Population divergence in the ontogenetic trajectories of foliar terpenes of a Eucalyptus species

Annals of Botany

Volumn 115, Issue 1, 2015, Pages 159-170

  Borzak, Christina L ^a   Potts, Brad M ^a   Davies, Noel W ^b   O'Reilly Wapstra, Julianne M ^a  

^a UNIVERSITY OF TASMANIA   (Australia)

^b UNIVERSITY OF TASMANIA   (Australia)

Author keywords

Chemical defence; Eucalyptus globules; Foliar terpenes; Genetic variation; Herbivory; Monoterpene; Ontogenetic trajectory; Plant ontogeny; Population divergence; Secondary metabolite; Seedlings; Sesquiterpene

Indexed keywords

DIVERGENCE; EVERGREEN TREE; EVOLUTIONARY BIOLOGY; GENETIC VARIATION; HERBIVORY; LEAF; MAMMAL; MONOTERPENE; ONTOGENY; SECONDARY METABOLITE; SEEDLING;

EUCALYPTUS; EUCALYPTUS GLOBULUS; MAMMALIA;

SESQUITERPENE; TERPENE;

EUCALYPTUS; GENETICS; METABOLISM; PLANT LEAF; SEEDLING;

EUCALYPTUS; MONOTERPENES; PLANT LEAVES; SEEDLINGS; SESQUITERPENES; TERPENES;

EID: 84979851895     PISSN: 03057364     EISSN: 10958290     Source Type: Journal    
DOI: 10.1093/aob/mcu222     Document Type: Article

References (93)

