Explaining intraspecific diversity in plant secondary metabolites in an ecological context

New Phytologist

Volumn 201, Issue 3, 2014, Pages 733-750

  Moore, Ben D ^a   Andrew, Rose L ^b   Külheim, Carsten ^c   Foley, William J ^c  

^a WESTERN SYDNEY UNIVERSITY   (Australia)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

Biosynthesis; Evolvability; Herbivore; Heritability; Plant defence; Transgenic; Variance

Indexed keywords

GENETIC VARIATION; HERBIVORE; HERITABILITY; INTRASPECIFIC VARIATION; LIFE HISTORY TRAIT; MOLECULAR ANALYSIS; ONTOGENY; PLANT DEFENSE; POLYMORPHISM; SECONDARY METABOLITE; SPATIOTEMPORAL ANALYSIS;

PLANT MEDICINAL PRODUCT;

BIODIVERSITY; BIOSYNTHESIS; EVOLUTION; EVOLVABILITY; GENETICS; HERBIVORE; HERITABILITY; METABOLISM; PLANT DEFENCE; REVIEW; SECONDARY METABOLISM; SPECIES DIFFERENCE; TRANSGENIC; VARIANCE;

BIOSYNTHESIS; EVOLVABILITY; HERBIVORE; HERITABILITY; PLANT DEFENCE; TRANSGENIC; VARIANCE;

BIODIVERSITY; BIOLOGICAL EVOLUTION; BIOSYNTHETIC PATHWAYS; PHYTOCHEMICALS; SECONDARY METABOLISM; SPECIES SPECIFICITY;

EID: 84891900884     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12526     Document Type: Review

References (216)

