canberra, ACT 0200, Australia.

B CSIRO Division of Plant Industry, Black Mountain, Canberra, ACT 2601, Australia.

C Present address: Bayer BioScience N.V., Technologiepark 38 B-9052, Gent, Belgium.

D Corresponding author. Email: william.foley@anu.edu.au

Australian Journal of Botany 56(3) 197-213 https://doi.org/10.1071/BT07146
Submitted: 1 August 2007  Accepted: 24 December 2007   Published: 21 May 2008

Abstract

The terpenoid-dominated essential oils in Australian Myrtaceae mediate many ecological interactions and are important industrially. Of all the significant essential oil-producing families, Myrtaceae is the only one for which there is no molecular information on terpene biosynthesis. Here we summarise available knowledge on terpene biosynthesis and its relevance to the Myrtaceae to provide a foundation for ecological and genetic studies of chemical diversity. There are several steps in the terpene biosynthesis pathway that have potential for influencing the oil yield, profile and composition of leaf oils in Myrtaceae. The biochemical steps that influence oil yield in Myrtaceae probably occur in the steps of the pathway leading up to the synthesis of the terpene backbone. Qualitative differences in oil profiles are more likely to be due to variation in terpene synthases and terpene-modifying enzymes. Most of the information on molecular variation in terpene biosynthesis is based on the analysis of artificially derived mutants but Australian Myrtaceae can provide examples of the same mechanisms in an ecological context.


Acknowledgements

Comments by Rose Andrew, Erich Lassak and anonymous reviewers improved this manuscript significantly. We are grateful to Charles Cornwell, Erich Lassak, Joe Brophy, Noel Davies, Jonathan Gershenzon and Jörg Degenhardt for enjoyable discussions of terpene metabolism. This work was supported by a grant from the Australian Research Council to William J. Foley and by Andras Keszei who was supported by an International Postgraduate Research Award from the Australian National University.


References


Allen BE, Banthorpe DV (1981) Partial purification and properties of prenyltransferase from Pisum sativum. Phytochemistry 20, 35–40.
CrossRef |

Alves MDC, Medeiros S, Innecco R, Torres SB (2004) Allelopathy of plant volatile extracts on seed germination and radicle length of lettuce. Pesquisa Agropecuaria Brasileira 39, 1083–1086.

Anon. (2004) Opinion on Tea Tree Oil. Scientific Committee on Consumer Products. Opinion Number SCCP/08438/04. European Commission Health & Consumer Protection Directorate-General, Brussels.

Asante KS, Brophy JJ, Doran JC, Goldsack RJ, Hibbert DB, Larmour JS (2001) A comparative study of the seedling leaf oils of the spotted gums: species of the Corymbia (Myrtaceae) Section Politaria. Australian Journal of Botany 49, 55–66.
CrossRef |

Aubourg S, Lecharny A, Bohlmann J (2002) Genomic analysis of the terpenoid synthase (AtTPS) gene family of Arabidopsis thaliana. Molecular Genetics and Genomics 267, 730–745.
CrossRef | PubMed |

Back KW, He SL, Kim KU, Shin DH (1998) Cloning and bacterial expression of sesquiterpene cyclase a key branch point enzyme for the synthesis of sesquiterpenoid phytoalexin capsidiol in UV-challenged leaves of Capsicum annuum. Plant & Cell Physiology 39, 899–904.
PubMed |


Barnola LF, Hasegawa M, Cedeno A (1994) Monoterpene and sesquiterpene variation in Pinus caribaea needles and its relationship to Atta laevigata herbivory. Biochemical Systematics and Ecology 22, 437–445.
CrossRef |

Bell SJ, Barton AFM, Stocker LJ (2001) Agriculture for health and profit in Western Australia: The Western Oil Mallee Project. Ecosystem Health 7, 116–121.
CrossRef |

Benderoth M, Textor S, Windsor AJ, Mitchell-Olds T, Gershenzon J, Kroymann J (2006) Positive selection driving diversification in plant secondary metabolism. Proceedings of the National Academy of Sciences, SA 103, 9118–9123.
CrossRef |

Bignell CM, Dunlop PJ, Brophy JJ (1998) Volatile leaf oils of some south-western and southern Australian species of the genus Eucalyptus (Series 1). Part XIX. Flavour and Fragrance Journal 13, 131–139.
CrossRef |

Bohlmann J, Steele CL, Croteau RB (1997) Monoterpene synthases from grand fir (Abies grandis). cDNA isolation characterization and functional expression of myrcene synthase (-)-(4S)-limonene synthase and (-) (1S 5S)-pinene synthase. Journal of Biological Chemistry 272, 21784–21792.
CrossRef | PubMed |

Bohlmann J, Crock J, Jetter R, Croteau RB (1998a) Terpenoid-based defenses in conifers: cDNA cloning characterization and functional expression of wound-inducible (E)-alpha-bisabolene synthase from grand fir (Abies grandis). Proceedings of the National Academy of Sciences, USA 95, 6756–6761.
CrossRef |