1. Andrew RL, Peakall R, Wallis IR, Wood JT, Knight EJ, Foley WJ. 2005 Marker-based quantitative genetics in the wild? The heritability and genetic correlation of chemical defenses in Eucalyptus. Genetics 171: 1989-1998
2. Barton KE. 2007. Early ontogenetic patterns in chemical defense in Plantago (Plantaginaceae): genetic variation and trade-offs. American Journal of Botany 94: 56-66
3. Barton KE, Hanley ME. 2013. Seedling-herbivore interactions: insights into plant defence and regeneration patterns. Annals of Botany 112: 643-650
4. Barton KE, Koricheva J. 2010. The ontogeny of plant defense and herbivory: characterizing general patterns using meta-Analysis. American Naturalist 175: 481-493
5. Boege K, Marquis RJ. 2005. Facing herbivory as you grow up: The ontogeny of resistance in plants. Trends in Ecologyamp; Evolution 20: 441-448
6. Boland DJ, Brophy JJ, House APN. 1991. Eucalyptus leaf oils-use, chemistry, distillation and marketing. Melbourne: ACIAR, CSIRO, Inkata Press
7. Brooker MIH, Kleinig DA. 1999. Field guide to eucalypts, Vol. 1, revised edn Melbourne: Bloomings Books
8. Brophy JJ, Southwell IA. 2002. Eucalyptus chemistry. In: JJW Coppen, ed Medicinal and aromatic plants-industrial profiles. eucalyptus: The genus Eucalyptus. London: Taylor & Francis Inc., 102-160
9. Bryant JP, Reichardt PB, Clausen TP, Provenza FD, Kuropat PJ. 1992 Woody plant-mammal interactions. In: GA Rosenthal, MR Berenbaum, eds. Herbivores: Their interactions with plant metabolites. New York: Academic Press, 344-371
10. De Martino L, Mancini E, De Almeida LFR, De Feo V. 2010. The antigerminative activity of twenty-seven monoterpenes. Molecules 15: 6630-6637
11. Dechaine JM, Brock MT, Iniguez-Luy FL, Weinig C. 2014. Quantitative trait loci environment interactions for plant morphology vary over ontogeny in Brassica rapa. New Phytologist 201: 657-669
12. Degenhardt J, Köllner TG, Gershenzon J. 2009. Monoterpene and sesquiterpene synthases and the origin of terpene skeletal diversity in plants Phytochemistry 70: 1621-1637
13. Dewick PM. 2009. Medicinal natural products: A biosynthetic approach, 3rd edn. Chichester: John Wiley & Sons Ltd Diggle PK. 2002. A developmental morphologist's perspective on plasticity Evolutionary Ecology 16: 267-283
14. Doran JC, Matheson AC. 1994. Genetic parameters and expected gains from selection for monoterpene yields in Petford Eucalyptus camaldulensis New Forests 8: 155-167
15. Dudai N, Lewinsohn E, Larkov O, et al. 1999. Dynamics of yield components and essential oil production in a commercial hybrid sage (Salvia officinalis Salvia fruticosa cv. Newe Ya'ar No. 4). Journal of Agricultural and Food Chemistry 47: 4341-4345
16. Dutkowski GW, Potts BM. 1999. Geographic patterns of genetic variation in Eucalyptus globulus ssp. globulus and a revised racial classification Australian Journal of Botany 47: 237-263
17. Edwards PB, Wanjura WJ, Brown WV, Dearn JM. 1990. Mosaic resistance in plants. Nature 347: 434
18. Edwards PB, Wanjura WJ, Brown WV. 1993. Selective herbivory by Christmas beetles in response to intraspecific variation in Eucalyptus terpenoids. Oecologia 95: 551-557
19. Elger A, Lemoine DG, Fenner M, Hanley ME. 2009. Plant ontogeny and chemical defence: older seedlings are better defended. Oikos 118: 767-773
20. Fähnrich A, Brosemann A, Teske L, Neumann M, Piechulla B. 2012 Synthesis of 'cineole cassette' monoterpenes in Nicotiana section Alatae: gene isolation, expression, functional characterization and phylogenetic analysis. Plant Molecular Biology 79: 537-553
21. Farrow RA, Floyd RB, Neumann FG. 1994. Inter-provenance variation in resistance of Eucalyptus globulus juvenile foliage to insect feeding Australian Forestry 57: 65-68
22. Goodger JQD, Woodrow IE. 2009. The influence of ontogeny on essential oil traits when micropropagating Eucalyptus polybractea. Forest Ecology and Management 258: 650-656
23. Goodger JQD, Gleadow RM, Woodrow IE. 2006. Growth cost and ontogenetic expression patterns of defence in cyanogenic Eucalyptus spp. Trees-Structure and Function 20: 757-765
24. Goodger JQD, Choo TYS, Woodrow IE. 2007. Ontogenetic and temporal trajectories of chemical defence in a cyanogenic eucalypt. Oecologia 153: 799-808
25. Goodger JQD, Heskes AM, Woodrow IE. 2013a. Contrasting ontogenetic trajectories for phenolic and terpenoid defences in Eucalyptus froggattii Annals of Botany 112: 651-659
