The evolution of foliar terpene diversity in Myrtaceae

Phytochemistry Reviews

Volumn 13, Issue 3, 2014, Pages 695-716

  Padovan, Amanda ^a   Keszei, András ^a   Külheim, Carsten ^a   Foley, William J ^a  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

Cineole; Eucalyptus; Evolution; Melaleuca; Monoterpene; Sesquiterpene; Terpene synthase

Indexed keywords

CINEOLE; ESSENTIAL OIL; PINENE; SYNTHETASE; TERPENE; TERPENE SYNTHASE; UNCLASSIFIED DRUG;

CONCENTRATION (PARAMETERS); ENZYME ACTIVITY; ENZYME STRUCTURE; ENZYME SYNTHESIS; EVOLUTION; INFORMATION PROCESSING; MYRTACEAE; NONHUMAN; PHYLOGENY; POPULATION ABUNDANCE; PRIORITY JOURNAL; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS; REVIEW; SPECIES DIVERSITY; STANDARDIZATION; SYNTHESIS;

EID: 84921001742     PISSN: 15687767     EISSN: 1572980X     Source Type: Journal    
DOI: 10.1007/s11101-013-9331-3     Document Type: Review

References (90)

1. Aharoni A, Giri AP, Verstappen FWA, Bertea CM, Sevenier R, Sun Z, Jongsma MA, Schwab W, Bouwmeester HJ (2004) Gain and loss of fruit flavor compounds produced by wild and cultivated strawberry species. Plant Cell 16:3110-3131 (Pubitemid 41075756)
2. Ammon DG, Barton AFM, Clarke DA, Tjandra J (1985) Rapid and accurate chemical determination of the water content of plants containing volatile oils. Analyst 110:917-920
3. Andrew R, Wallis I, Harwood C, Henson M, Foley W (2007) Heritable variation in the foliar secondary metabolite sideroxylonal in Eucalyptus confers cross-resistance to herbivores. Oecologia 153:891-901 (Pubitemid 47389319)
4. Andrew RL, Wallis IR, Harwood CE, Foley WJ (2010) Genetic and environmental contributions to variation and population divergence in a broad-spectrum foliar defence of Eucalyptus tricarpa. Ann Bot 105:707-717
5. Andrew RL, Keszei A, Foley WJ (2013) Intensice sampling identifies new chemotypes, population divergence and biosynthetic connections among terpenoids in Eucalyptus tricarpa. Phytochemistry 94:148-158
6. Arnold K, Bordoli L, Kopp J, Schwede T (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22:195-201 (Pubitemid 43205406)
7. Biffin E, Lucas EJ, Craven LA, Ribeiro da Costa I, Harrington MG, Crisp MD (2010) Evolution of exceptional species richness among lineages of fleshy-fruited Myrtaceae. Ann Bot 106:79-93
8. Birks JS, Kanowski PJ (1993) Analysis of resin compositional data. Silvae Genet 42:340-350
9. Bohlmann J, Keeling CI (2008) Terpenoid biomaterials. Plant J 54:656-669 (Pubitemid 351678044)
10. Bohlmann J, Crock J, Jetter R, Croteau R (1998) Terpenoidbased defenses in conifers: cDNA cloning, characterization, and functional expression of wound-inducible (E)-alpha-bisabolene synthase from grand fir (Abies grandis). PNAS 95:6756-6761 (Pubitemid 28278053)
11. Boland DJ, Brophy JJ, House APN (1991) Eucalyptus leaf oils. Use, chemistry, distillation and marketing. Inkata Press, Sydney, Australia
12. Bouwmeester HJ, Verstappen FWA, Posthumus MA, Dicke M (1999) Spider mite-induced (3S)-(E)-nerolidol synthase activity in cucumber and lima bean. The first dedicated step in acyclic C11-homoterpene biosynthesis. Plant Physiol 121:173-180 (Pubitemid 29452003)
13. Brophy JJ, Southwell IA (2002) Eucalyptus chemistry. In: Coppen JJ (ed) Eucalyptus: the genus Eucalyptus. Taylor and Francis, New York
14. Brophy JJ, Goldsack RJ, Forster PI (2006) A preliminary examination of the leaf oils of the genus Xanthostemon (Myrtaceae) in Australia. J Essent Oil Res 18:222-230
15. Butcher PA, Doran JC, Slee MU (1994) Intraspecific variation in the leaf oils of Melaleuca alternifolia (Myrtaceae). Biochem Syst Ecol 22:419-430 (Pubitemid 2099424)