Bohlmann J, Meyer-Gauen G, Croteau RB (1998b) Plant terpenoid synthases: molecular biology and phylogenetic analysis. Proceedings of the National Academy of Sciences, USA 95, 4126–4133.
CrossRef |

Bohlmann J, Phillips M, Ramachandiran V, Katoh S, Croteau RB (1999) cDNA cloning characterization and functional expression of four new monoterpene synthase members of the Tpsd gene family from grand fir (Abies grandis). Archives of Biochemistry and Biophysics 368, 232–243.
CrossRef | PubMed |

Boland DJ, Brophy JJ, Flynn TM, Lassak EV (1982) Volatile leaf oils of Eucalyptus delegatensis seedlings. Phytochemistry 21, 2467–2469.
CrossRef |

Boland DJ , Brophy JJ , House APN (1991) ‘Eucalyptus leaf oils.’ (Inkata Press: Sydney)

Bouvier F, Suire C, d’Harlingue A, Backhaus RA, Camara B (2000) Molecular cloning of geranyl diphosphate synthase and compartmentation of monoterpene synthesis in plant cells. The Plant Journal 24, 241–252.
CrossRef | PubMed |

Brennan EB, Weinbaum SA, Rosenheim JA, Karban R (2001) Heteroblasty in Eucalyptus globulus (Myricales: Myrtaceae) affects ovipositonal and settling preferences of Ctenarytaina eucalypti and C. spatulata (Homoptera: Psyllidae). Environmental Entomology 30, 1144–1149.

Brophy JJ , Southwell IA (2002) Eucalyptus chemistry. In ‘Eucalyptus: the genus Eucalyptus’. (Ed. JJW Coppen) pp. 102–160. (Taylor & Francis: London)

Brophy JJ, Clarkson JR, Craven LA, Forrester RI (1994) The essential oils of Australian members of the genus Asteromyrtus (Myrtaceae). Biochemical Systematics and Ecology 22, 409–417.
CrossRef |

Brophy JJ, Goldsack RJ, Bean AR, Forster PI, Lepschi BJ (1999a) Leaf essential oils of the genus Leptospermum (Myrtaceae) in eastern Australia Part 4. Leptospermum deanei and allies. Flavour and Fragrance Journal 14, 92–97.
CrossRef |

Brophy JJ, Goldsack RJ, Bean AR, Forster PI, Lepschi BJ (1999b) Leaf essential oils of the genus Leptospermum (Myrtaceae) in eastern Australia. Part 5. Leptospermum continentale and allies. Flavour and Fragrance Journal 14, 98–104.
CrossRef |

Brophy JJ, Goldsack RJ, Bean AR, Forster PI, Lepschi BJ (2000a) Leaf essential oils of the genus Leptospermum (Myrtaceae) in eastern Australia. Part 6. Leptospermum polygalifolium and allies. Flavour and Fragrance Journal 15, 271–277.
CrossRef |

Brophy JJ, Goldsack RJ, Punruckvong A, Bean AR, Forster PI, Lepschi BJ, Doran JC, Rozefelds AC (2000b) Leaf essential oils of the genus Leptospermum (Myrtaceae) in eastern Australia. Part 7. Leptospermum petersonii, L. liversidgei and allies. Flavour and Fragrance Journal 15, 342–351.
CrossRef |

Bruce BD (2000) Chloroplast transit peptides: structure function and evolution. Trends in Cell Biology 10, 440–447.
CrossRef | PubMed |

Butcher PA, Doran JC, Slee MU (1994) Intraspecific variation in leaf oils of Melaleuca alternifolia (Myrtaceae). Biochemical Systematics and Ecology 22, 419–430.
CrossRef |

Cano-Camacho H, Lopez-Romero E, Lozoya-Gloria E (1997) Partial purification and characterization of an elicitor stimulated sesquiterpene cyclase from chili pepper (Capsicum annuum L.) fruits. Plant Science 124, 23–31.
CrossRef |

Chen F, Ro DK, Petri J, Gershenzon J, Bohlmann J, Pichersky E, Tholl D (2004) Characterization of a root-specific Arabidopsis terpene synthase responsible for the formation of the volatile monoterpene 1,8-cineole. Plant Physiology 135, 1956–1966.
CrossRef | PubMed |

Copolovici LO, Filella I, Llusia J, Niinemets U, Penuelas J (2005) The capacity for thermal protection of photosynthetic electron transport varies for different monoterpenes in Quercus ilex. Plant Physiology 139, 485–496.
CrossRef | PubMed |

Cornwell CP, Reddy N, Leach DN, Wyllie SG (2000a) Hydrolysis of hedycaryol: the origin of the eudesmols in the Myrtaceae. Flavour and Fragrance Journal 15, 421–431.
CrossRef |

Cornwell CP, Reddy N, Leach DN, Wyllie SG (2000b) Origin of (+)-delta-cadinene and the cubenols in the essential oils of the Myrtaceae. Flavour and Fragrance Journal 15, 352–361.
CrossRef |

Cornwell CP, Reddy N, Leach DN, Wyllie SG (2001) Germacradienols in the essential oils of the Myrtaceae. Flavour and Fragrance Journal 16, 263–273.
CrossRef |