26. Goodger JQD, Mitchell MC, Woodrow IE. 2013b. Differential patterns of mono-And sesquiterpenes with leaf ontogeny influence pharmaceutical oil yield in Eucalyptus polybractea R.T. Baker. Trees-Structure and Function 27: 511-521
27. Hanley ME. 1998. Seedling herbivory, community composition and plant life history traits. Perspectives in Plant Ecology, Evolution and Systematics 1: 191-205
28. Herms DA, Mattson WJ. 1992. The dilemma of plants: To grow or defend Quarterly Review of Biology 67: 283-335
29. Hoan RP, Ormond RA, Barton KE. 2014. Prickly poppies can get pricklier: ontogenetic patterns in the induction of physical defense traits. PLoS One 9: e96796
30. Holeski LM, Kearsley MJC, Whitham TG. 2009. Separating ontogenetic and environmental determination of resistance to herbivory in cottonwood Ecology 90: 2969-2973
31. Holeski LM, Hillstrom ML, Whitham TG, Lindroth RL. 2012. Relative importance of genetic, ontogenetic, induction, and seasonal variation in producing a multivariate defense phenotype in a foundation tree species Oecologia 170: 695-707
32. Huang M, Sanchez-Moreiras AM, Abel C, et al. 2012. The major volatile organic compound emitted from Arabidopsis thaliana flowers, the sesquiterpene (E)-b-caryophyllene, is a defense against a bacterial pathogen New Phytologist 193: 997-1008
33. Huang X, Xiao Y, Köllner TG, et al. 2013. Identification and characterization of (E)-b-caryophyllene synthase and a/b-pinene synthase potentially involved in constitutive and herbivore-induced terpene formation in cotton Plant Physiology and Biochemistry 73: 302-308
34. Huber D, Bohlmann J. 2004. Terpene synthases and the mediation of plantinsect ecological interactions by terpenoids: A mini-review. In: Q Cronck, J Whitton, R Ree, I Taylor, eds. Plant adaptation: molecular genetics and ecology. Ottawa, Ontario: NRC Research Press, 70-81
35. Hudson CJ, Freeman JS, Jones RC, et al. 2014. Genetic control of heterochrony in Eucalyptus globulus. G3: Genes, Genomes, Genetics 4: 1235-1245
36. Iason GR, O'Reilly-Wapstra JM, Brewer MJ, Summers RW, Moore BD 2011. Do multiple herbivores maintain chemical diversity of scots pine monoterpenes? Philosophical Transactions of the Royal Society B: Biological Sciences 366: 1337-1345
37. Ibanez S, Dötterl S, Anstett MC, et al. 2010. The role of volatile organic compounds, morphology and pigments of globeflowers in the attraction of their specific pollinating flies. New Phytologist 188: 451-463
38. Jones RC, Steane DA, Lavery M, Vaillancourt RE, Potts BM. 2013. Multiple evolutionary processes drive the patterns of genetic differentiation in a forest tree species complex. Ecology and Evolution 3: 1-17
39. Jordan GJ, Potts BM, Wiltshire RJE. 1999. Strong, independent, quantitative genetic control of the timing of vegetative phase change and first flowering in Eucalyptus globulus ssp. globulus (Tasmanian Blue Gum). Heredity 83: 179-187
40. Jordan GJ, Potts BM, Chalmers P, Wiltshire RJE. 2000. Quantitative genetic evidence that the timing of vegetative phase change in Eucalyptus globulus ssp. globulus is an adaptive trait. Australian Journal of Botany 48: 561-567
41. Kelly D, Sork VL. 2002. Mast seeding in perennial plants: why, how, where? Annual Review of Ecology and Systematics 33: 427-447
42. 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
43. Köllner TG, Held M, Lenk C, et al. 2008. A maize (E)-b-caryophyllene synthase implicated in indirect defense responses against herbivores is not expressed in most American maize varieties. Plant Cell 20: 482-494
44. Kramer R, Abraham WR. 2012. Volatile sesquiterpenes from fungi: what are they good for? Phytochemistry Reviews 11: 15-37
45. Külheim C, Yeoh SH, Wallis IR, Laffan S, Moran GF, Foley WJ. 2011 The molecular basis of quantitative variation in foliar secondary metabolites in Eucalyptus globulus. New Phytologist 191: 1041-1053
46. Lawler IR, Eschler BM, Schliebs DM, FoleyWJ. 1999. Relationship between chemical functional groups on Eucalyptus secondary metabolites and their effectiveness as marsupial antifeedants. Journal of Chemical Ecology 25: 2561-2573
47. Lawler IR, FoleyWJ, Eschler BM. 2000. Foliar concentration of a single toxin creates habitat patchiness for a marsupial folivore. Ecology 81: 1327-1338