16. Carnegie AJ, Lidbetter JR, Walker J, Horwood MA, Tesoriero L, Glen M, Priest MJ (2010) Uredo rangelii, a taxon in the guava rust complex, newly recorded on Myrtaceae in Australia. Australas Plant Pathol 39:463-466
17. Carson CF, Hammer KA, Riley TV (2006) Melaleuca alternifolia (tea tree) oil: a review of antimicrobial and other medicinal properties. Clin Microbiol Rev 19:50-62 (Pubitemid 43158450)
18. Charles DJ, Simon JE (1990) Comparison of extraction methods for the rapid determination of essential oil content and composition of basil. J Am Soc Hortic Sci 115:458-462
19. Chen H-C, Sheu M-J, Lin L-Y, Wu C-M (2007) Chemical composition of the leaf essential oil of Psidium guajava L. from Taiwan. J Essent Oil Res 19:345-347 (Pubitemid 47167654)
20. Christensson JB, Forsström P, Wennberg A-M, Karlberg A-T, Matura M (2009) Air oxidation increases skin irritation from fragrance terpenes. Contact Dermatitis 60:32-40
21. Cornwell CP, Reddy N, Leach DN, Grant WS (2000a) Origin of (+)-delta-cadinene and the cubenols in the essential oils of the Myrtaceae. Flavour Fragr J 15:352-361
22. Cornwell CP, Reddy N, Leach DN, Wyllie SG (2000b) Hydrolysis of hedycaryol: the origin of the eudesmols in the Myrtaceae. Flavour Fragr J 15:421-431 (Pubitemid 32124342)
23. Cornwell CP, Reddy N, Leach DN, Wyllie SG (2001) Germacradienols in the essential oils of the Myrtaceae. Flavour Fragr J 16:263-273 (Pubitemid 32685125)
24. Crankshaw DR, Langenheim JH (1981) Variation in terpenes and phenolics through leaf development in Hymenaea and its possible significance to herbivory. Biochem Syst Ecol 9:115-124
25. Croteau R, Davis E, Ringer K, Wildung M (2005) (-)-Menthol biosynthesis and molecular genetics. Naturwissenschaften 92:562-577 (Pubitemid 41720261)
26. De Vincenzi M, Silano M, De Vincenzi A, Maialetti F, Scazzocchio B (2002) Constituents of aromatic plants: eucalyptol. Fitoterapia 73:269-275 (Pubitemid 34603686)
27. DeGabriel J, Moore B, Shipley L, Krockenberger A, Wallis IR, Johnson C, Foley WJ (2009) Inter-population differences in the tolerance of a marsupial folivore to plant secondary metabolites. Oecologia 161:539-548
28. Degenhardt J, Köllner TG, Gershenzon J (2009) Monoterpene and sesquiterpene synthases and the origin of terpene skeletal diversity in plants. Phytochemistry 70:1621-1637
29. Dudareva N, Andersson S, Orlova I, Gatto N, Reichelt M, Rhodes D, Boland W, Gershenzon J (2005) The nonmevalonate pathway supports both monoterpene and sesquiterpene formation in snapdragon flowers. Plant Biol 102:933-938 (Pubitemid 40282768)
30. Fähnrich A, Krause K, Piechulla B (2011) Product variability of the 'cineole cassette' monoterpene synthases of related Nicotiana species. Mol Plant 4:965-984
31. Govaerts, R (2008) World checklist of Myrtaceae: Kew Pub
32. Grattapaglia D, Vaillancourt R, Shepherd M, Thumma B, Foley W, Külheim C, Potts B, Myburg A (2012) Progress in Myrtaceae genetics and genomics: Eucalyptus as the pivotal genus. TGG 8:463-508
33. Greenhagen BT, O'Maille PE, Noel JP, Chappell J (2006) Identifying and manipulating structural determinates linking catalytic specificities in terpene synthases. PNAS 103:9826-9831 (Pubitemid 43993582)
34. Grubb PJ, Metcalfe DJ, Grubb EA, Jones GD (1998) Nitrogen-richness and prtoection of seeds in Australian tropical rainforest: a test of plant defence theory. Oikos 82:467-482 (Pubitemid 28370189)
35. Guex N, Peitsch M, Schwede T, Diemand A (1995-2011) DeepView/Swiss- PdbViewer v4.0.4. Swiss Institute of Bioinformatics