Davilahuerta G, Hamada H, Davis GD, Stipanovic RD, Adams CM, Essenberg M (1995) Cadinane-type sesquiterpenes induced in Gossypium cotyledons by bacterial inoculation. Phytochemistry 39, 531–536.
CrossRef |

Davis EM, Ringer KL, McConkey ME, Croteau RB (2005) Monoterpene metabolism cloning expression and characterization of menthone reductases from peppermint. Plant Physiology 137, 873–881.
CrossRef | PubMed |

de Carvalho LR, Roque NF (2004) Correlations between primary and secondary metabolites in Ceramiales (Rhodophyta). Biochemical Systematics and Ecology 32, 337–342.
CrossRef |

Degenhardt J, Gershenzon J, Baldwin IT, Kessler A (2003) Attracting friends to feast on foes: engineering terpene emission to make crop plants more attractive to herbivore enemies. Current Opinion in Biotechnology 14, 169–176.
CrossRef | PubMed |

de Kraker JW, Franssen MCR, de Groot A, Konig WA, Bouwmeester HJ (1998) (+)-Germacrene a biosynthesis the committed step in the biosynthesis of bitter sesquiterpene lactones in chicory. Plant Physiology 117, 1381–1392.
CrossRef | PubMed |

de Meijer EPM, Hammond KM (2005) The inheritance of chemical phenotype in Cannabis sativa L. (II): Cannabigerol predominant plants. Euphytica 145, 189–198.
CrossRef |

Denson J, Xi Z, Wu Y, Yang W, Neale G, Zhang J (2006) Screening for inter-individual splicing differences in human GSTM4 and the discovery of a single nucleotide substitution related to the tandem skipping of two exons. Gene 379, 148–155.
CrossRef | PubMed |

Di Stefano J (2005) Mammalian browsing damage in the Mt. Cole State Forest southeastern Australia: analysis of browsing patterns spatial relationships and browse selection. New Forests 29, 43–61.
CrossRef |

Doran JC, Williams ER, Brophy JJ (1995) Patterns of variation in the seedling leaf oils of Eucalyptus urophylla E. pellita and E. scias. Australian Journal of Botany 43, 327–336.
CrossRef |

Doran JC, Brophy JJ, Lassak EV, House APN (2001) Backhousia citriodora F.Muell: rediscovery and chemical characterization of the L-citronellal form and aspects of its breeding system. Flavour and Fragrance Journal 16, 325–328.
CrossRef |

Dubey VS, Ritu Bhalla R, Luthra R (2003) An overview of the non-mevalonate pathway for terpenoid biosynthesis in plants. Journal of Biosciences 28, 637–646.
CrossRef | PubMed |

Dudareva N, Cseke L, Blanc VM, Pichersky E (1996) Evolution of floral scent in Clarkia: novel patterns of S-linalool synthase gene expression in the C. breweri flower. The Plant Cell 8, 1137–1148.
CrossRef | PubMed |

Dudareva N, Martin D, Kish CM, Kolosova N, Gorenstein N, Faldt J, Miller B, Bohlmann J (2003) (E)-beta-ocimene and myrcene synthase genes of floral scent biosynthesis in snapdragon: function and expression of three terpene synthase genes of a new terpene synthase subfamily. The Plant Cell 15, 1227–1241.
CrossRef | PubMed |

Dungey HS, Potts BM, Whitham TG, Li HF (2000) Plant genetics affects arthropod community richness and composition: Evidence from a synthetic eucalypt hybrid population. Evolution 54, 1938–1946.
PubMed |


Dunlop PJ, Bignell CM, Brooker MIH, Brophy JJ, Hibbert DB (1999) Use of gas chromatograms of essential leaf oils to compare eight taxa of genus Angophora (Myrtaceae): possible relationships to the genus Eucalyptus. Biochemical Systematics and Ecology 27, 815–830.
CrossRef |

Edwards PB, Wanjura WJ, Brown WV, Dearn JM (1990) Mosaic resistance in plants. Nature 347, 434.
CrossRef |

Edwards PB, Wanjura WJ, Brown WV (1993) Selective herbivory by Christmas beetles in response to intraspecific variation in Eucalyptus. Oecologia 95, 551–557.

Egerton-Warburton LM, Ghisalberti EL, Considine JA (1998a) Infraspecific variability in the volatile leaf oils of Chamelaucium uncinatum (Myrtaceae). Biochemical Systematics and Ecology 26, 873–888.
CrossRef |

Egerton-Warburton LM, Ghisalberti EL, Burton NC (1998b) Intergeneric hybridism between Chamelaucium and Verticordia (Myrtaceae) based on analysis of essential oils and morphology. Australian Journal of Botany 46, 201–208.
CrossRef |

Eisenreich W, Schwarz M, Cartayrade A, Arigoni D, Zenk MH, Bacher A (1998) The deoxyxylulose phosphate pathway of terpenoid biosynthesis in plants and microorganisms. Chemistry & Biology 5, R221–R233.
CrossRef | PubMed |