48. Lawrence R, Potts BM, Whitham TG. 2003. Relative importance of plant ontogeny, host genetic variation, and leaf age for a common herbivore Ecology 84: 1171-1178
49. Leach GJ, Whiffin T. 1989. Ontogenetic, seasonal and diurnal variation in leaf volatile oils and leaf phenolics of Angophora costata. Australian Systematic Botany 2: 99-111
50. Ludley KE, Robinson CH, Jickells S, Chamberlain PM, Whitaker J. 2009 Potential for monoterpenes to affect ectomycorrhizal and saprotrophic fungal activity in coniferous forests is revealed by novel experimental system Soil Biology and Biochemistry 41: 117-124
51. Massad TJ. 2013. Ontogenetic differences of herbivory on woody and herbaceous plants: A meta-Analysis demonstrating unique effects of herbivory on the young and the old, the slow and the fast Oecologia 172: 1-10
52. McArthur C, Loney P, Davies NW, Jordan GJ. 2010. Early ontogenetic trajectories vary among defence chemicals in seedlings of a fast-growing eucalypt. Austral Ecology 35: 157-166
53. Moore BD, Andrew RL, Külheim C, FoleyWJ. 2014. Explaining intraspecific diversity in plant secondary metabolites in an ecological context New Phytologist 201: 733-750
54. Myburg AA, Grattapaglia D, Tuskan GA, et al. 2014. The genome of Eucalyptus grandis. Nature 510: 356-362
55. O'Reilly-Wapstra JM, McArthur C, Potts BM. 2002. Genetic variation in resistance of Eucalyptus globulus to marsupial browsers. Oecologia 130: 289-296
56. O'Reilly-Wapstra JM, McArthur C, Potts BM. 2004. Linking plant genotype, plant defensive chemistry and mammal browsing in a Eucalyptus species Functional Ecology 18: 677-684
57. O'Reilly-Wapstra JM, Potts BM, McArthur C, Davies NW. 2005a. Effects of nutrient variability on the genetic-based resistance of Eucalyptus globulus to a mammalian herbivore and on plant defensive chemistry. Oecologia 142: 597-605
58. O'Reilly-Wapstra JM, Potts BM, McArthur C, Davies NW, Tilyard P 2005b. Inheritance of resistance to mammalian herbivores and of plant defensive chemistry in a Eucalyptus species. Journal of Chemical Ecology 31: 519-537
59. O'Reilly-Wapstra JM, Humphreys JR, Potts BM. 2007. Stability of geneticbased defensive chemistry across life stages in a Eucalyptus species Journal of Chemical Ecology 33: 1876-1884
60. O'Reilly-Wapstra JM, Freeman JS, Davies NW, Vaillancourt RE, Fitzgerald H, Potts BM. 2011. Quantitative trait loci for foliar terpenes in a global eucalypt species. Tree Genetics and Genomes 7: 485-498
61. O'Reilly-Wapstra JM, McArthur C, Potts BM. 2012. Natural selection for anti-herbivore plant secondary metabolites: A Eucalyptus system. In: GI Iason, M Dicke, S Hartley, eds. The ecology of plant secondary metabolites: genes to global processes. London: Cambridge University Press, 10-33
62. O'Reilly-Wapstra JM, Miller AM, HamiltonMG, Williams D, Glancy-Dean N, Potts BM. 2013. Chemical variation in a dominant tree species: population divergence, selection and genetic stability across environments. PLoS One 8: e58416
63. Ormeno E, Céspedes B, Sánchez IA, et al. 2009. The relationship between terpenes and flammability of leaf litter. Forest Ecology and Management 257: 471-482
64. Östrand F, Wallis IR, Davies NW, Matsuki M, Steinbauer MJ. 2008. Causes and consequences of host expansion by Mnesampela privata. Journal of Chemical Ecology 34: 153-167
65. Ott DS, Yanchuk AD, Huber DPW, Wallin KF. 2011. Genetic variation of Lodgepole pine, Pinus contorta var. latifolia, chemical and physical defenses that affect Mountain pine beetle, Dendroctonus ponderosae, attack and tree mortality. Journal of Chemical Ecology 37: 1002-1012
66. Padovan A, Keszei A, Foley WJ, Külheim C. 2013. Differences in gene expression within a striking phenotypic mosaic Eucalyptus tree that varies in susceptibility to herbivory. BMC Plant Biology 13: 29
67. Piechowski D, Dötterl S, Gottsberger G. 2011. Pollination biology and floral scent chemistry of the Neotropical chiropterophilous Parkia pendula. Plant Biology 12: 172-182
68. Potts BM, Jordan GJ. 1994. The spatial pattern and scale of variation in Eucalyptus globulus ssp. globulus: variation in seedling abnormalities and early growth. Australian Journal of Botany 42: 471-492
69. Quintero C, BowersMD. 2013. Effects of insect herbivory on induced chemical defences and compensation during early plant development in Penstemon virgatus. Annals of Botany 112: 661-669