36. Hall D, Robert J, Keeling C, Domanski D, Lara A, Jancsik S, Kuzyk M, Hamberger B, Borchers C, Bohlmann J (2011) An integrated genomic, proteomic and biochemical analysis of (+)-3-carene biosynthesis in Sitka spruce (Picea sitchensis) genotypes that are resistant or susceptible to white pine weevil. Plant J 65:936-948
37. Homer LE, Leach DN, Lea D, Slade Lee L, Henry RJ, Baverstock PR (2000) Natural variation in the essential oil content of Melaleuca alternifolia Cheel (Myrtaceae). Biochem Syst Ecol 28:367-382 (Pubitemid 30191014)
38. Horner JD, Gosz JR, Cates RG (1988) The role of carbon-based plant secondary metabolites in decomposition in terrestrial ecosystems. Am Nat 132:869-883 (Pubitemid 19324890)
39. Huang M, Sanchez-Moreiras AM, Abel C, Sohrabi R, Lee S, Gershenzon J, Tholl D (2012) The major volatile organic compound emitted from Arabidopsis thaliana flowers, the sesquiterpene (E)-β-caryophyllene, is a defense against a bacterial pathogen. New Phytol 193:997-1008
40. Hyatt DC, Croteau R (2005) Mutational analysis of a monoterpene synthase reaction: altered catalysis through directed mutagenesis of (-)-pinene synthase from Abies grandis. Arch Biochem Biophys 439:222-233 (Pubitemid 40922708)
41. Iguchi M, Nishiyama A, Yamamura S, Hirata Y (1969) Conversion of elemene-type sesquiterpenes into cadinene-type compounds and formation of ten-membered germacronetype intermediates. Tetrahedron Lett 10:4295-4298
42. Ireland B, Hibbert D, Goldsack R, Doran J, Brophy J (2002) Chemical variation in the leaf essential oil of Melaleuca quinquenervia (Cav.) S.T. Blake. Biochem Syst Ecol 30:457-470 (Pubitemid 34555948)
43. Kampranis SC, Ioannidis D, Purvis A, Mahrez W, Ninga E, Katerelos NA, Anssour S, Dunwell JM, Degenhardt J, Makris AM, Goodenough PW, Johnson CB (2007) Rational conversion of substrate and product specificity in a Salvia monoterpene synthase: structural insights into the evolution of terpene synthase function. Plant Cell 19:1994-2005 (Pubitemid 47218854)
44. Kant M, Baldwin I (2007) The ecogenetics and ecogenomics of plant-herbivore interactions: rapid progress on a slippery road. Curr Opin Genet Dev 17:519-524 (Pubitemid 350184309)
45. Katoh S, Hyatt D, Croteau R (2004) Altering product outcome in Abies grandis (-)-limonene synthase and (-)-limonene/(-)-alpha-pinene synthase by domain swapping and directed mutagenesis. Arch Biochem Biophys 425:65-76 (Pubitemid 38479605)
46. Kaur R, Kaur H(2010) The antimicrobial activity of essential oil and plant extracts of Woodfordia fruticosa. Arch Appl Sci Res 2:302-309
47. Keeling C, Bohlmann J (2006) Genes, enzymes and chemicals of terpenoid diversity in the constitutive and induced defence of conifers against insects and pathogens. New Phytol 170:657-675 (Pubitemid 43733630)
48. Keszei A, Brubaker CL, Foley WJ (2008) A molecular perspective on terpene variation in Australian Myrtaceae. Aust J Bot 56:197-213 (Pubitemid 351725021)
49. Keszei A, Brubaker CL, Carter R, Köllner T, Degenhardt J, Foley WJ (2010) Functional and evolutionary relationships between terpene synthases from Australian Myrtaceae. Phytochemistry 71:844-852
50. 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. Plant Cell 16:1115-1131 (Pubitemid 38641509)
51. Köllner TG, O'Maille PE, Gatto N, Boland W, Gershenzon J, Degenhardt J (2006) Two pockets in the active site of maize sesquiterpene synthase TPS4 carry out sequential parts of the reaction scheme resulting in multiple products. Arch Biochem Biophys 448:83-92
52. Köllner TG, Gershenzon J, Degenhardt J (2009) Molecular and biochemical evolution of maize terpene synthase 10, an enzyme of indirect defense. Phytochemistry 70:1139-1145