Eschler BM, Pass DM, Willis R, Foley WJ (2000) Distribution of foliar formylated phloroglucinol derivatives amongst Eucalyptus species. Biochemical Systematics and Ecology 28, 813–824.
CrossRef | PubMed |

Eyles A, Davies NW, Yuan ZQ, Mohammed C (2003) Host responses to natural infection by Cytonaema sp. in the aerial bark of Eucalyptus globulus. Forest Pathology 33, 317–331.
CrossRef |

Fadel H, Marx F, El-Sawy A, El-Ghorab A (1999) Effect of extraction techniques on the chemical composition and antioxidant activity of Eucalyptus camaldulensis var. brevirostris leaf oils. Zeitschrift fur Lebensmittel-Untersuchung und – Forschung. A, Food Research and Technology 208, 212–216.
CrossRef |

Fernandez MA, Tornos MP, Garcia MD, de las Heras B, Villar AM, Saenz MT (2001) Anti-inflammatory activity of abietic acid a diterpene isolated from Pimenta racemosa var. grissea. Journal of Pharmacy and Pharmacology 53, 867–872.
CrossRef | PubMed |

Gershenzon J , Croteau R (1993) Terpenoid biosynthesis: the basic pathway and formation of monoterpenes, sesquiterpenes, and diterpenes. In ‘Lipid metabolism in plants’. (Ed. TSJ Moore) pp. 339–388. (CRC Press: Boca Raton: FL).

Ghisalberti EL (1996) Bioactive acylphloroglucinol derivatives from Eucalyptus species. Phytochemistry 41, 7–22.
CrossRef | PubMed |

Giamakis A, Kretsi O, Chinou I, Spyropoulos CG (2001) Eucalyptus camaldulensis: volatiles from immature flowers and high production of 1,8-cineole and beta-pinene by in vitro cultures. Phytochemistry 58, 351–355.
CrossRef | PubMed |

Guenther AB, Monson RK, Fall R (1991) Isoprene and monoterpene emission rate variability observations with Eucalyptus and emission rate algorithm development. Journal of Geophysical Research—Atmospheres 96, 10799–10808.
CrossRef |


Harder J, Foss S (1999) Anaerobic formation of the aromatic hydrocarbon p-cymene from monoterpenes by methanogenic enrichment cultures. Geomicrobiology Journal 16, 295–305.
CrossRef |

He C, Murray F, Lyons T (2000a) Monoterpene and isoprene emissions from 15 Eucalyptus species in Australia. Atmospheric Environment 34, 645–655.
CrossRef |

He C, Murray F, Lyons T (2000b) Seasonal variations in monoterpene emissions from Eucalyptus species. Chemosphere—Global Change Science 2, 65–76.
CrossRef |

Homer LE, Leach DN, Lea D, Slade LL, Henry RJ, Baverstock PR (2000) Natural variation in the essential oil content of Melaleuca alternifolia Cheel (Myrtaceae). Biochemical Systematics and Ecology 28, 367–382.
CrossRef | PubMed |

Hugueney P, Camara B (1990) Purification and characterization of farnesyl pyrophosphate synthase from Capsicum annuum. FEBS Letters 273, 235–238.
CrossRef | PubMed |

Hume ID, Esson C (1993) Nutrients, antinutrients and leaf selection by captive koalas (Phascolarctos cinereus). Australian Journal of Zoology 41, 379–392.
CrossRef |

Iason G (2005) The role of plant secondary metabolites in mammalian herbivory: ecological perspectives. Proceedings of the Nutrition Society 64, 123–131.
CrossRef | PubMed |

Iijima Y, Gang DR, Fridman E, Lewinsohn E, Pichersky E (2004) Characterization of geraniol synthase from the peltate glands of sweet basil. Plant Physiology 134, 370–379.
CrossRef | PubMed |

Ireland BF, Hibbert DB, Goldsack RJ, Doran JC, Brophy JJ (2002) Chemical variation in the leaf essential oil of Melaleuca quinquenervia (Cav.) S.T.Blake. Biochemical Systematics and Ecology 30, 457–470.
CrossRef |

Johnstone PC (1984) Chemosystematic and morphometric relationships of populations of some peppermint eucalypts. PhD Thesis, Monash University, Melbourne.

Jones TGH (1937) Essential oils from the Queensland flora. X. Melaleuca linariifolia. Proceedings of the Royal Society of Queensland 48, 48–50.

Jones RVH, Sutherland MD (1968) Terpenoid chemistry. XV. 1,5-Dimethylcyclodeca-1,5,7-triene, the precursor of geijerene in Geijera parviflora. Australian Journal of Chemistry 21, 2255–2264.

Kearsley MJC, Whitham TG (1998) The developmental stream of cottonwoods affects ramet growth and resistance to galling aphids. Ecology 79, 178–191.