70. Quintero C, Barton KE, Boege K. 2013. The ontogeny of plant indirect defenses Perspectives in Plant Ecology, Evolution and Systematics 15: 245-254
71. Rehill BJ, Whitham TG, Martinsen GD, Schweitzer JA, Bailey JK, Lindroth RL. 2006. Developmental trajectories in cottonwood phytochemistry Journal of Chemical Ecology 32: 2269-2285
72. Reisenman CE, Riffell JA, Bernays EA, Hildebrand JG. 2010. Antagonistic effects of floral scent in an insect-plant interaction. Proceedings of the Royal Society B: Biological Sciences 277: 2371-2379
73. Sabulal B, Dan M, Anil JJ, et al. 2006. Caryophyllene-rich rhizome oil of Zingiber nimmonii from South India: Chemical characterization and antimicrobial activity. Phytochemistry 67: 2469-2473
74. Safaei-Ghomi J, Batooli H. 2010. Chemical composition and antimicrobial activity of the volatile oil of Eucalyptus sargentii Maiden cultivated in central Iran. International Journal of Green Pharmacy 4: 174-177
75. Silva SM, Abe SY, Murakami FS, Frensch G, Marques FA, Nakashima T 2011. Essential oils from different plant parts of Eucalyptus cinerea F
76. Muell. ex Benth. (Myrtaceae) as a source of 1, 8-cineole and their bioactivities Pharmaceuticals 4: 1535-1550
77. Simmons D, Parsons RF. 1987. Seasonal variation in the volatile leaf oils of two Eucalyptus species. Biochemical Systematics and Ecology 15: 209-215
78. Simms EL, Fritz RS. 1990. The ecology and evolution of host-plant resistance to insects. Trends in Ecology and Evolution 5: 356-360
79. Singer MC, McBride CS. 2012. Geographic mosaics of species' association: A definition and an example driven by plant-insect phenological synchrony Ecology 93: 2658-2673
80. Singh HP, Kaur S, Mittal S, Batish DR, Kohli RK. 2009. Essential oil of Artemisia scoparia inhibits plant growth by generating reactive oxygen species and causing oxidative damage. Journal of Chemical Ecology 35: 154-162
81. Steane DA, Conod N, Jones RC, Vaillancourt RE, Potts BM. 2006. A comparative analysis of population structure of a forest tree, Eucalyptus globulus (Myrtaceae), using microsatellite markers and quantitative traits. Tree Genetics and Genomes 2: 30-38
82. Steinbauer MJ. 2010. Latitudinal trends in foliar oils of eucalypts: environmental correlates and diversity of chrysomelid leaf-beetles. Austral Ecology 35: 204-213
83. Steinbauer MJ, Schiestl FP, Davies NW. 2004. Monoterpenes and epicuticular waxes help female autumn gummoth differentiate between waxy and glossy Eucalyptus and leaves of different ages. Journal of Chemical Ecology 30: 1117-1142
84. Wallis IR, Watson ML, Foley WJ. 2002. Secondary metabolites in Eucalyptus melliodora: field distribution and laboratory feeding choices by a generalist herbivore, the common brushtail possum. Australian Journal of Zoology 50: 507-519
85. Wallis IR, Keszei A, Henery ML, et al. 2011. A chemical perspective on the evolution of variation in Eucalyptus globulus. Perspectives in Plant Ecology, Evolution and Systematics 13: 305-318
86. Wang G, Tian L, Aziz N, et al. 2008. Terpene biosynthesis in glandular trichomes of hop. Plant Physiology 148: 1254-1266
87. Wiggins NL, McArthur C, McLean S, Boyle, R. 2003. Effects of two plant secondary metabolites, cineole and gallic acid, on nightly feeding patterns of the common brushtail possum. Journal of Chemical Ecology 29: 1447-1464
88. Wiggins NL, McArthur C, Davies NW. 2006. Diet switching in a generalist mammalian folivore: fundamental to maximising intake. Oecologia 147: 650-657
89. 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 Williams JE, Brooker MIH (eds) 1997 Eucalypts: An introduction Cambridge: Cambridge University Press
90. Wiltshire RJE, Potts BM, Reid JB. 1998. Genetic control of reproductive and vegetative phase change in the Eucalyptus risdonii-E.Tenuiramis complex Australian Journal of Botany 46: 45-63
91. Xiao Y, Wang Q, Erb M, et al. 2012. Specific herbivore-induced volatiles defend plants and determine insect community composition in the field Ecology Letters 15: 1130-1139
92. Yang CQ, Wu XM, Ruan JX, et al. 2013. Isolation and characterization of terpene synthases in cotton (Gossypium hirsutum). Phytochemistry 96: 46-56
93. Zhao F, Shu L, Wang Q, WangM, Tian X. 2011. Emissions of volatile organic compounds from heated needles and twigs of Pinus pumila. Journal of Forestry Research 22: 243-248