53. Külheim C, Webb H, Yeoh SH, Wallis I, Moran G, Foley W (2011) Using the Eucalyptus genome to understand the evolution of plant secondary metabolites in the Myrtaceae. BMC Proc 5:O11
54. Külheim C, Padovan A, Hefer C, Krause S, Degenhardt J, Myburg A, Foley WJ (2013) The Eucalyptus terpene synthase gene family. New Phytol (in press)
55. Langenheim JH, Foster CE, McGinley RB (1980) Inhibitory effects of different quantitative compositions of Hymenaea leaf resins on a generalist herbivore Spodoptera exigua. Biochem Syst Ecol 8:385-396
56. Lawler IR, Foley WJ, Eschler BM, Pass DM, Handasyde K (1998) Intraspecific variation in Eucalyptus secondary metabolites determines food intake by folivorous marsupials. Oecologia 116:160-169 (Pubitemid 28402861)
57. Levin DA (1976) The chemical defenses of plants to pathogens and hrbivores. Annu Rev Ecol Syst 7:121-159
58. Lichtenthaler HK (1999) The 1-deoxy-D-xylulose-5-phosphate pathway of isoprenoid biosynthesis in plants. Annu Rev Plant Physiol Plant Mol Biol 50:47-65
59. Linhart YB, Thompson JD (1995) Terpene-based selective herbivory by Helix aspersa (Mollusca) on Thymus vulgaris (Labiatae). Oecologia 102:126-132
60. Macel M, Klinkhamer P (2010) Chemotype of Senecio jacobaea affects damage by pathogens and insect herbivores in the field. Evol Ecol 24:237-250
61. Maida M, Carroll A, Coll J (1993) Variability of terpene content in the soft coral Sinularia flexibilis (Coelenterata: Octocorallia), and its ecological implications. J Chem Ecol 19:2285-2296 (Pubitemid 2000844)
62. Martin D, Aubourg S, Schouwey M, Daviet L, Schalk M, Toub O, Lund S, Bohlmann J (2010) Functional annotation, genome organization and phylogeny of the grapevine (Vitis vinifera) terpene synthase gene family based on genome assembly, FLcDNA cloning, and enzyme assays. BMC Plant Biol 10:226-248
63. Matsuki M, Foley WJ, Floyd R (2011) Role of volatile and nonvolatile plant secondary metabolites in host tree selection by Christmas beetles. J Chem Ecol 37:286-300
64. McCaskill D, Croteau R (1995) Monoterpene and sesquiterpene biosynthesis in glandular trichomes of peppermint (Mentha x piperita) rely exclusively on plastid-derived isopentenyl diphosphate. Planta 197:49-56
65. Moore BD, Andrew RL, Külheim C, Foley WJ (2013) Causes and consequences of intraspecific chemical diversity. New Phytol (in press)
66. Ogunbinu AO, Ogunwande IA, Walker TM, Setzer WN (2007) Study on the essential oil of Lawsonia inermis (L) Lythraceae. J Essent Oil Bear Plants 10:184-188 (Pubitemid 47152936)
67. Padovan A, Keszei A, Koellner TG, Degenhardt J, Foley WJ (2010) The molecular basis of host plant selection in Melaleuca quinquenervia by a successful biological control agent. Phytochemistry 71:1237-1244
68. Padovan A, Keszei A, Wallis IR, Foley WJ (2012) Mosaic eucalypt trees suggest genetic control at a point that influences several metabolic pathways. J Chem Ecol 38:914-923
69. Pichersky E, Gershenzon J (2002) The formation and function of plant volatiles: perfumes for pollinator attraction and defense. Curr Opin Plant Biol 5:237-243 (Pubitemid 34452071)
70. Prosser I, Altug IG, Phillips AL, König WA, Bouwmeester HJ, Beale MH (2004) Enantiospecific (+)- and (-)-germacrene D synthases, cloned from goldenrod, reveal a functionally active variant of the universal isoprenoidbiosynthesis aspartate-rich motif. Arch Biochem Biophys 432:136-144 (Pubitemid 39470010)
71. 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 x piperita) and direct evidence for a chemotype unable to synthesise farnesene. Phytochemistry 67:1564-1571 (Pubitemid 44251217)