Kindle KL (1998) Amino-terminal and hydrophobic regions of the Chlamydomonas reinhardtii plastocyanin transit peptide are required for efficient protein accumulation in vivo. Plant Molecular Biology 38, 365–377.
CrossRef | PubMed |

Kindle KL, Lawrence SD (1998) Transit peptide mutations that impair in vitro and in vivo chloroplast protein import do not affect accumulation of the gamma-subunit of chloroplast ATPase. Plant Physiology 116, 1179–1190.
CrossRef | PubMed |

King DJ, Gleadow RM, Woodrow IE (2006) The accumulation of terpenoid oils does not incur a growth cost in Eucalyptus polybractea seedlings. Functional Plant Biology 33, 497–505.
CrossRef |

Kliebenstein DJ, Lambrix VM, Reichelt M, Gershenzon J, Mitchell-Olds T (2001) Gene duplication in the diversification of secondary metabolism: tandem 2-oxoglutarate-dependent dioxygenases control glucosinolate biosynthesis in Arabidopsis. The Plant Cell 13, 681–693.
CrossRef | PubMed |

Köllner TG, Schnee C, Gershenzon J, Degenhardt J (2004) The variability of sesquiterpenes emitted from two Zea mays cultivars is controlled by allelic variation of two terpene synthase genes encoding stereoselective multiple product enzymes. The Plant Cell 16, 1115–1131.
CrossRef | PubMed |

Lassak EV, Southwell IA (1982) The steam volatile leaf oils of some species of Eucalyptus subseries Strictinae. Phytochemistry 21, 2257–2261.
CrossRef |

Lawler IR, Stapley J, Foley WJ, Eschler BM (1999) Ecological example of a conditioned food aversion in plant-herbivore interactions: the effect of terpenes of Eucalyptus leaves on feeding by common ringtail and brushtail possums. Journal of Chemical Ecology 25, 401–415.
CrossRef |

Lawrence SD, Kindle KL (1997) Alterations in the Chlamydomonas plastocyanin transit peptide have distinct effects on in vitro import and in vivo protein accumulation. Journal of Biological Chemistry 272, 20357–20363.
CrossRef | PubMed |

Lee CK (1998) Ursane triterpenoids from leaves of Melaleuca leucadendron. Phytochemistry 49, 1119–1122.
CrossRef |

Lee LS, Brooks LO, Homer LE, Rossetto M, Henry RJ, Baverstock PR (2002) Geographic variation in the essential oils and morphology of natural populations of Melaleuca alternifolia (Myrtaceae). Biochemical Systematics and Ecology 30, 343–360.
CrossRef |

Li H, Madden JL, Potts BM (1996) Variation in volatile leaf oils of the Tasmanian Eucalyptus species II. Subgenus Symphyomyrtus. Biochemical Systematics and Ecology 24, 547–569.
CrossRef |

Linhart YB, Thompson JD (1995) Terpene-based selective herbivory by Helix aspersa (Mollusca) on Thymus vulgaris (Labiatae). Oecologia 102, 126–132.

Loreto F, Forster A, Durr M, Csiky O, Seufert G (1998) On the monoterpene emission under heat stress and on the increased thermotolerance of leaves of Quercus ilex L. fumigated with selected monoterpenes. Plant, Cell & Environment 21, 101–107.
CrossRef |

Lowe RF, Russell MF, Southwell IA, Day J (2005) Astartea a new source of (+) (1S 5R)-myrtenal. Journal of Essential Oil Research 17, 683–685.

Lowman MD, Heatwole H (1992) Spatial and temporal variability in defoliation of Australian eucalypts. Ecology 73, 129–142.
CrossRef |

Lu S, Xu R, Jia JW, Pang JH, Matsuda SPT, Chen XY (2002) Cloning and functional characterization of a beta-pinene synthase from Artemisia annua that shows a circadian pattern of expression. Plant Physiology 130, 477–486.
CrossRef | PubMed |

Lücker J, Bouwmeester HJ, Schwab W, Blaas J, van der Plas LH, Verhoeven HA (2001) Expression of Clarkia S-linalool synthase in transgenic petunia plants results in the accumulation of S-linalyl-beta-D-glucopyranoside. The Plant Journal 27, 315–324.
CrossRef | PubMed |

Lücker J, EI Tamer MK, Schwab W, Verstappen FWA, van der Plas LHW, Bouwmeester HJ, Verhoeven HA (2002) Monoterpene biosynthesis in lemon (Citrus limon). cDNA isolation and functional analysis of four monoterpene synthases. European Journal of Biochemistry 269, 3160–3171.
CrossRef | PubMed |

Lupien S, Karp F, Wildung M, Croteau RB (1999) Regiospecific Cytochrome P450 limonene hydroxylases from mint (Mentha) species: cDNA isolation characterization and functional expression of (-)-4S-limonene-3-hydroxylase and (-) 4S-limonene-6-hydroxylase. Archives of Biochemistry and Biophysics 368, 181–192.
CrossRef | PubMed |

Mansfield S, Withers TM, Gous SF, Potter KJB, Kriticos DJ, Watson MC, Kimberley MO (2006) Potential of selective insecticides for managing Uraba lugens (Lepidoptera: Nolidae) on eucalypts. Journal of Economic Entomology 99, 780–789.
PubMed |


Martin DM, Bohlmann J (2004) Identification of Vitis vinifera (-)-alpha-terpineol synthase by in silico screening of full-length cDNA ESTs and functional characterization of recombinant terpene synthase. Phytochemistry 65, 1223–1229.
CrossRef | PubMed |


Martin DM, Faldt J, Bohlmann J (2004) Functional characterization of nine Norway spruce TPS genes and evolution of Gymnosperm terpene synthases of the TPS-d subfamily. Plant Physiology 135, 1908–1927.
CrossRef | PubMed |

Mastelic J, Jerkovic I (2003) Application of co-distillation with superheated pentane vapour to the isolation of unstable essential oils. Flavour and Fragrance Journal 18, 521–526.
CrossRef |

Mayer R (1990) Flavonoids from Leptospermum scoparium. Phytochemistry 29, 1340–1342.
CrossRef |

McConkey ME, Gershenzon J, Croteau RB (2000) Developmental regulation of monoterpene biosynthesis in the glandular trichomes of peppermint. Plant Physiology 122, 215–224.
CrossRef | PubMed |

Mercke P, Crock J, Croteau RB, Brodelius PE (1999) Cloning expression and characterization of epi-cedrol synthase a sesquiterpene cyclase from Artemisia annua L. Archives of Biochemistry and Biophysics 369, 213–222.
CrossRef | PubMed |

Milborrow BV (2001) The pathway of biosynthesis of abscisic acid in vascular plants: a review of the present state of knowledge of ABA biosynthesis. Journal of Experimental Botany 52, 1145–1164.
CrossRef | PubMed |

Miller B, Oschinski C, Zimmer W (2001) First isolation of an isoprene synthase gene from poplar and successful expression of the gene in Escherichia coli. Planta 213, 483–487.
CrossRef | PubMed |

Molina A, Reigosa MJ, Carballeira A (1991) Release of allelochemical agents from litter throughfall and topsoil in plantations of Eucalyptus globulus Labill in Spain. Journal of Chemical Ecology 17, 147–160.
CrossRef |

Moore BD, Wallis IR, Pala-Paul J, Brophy JJ, Willis RH, Foley WJ (2004) Antiherbivore chemistry of Eucalyptus – Cues and deterrents for marsupial folivores. Journal of Chemical Ecology 30, 1743–1769.
CrossRef | PubMed |

Morrow PA, Fox LR (1980) Effects of variation in Eucalyptus essential oil yield on insect growth and grazing damage. Oecologia 45, 209–219.
CrossRef |

Nakagiri T, Lee J-B, Hayashi T (2005) cDNA cloning functional expression and characterization of ent-copalyl diphosphate synthase from Scoparia dulcis L. Plant Science 169, 760–767.
CrossRef |

Nishimura K, Shinoda N, Hirose Y (1969) A new sesquiterpen, bicyclogermacrene. Tetrahedron Letters 10, 3097–3100.
CrossRef |

Ohnuma S, Koyama T, Ogura K (1989) Kinetic studies on the prenyl chain elongation by undecaprenyl diphosphate synthase with artificial substrate homologues. FEBS Letters 257, 71–74.
CrossRef | PubMed |

Penfold AR (1925) Essential oils of Melaleuca linarifolia (Smith) and M. alternifolia (Cheel). Journal and Proceedings of the Royal Society of New South Wales 59, 306–324.

Penfold AR, Morrison FR (1927) The occurrence of a number of varieties of Eucalyptus dives as determined by chemical analyses of the essential oils. Journal and Proceedings of the Royal Society of New South Wales 61, 54–67.

Penfold AR, Morrison FR (1937) The occurrence of a number of varieties of Eucalyptus radiata (E. numerosa) as determined by chemical analyses of the essential oils. Journal and Proceedings of the Royal Society of New South Wales 70, 375–377.

Penfold AR, Willis JL (1953) Physiological forms of Eucalyptus citriodora Hooker. Nature 171, 883–884.
CrossRef | PubMed |

Perry NB, Brennan NJ, Van Klink JW, Harris W, Douglas MH, McGimpsey JA, Smallfield BM, Anderson RE (1997) Essential oils from New Zealand manuka and kanuka: chemotaxonomy of Leptospermum. Phytochemistry 44, 1485–1494.
CrossRef |

Pichersky E, Noel JP, Dudareva N (2006) Biosynthesis of plant volatiles: nature’s diversity and ingenuity. Science 311, 808–811.
CrossRef | PubMed |

Plomion C, Yani A, Marpeau A (1996) Genetic determinism of delta 3-carene in maritime pine using RAPD markers. Genome 39, 1123–1127.
CrossRef | PubMed |


Prosser IM, Adams RJ, Beale MH, Hawkins ND, Phillips AL, Pickett JA, Field LM (2006) Cloning and functional characterisation of a cis-muuroladiene synthase from black peppermint (Mentha × piperita) and direct evidence for a chemotype unable to synthesise farnesene. Phytochemistry 67, 1564–1571.
CrossRef | PubMed |