72. Rasmann S, De Vos M, Casteel CL, Tian D, Halitschke R, Sun JY, Agrawal AA, Felton GW, Jander G (2012) Herbivory in the previous generation primes plants for enhanced insect resistance. Plant Physiol 158:854-863
73. Slee AV, Brooker MIH, Duffy SM, West JG (2006) EUCLID eucalypts of Australia third edition. CSIRO, Canberra
74. Steffen RB, Antoniolli ZI, Steffen GPK, da Silva RF (2012) Essential oil of Eucalyptus grandis Hill ex Maiden in stimulating mycorrhizal sibipiruna seedlings (Ceasalpinia peltophoroides Benth.). Cienc Florest 22:69-78
75. Steinbauer MJ (2010) Latitudinal trends in foliar oils of eucalypts: environmental correlates and diversity of chrysomelid leaf-beetles. Austral Ecol 35:204-213
76. Stubbs BJ, Specht A, Brushett D (2004) The essential oil of Cinnamomum camphora (L.) Nees and Eberm. - variation in oil composition throughout the tree in two chemotypes from eastern Australia. J Essent Oil Res 16:200-205
77. Suni T, Kulmala M, Hirsikko A, Bergman T, Laakso L, Aalto P, Leuning R, Cleugh H, Zegelin S, Hughes D, van Gorsel E, Kitchen M, Vana M, Hõrrak U, Mirme S, Mirme A, Sevanto S, Twining J, Tadros C (2008) Formation and characteristics of ions and charged aerosol particles in a native Australian eucalypt forest. Atmos Chem Phys 8:129-139
78. Thornhill AH, Crisp MD (2012) Phylogenetic assessment of pollen characters in Myrtaceae. Aust Syst Bot 25:171-187
79. Thornhill AH, Hope GS, Craven LA, Crisp MD (2012) Pollen morphology of the Myrtaceae. Part 4: tribes Kanieae, Myrteae and Tristanieae. Aust J Bot 60:260-289
80. Toudahl AB, Filho SAV, Souza GHB, Morais LD, Santos ODH, Jäger AK (2012) Chemical composition of the essential oil from Microlicia graveolens growing wild in Minas Gerais. Rev Bras Farmacogn 22:680-681
81. Unsicker SB, Kunert G, Gershenzon J (2009) Protective perfumes: the role of vegetative volatiles in plant defense against herbivores. Curr Opin Plant Biol 12:479-485
82. Van Poecke RMP, Posthumus MA, Dicke M (2001) Herbivore-induced volatile production by Arabidopsis thaliana leads to attraction of the parasitoid Cotesia rubecula: chemical, behavioral, and gene-expression analysis. J Chem Ecol 27:1911-1928 (Pubitemid 33032149)
83. Vickers CE, Gershenzon J, Lerdau MT, Loreto F (2009) A unified mechanism of action for volatile isoprenoids in plant abiotic stress. Nat Chem Biol 5:283-291
84. Wallis IR, Keszei A, Henery ML, Moran GF, Forrester R, Maintz J, Marsh KJ, Andrew RL, Foley WJ (2011) A chemical perspective on the evolution of variation in Eucalyptus globulus. Perspect Plant Ecol Evol Syst 13:305-318
85. Webb H, Lanfear R, Hamill J, Foley WJ, Külheim C (2013) The yield of essential oils in Melaleuca alternifolia (Myrtaceae) is regulated through transcript abundance of genes in the MEP pathway. PLoS One 8:e60631
86. Wilson PG (2011) Myrtaceae. In: Kubitzki K (ed) The families and genera of vascular plants, vol 10. Springer, Berlin, pp 212-271
87. Wilson P, O'Brien M, Heslewood M, Quinn C (2005) Relationships within Myrtaceae sensu lato based on a matK phylogeny. Plant Syst Evol 251:3-19 (Pubitemid 40560810)
88. Wise ML, Savage TJ, Katahira E, Croteau R (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. J Biol Chem 273:14891-14899 (Pubitemid 28272778)
89. World-Health-Organisation (1999) d-Limonene. In Some chemicals that cause tumours of the kidney or urinary bladder in rodents and some other substances: summary of data reported and evaluation. IARC, pp 307-327
90. Zhuang X, Köllner TG, Zhao N, Li G, Jiang Y, Zhu L, Ma J, Degenhardt J, Chen F (2012) Dynamic evolution of herbivore-induced sesquiterpene biosynthesis in sorghum and related grass crops. Plant J 69:70-80