Qi X, Bakht S, Leggett M, Maxwell C, Melton R, Osbourn A (2004) A gene cluster for secondary metabolism in oat: implications for the evolution of metabolic diversity in plants. Proceedings of the National Academy of Sciences, USA 101, 8233–8238.
CrossRef |

Rasmann S, Kollner TG, Degenhardt J, Hiltpold I, Toepfer S, Kuhlmann U, Gershenzon J, Turlings TCJ (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434, 732–737.
CrossRef | PubMed |

Ringer KL, Davis EM, Croteau RB (2005) Monoterpene metabolism. Cloning expression and characterization of (-)-isopiperitenol/(-)-carveol dehydrogenase of peppermint and spearmint. Plant Physiology 137, 863–872.
CrossRef | PubMed |

Russell M, Southwell IA (2002) Monoterpenoid accumulation in Melaleuca alternifolia seedlings. Phytochemistry 59, 709–716.
CrossRef | PubMed |

Santos GG, Alves JCN, Rodilla JML, Duarte AP, Lithgow AM, Urones JG (1997) Terpenoids and other constituents of Eucalyptus globulus. Phytochemistry 44, 1309–1312.
CrossRef |

Schepmann HG, Pang J, Matsuda SPT (2001) Cloning and characterization of Ginkgo biloba levopimaradiene synthase which catalyzes the first committed step in ginkgolide biosynthesis. Archives of Biochemistry and Biophysics 392, 263–269.
CrossRef | PubMed |

Sefidkon F, Dabiri M, Rahimi-Bidgoly A (1999) The effects of distillation methods and stage of plant growth on the essential oil content and composition in Tymus kotschyanus. Flavour and Fragrance Journal 14, 405–408.
CrossRef |

Schwab W (2003) Metabolome diversity: too few genes too many metabolites? Phytochemistry 62, 837–849.
CrossRef | PubMed |

Sharkey TD, Yeh S, Wiberley AE, Falbel TG, Gong D, Fernandez DE (2005) Evolution of the isoprene biosynthetic pathway in Kudzu. Plant Physiology 137, 700–712.
CrossRef | PubMed |

Shelton DA, Leach DN, Henry RJ (2004a) Isopentenyl pyrophosphate isomerases from Melaleuca alternifolia (Cheel) and their role in isoprenoid biosynthesis. Journal of Horticultural Science & Biotechnology 79, 289–292.

Shelton D, Zabaras D, Chohan S, Wyllie SG, Baverstock P, Leach D, Henry R (2004b) Isolation and partial characterisation of a putative monoterpene synthase from Melaleuca alternifolia. Plant Physiology and Biochemistry 42, 875–882.
CrossRef | PubMed |

Shepherd M, Chaparro JX, Teasdale R (1999) Genetic mapping of monoterpene composition in an interspecific eucalypt hybrid. Theoretical and Applied Genetics 99, 1207–1215.
CrossRef |

Shimada T, Endo T, Fujii H, Hara M, Ueda T, Kita M, Omura M (2004) Molecular cloning and functional characterization of four monoterpene synthase genes from Citrus unshiu Marc. Plant Science 166, 49–58.
CrossRef |

Shimada T, Endo T, Fujii H, Hara M, Omura M (2005) Isolation and characterization of (E)-beta-ocimene and 1,8-cineole synthases in Citrus unshiu Marc. Plant Science 168, 987–995.
CrossRef |

Silver GM, Fall R (1995) Characterization of aspen isoprene synthase an enzyme responsible for leaf isoprene emission to the atmosphere. Journal of Biological Chemistry 270, 13010–13016.
CrossRef | PubMed |

Simmons D, Parsons RF (1976) Analysis of a hybrid swarm involving Eucalyptus crenulata and E. ovata using leaf oils and morphology. Biochemical Systematics and Ecology 4, 97–101.
CrossRef |

Simmons D, Parsons RF (1987) Seasonal variation in the volatile leaf oils of two Eucalyptus species. Biochemical Systematics and Ecology 15, 209–215.
CrossRef |

Smith MW, Yamaguchi S, Ait-Ali T, Kamiya Y (1998) The first step of gibberellin biosynthesis in pumpkin is catalyzed by at least two copalyl diphosphate synthases encoded by differentially regulated genes. Plant Physiology 118, 1411–1419.
CrossRef | PubMed |

Southwell IA (1970) New occurrence of hedycaryol, the precursor of elemol, in Phebalium ozothamnoides (Rutaceae). Phytochemistry 9, 2243–2245.
CrossRef |

Southwell IA (1978) ‘Essential oil content of koala food trees’. In ‘The koala: proceedings of the Taronga symposium’. (Ed. TJ Bergin) pp. 62–74. (Royal Zoological Society of NSW: Sydney)

Southwell IA , Lowe R (1999) ‘Tea tree: the genus Melaleuca.’ (CRC Press: Boca Raton, FL)

Southwell IA, Russell MF (2002) Volatile oil comparison of cotyledon leaves of chemotypes of Melaleuca alternifolia. Phytochemistry 59, 391–393.
CrossRef | PubMed |

Southwell IA, Stiff IA (1989) Ontogenetical changes in monoterpenoids of Melaleuca alternifolia leaf. Phytochemistry 28, 1047–1051.
CrossRef |

Southwell IA, Stiff IA (1990) Differentiation between Melaleuca alternifolia and M. linariifolia by monoterpenoid comparison. Phytochemistry 29, 3529–3533.
CrossRef |

Starks CM, Back K, Chappell J, Noel JP (1997) Structural basis for cyclic terpene biosynthesis by tobacco 5-epi-aristolochene synthase. Science 277, 1815–1820.
CrossRef | PubMed |

Staudt M, Joffre R, Rambal S (2003) How growth conditions affect the capacity of Quercus ilex leaves to emit monoterpenes. New Phytologist 158, 61–73.

Stone C, Bacon PE (1994) Relationships among moisture stress insect herbivory foliar cineole content and the growth of river red gum Eucalyptus camaldulensis. Journal of Applied Ecology 31, 604–612.
CrossRef |

Sun TP, Kamiya Y (1994) The Arabidopsis GA1 locus encodes the cyclase ent-kaurene synthetase A of gibberellin biosynthesis. The Plant Cell 6, 1509–1518.
CrossRef | PubMed |

Suomela J, Ayres MP (1994) Within-tree and among-tree variation in leaf characteristics of mountain birch and its implications for herbivory. Oikos 70, 212–222.
CrossRef |

Thumma BR, Nolan MR, Evans R, Moran GF (2005) Polymorphisms in cinnamoyl CoA reductase (CCR) are associated with variation in microfibril angle in Eucalyptus spp. Genetics 171, 1257–1265.
CrossRef | PubMed |

Toyota M, Koyama H, Mizutani M, Asakawa Y (1996) (-)-ent-Spathulenol isolated from liverworts is an artefact. Phytochemistry 41, 1347–1350.
CrossRef |

Wang H, Fujimoto Y (1993) Triterpene esters from Eucalyptus tereticornis. Phytochemistry 33, 151–153.
CrossRef |

Weston RJ (1984) Composition of essential oil from leaves of Eucalyptus delegatensis. Phytochemistry 23, 1943–1945.
CrossRef |

Whittington DA, Wise ML, Urbansky M, Coates RM, Croteau RB, Christianson DW (2002) Bornyl diphosphate synthase: structure and strategy for carbocation manipulation by a terpenoid cyclase. Proceedings of the National Academy of Sciences, USA 99, 15375–15380.
CrossRef |

Wildung MR, Croteau RB (2005) Genetic engineering of peppermint for improved essential oil composition and yield. Transgenic Research 14, 365–372.
CrossRef | PubMed |

Wildy DT, Pate JS, Bartle JR (2000) Variations in composition and yield of leaf oils from alley-farmed oil mallees (Eucalyptus spp.) at a range of contrasting sites in the Western Australian wheatbelt. Forest Ecology and Management 134, 205–217.
CrossRef |

Williams DC, McGarvey DJ, Katahira EJ, Croteau RB (1998) Truncation of limonene synthase preprotein provides a fully active ‘Pseudomature’ form of this monoterpene cyclase and reveals the function of the amino-terminal arginine pair. Biochemistry 37, 12213–12220.
CrossRef | PubMed |

Wink M (2003) Evolution of secondary metabolites from an ecological and molecular phylogenetic perspective. Phytochemistry 64, 3–19.
CrossRef | PubMed |

Wise ML, Savage TJ, Katahira E, Croteau RB (1998) Monoterpene synthases from common sage (Salvia officinalis) – cDNA isolation characterization and functional expression of (+)-sabinene synthase 1,8-cineole synthase and (+)-bornyl diphosphate synthase. Journal of Biological Chemistry 273, 14891–14899.
CrossRef | PubMed |

Yamakoshi Y, Murata M, Shimizu A, Homma S (1992) Isolation and characterization of macrocarpals B-G antibacterial compounds from Eucalyptus macrocarpa. Bioscience, Biotechnology, and Biochemistry 56, 1570–1576.
PubMed |


Yang T, Li J, Wang HX, Zeng Y (2005) A geraniol-synthase gene from Cinnamomum tenuipilum. Phytochemistry 66, 285–293.
CrossRef | PubMed |

Yoshioka H, Yamada N, Doke N (1999) cDNA cloning of sesquiterpene cyclase and squalene synthase and expression of the genes in potato tuber infected with Phytophthora infestans. Plant & Cell Physiology 40, 993–998.
PubMed |


Zabaras D, Wyllie SG (2002) Rearrangement of p-menthane terpenes by Carboxen during HS-SPME. Journal of Separation Science 25, 685–690.
CrossRef |

Zavala-Paramo G, Chavez-Moctezuma MP, Garcia-Pineda E, Yin S, Chappell J, Lozoya-Gloria E (2000) Isolation of an elicitor-stimulated 5-epi-aristolochene synthase gene (gPEAS1) from chili pepper (Capsicum annuum). Physiologia Plantarum 110, 410–418.
CrossRef |








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