1. Adler LS, Schmitt J, Bowers MD. 1995. Genetic variation in defensive chemistry in Plantago lanceolata (Plantaginaceae) and its effect on the specialist herbivore Junionia coenia (Nymphalidae). Oecologia 101: 75-85.
2. Agrawal AA. 2011. Current trends in the evolutionary ecology of plant defence. Functional Ecology 25: 420-432.
3. Agrawal AA, Conner JK, Johnson MTJ, Wallsgrove R. 2002. Ecological genetics of an induced plant defense against herbivores: additive genetic variance and costs of phenotypic plasticity. Evolution 56: 2206-2213.
4. Agrawal AA, Hastings AP, Johnson MTJ, Maron JJ, Salminen JP. 2012. Insect herbivores drive real-time ecological and evolutionary change in plant populations. Science 338: 113-116.
5. Aharoni A, Gaidukov L, Khersonsky O, Gould SM, Roodveldt C, Tawfik DS. 2005. The 'evolvability' of promiscuous protein functions. Nature Genetics 37: 73-76.
6. Alba C, Bowers MD, Blumenthal D, Hufbauer R. 2011. Evolution of growth but not structural or chemical defense in Verbascum thapsus (common mullein) following introduction to North America. Biological Invasions 13: 2379-2389.
7. Andrew RL, Peakall R, Wallis IR, Foley WJ. 2007. Spatial distribution of defense chemicals and markers and the maintenance of chemical variation. Ecology 88: 716-728.
8. Anssour S, Baldwin IT. 2010. Variation in antiherbivore defense responses in synthetic Nicotiana allopolyploids correlates with changes in uniparental patterns of gene expression. Plant Physiology 153: 1907-1918.
9. Appel HM. 1993. Phenolics in ecological interactions- the importance of oxidation. Journal of Chemical Ecology 19: 1521-1552.
10. Au J, Marsh KJ, Wallis IR, Foley WJ. 2013. Whole-body protein turnover reveals the cost of detoxification of secondary metabolites in a vertebrate browser. Journal of Comparative Physiology B. doi:10.1007/s00360-013-0754-3.
11. Baldwin IT. 1998. Jasmonate-induced responses are costly but benefit plants under attack in native populations. Proceedings of the National Academy of Sciences, USA 95: 8113-8118.
12. Baldwin IT, Halitschke R, Paschold A, von Dahl CC, Preston CA. 2006. Volatile signaling in plant-plant interactions: "Talking trees" in the genomics era. Science 311: 812-815.
13. Barbehenn RV, Constabel CP. 2011. Tannins in plant-herbivore interactions. Phytochemistry 72: 1551-1565.
14. Barton KE, Koricheva J. 2010. The ontogeny of plant defense and herbivory: characterizing general patterns using meta-analysis. American Naturalist 175: 481-493.
15. Becerra JX, Noge K, Venable DL. 2009. Macroevolutionary chemical escalation in an ancient plant-herbivore arms race. Proceedings of the National Academy of Sciences, USA 106: 18062-18066.
16. Bednarek P, Piślewska-Bednarek M, Svatoš M, Schneider B, Doubský J, Mansurova M, Humphry M, Consonni C, Panstruga R, Sanchez-Vallet A et al. 2009. A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense. Science 323: 101-106.
17. Bell G. 1982. The masterpiece of nature: the evolution and genetics of sexuality. London, UK: Croon Helm.
18. Benderoth M, Pfalz M, Kroymann J. 2009. Methylthioalkylmalate synthases: genetics, ecology and evolution. Phytochemistry Reviews 8: 255-268.
19. 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, USA 103: 9118-9123.
20. Bergvall UA, Leimar O. 2005. Plant secondary compounds and the frequency of food types affect food choice by mammalian herbivores. Ecology 86: 2450-2460.
21. Bohlmann J, Meyer-Gauen G, Croteau R. 1998. Plant terpenoid synthases: molecular biology and phylogenetic analysis. Proceedings of the National Academy of Sciences, USA 95: 4126-4133.
22. Bossdorf O, Auge H, Lafuma L, Rogers WE, Siemann E, Prati D. 2005. Phenotypic and genetic differentiation between native and introduced plant populations. Oecologia 144: 1-11.
23. Bowers JE, Chapman BA, Rong J, Paterson AH. 2003. Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422: 433-438.
24. Boyle RR, McLean S. 2004. Constraint of feeding by chronic ingestion of 1, 8-cineole in the brushtail possum (Trichosurus vulpecula). Journal Chemical Ecology 30: 757-775.
25. Bryant JP, Chapin FS III, Klein DR. 1983. Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40: 357-368.
26. Buckingham J. 1994. Dictionary of natural products. London, UK: Chapman and Hall.
27. Burchard P, Bilger W, Weissenböck G. 2000. Contribution of hydroxycinnamates and flavonoids to epidermal shielding of UV-A and UV-B radiation in developing rye primary leaves as assessed by ultraviolet-induced chlorophyll fluorescence measurements. Plant, Cell & Environment 23: 1373-1380.
28. Cacace S, Schroder G, Wehinger E, Strack D, Schmidt J, Schroder J. 2003. A flavonol O-methyltransferase from Catharanthus roseus performing two sequential methylations. Phytochemistry 62: 127-137.
29. Cantelo WW, Sanford LL. 1984. Insect population response to mixed and uniform plantings of resistant and susceptible plant material. Environmental Entomology 13: 1443-1445.
30. Carmona D, Lajeunesse MJ, Johnson MTJ. 2011. Plant traits that predict resistance to herbivores. Functional Ecology 25: 358-367.
31. Chen F, Tholl D, Bohlmann J, Pichersky E. 2011. The family of terpene synthases in plants: a mid-size family of genes for specialized metabolism that is highly diversified throughout the kingdom. Plant Journal 66: 212-229.
32. Chrispeels MJ, Varner JE. 1967. Hormonal control of enzyme synthesis: On the mode of action of gibberellic acid and abscisin in aleurone layers of barley. Plant Physiology 42: 1008-1016.
33. Clark JS. 2010. Individuals and the variation needed for high species diversity in forest trees. Science 327: 1129-1132.
34. Colquhoun TA. 2012. Delineating compartmentalized control of phenylpropanoid metabolism. Journal of Chemical Ecology 38: 230.
35. Connell JH 1971. On the role of natural enemies in preventing competitive exclusion in some marine animals and in rainforest trees. In: Den Boer PJ, Gradwell GR, eds. Dynamics of population. Wageningen, the Netherlands: Pudoc, 298-312.
36. Crocoll C, Asbach J, Novak J, Gershenzon J, Degenhardt J. 2010. Terpene synthases of oregano (Origanum vulgare L.) and their roles in the pathway and regulation of terpene biosynthesis. Plant Molecular Biology 73: 587-603.
37. Crutsinger GM, Collins MD, Fordyce JA, Gompert Z, Nice CC, Sanders NJ. 2006. Plant genotypic diversity predicts community structure and governs an ecosystem process. Science 313: 966-968.
38. Dall SRX, Bell AM, Bolnick DI, Ratnieks FLW. 2012. An evolutionary ecology of individual differences. Ecology Letters 15: 1189-1198.
39. Debat V, David P. 2001. Mapping phenotypes: canalization, plasticity and developmental stability. Trends in Ecology & Evolution 16: 555-561.
40. 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.
41. Degenhardt J, Hiltpold I, Kollner TG, Frey M, Gierl A, Gershenzon J, Hibbard BE, Ellersieck MR, Turlings TCJ. 2009. Restoring a maize root signal that attracts insect-killing nematodes to control a major pest. Proceedings of the National Academy of Sciences, USA 106: 13213-13218.
42. Denno RF, McClure MS. 1983 Variable plants and herbivores in natural and managed systems. New York, NY, USA: Academic Press.
43. Dixon RA, Paiva NL. 1995. Stress-induced phenylpropanoid metabolism. The Plant Cell 7: 1085-1097.
44. Doorduin LJ, Vrieling K. 2011. A review of the phytochemical support for the shifting defence hypothesis. Phytochemistry Reviews 10: 99-106.
45. Driebe EM, Whitham TG. 2000. Cottonwood hybridization affects tannin and nitrogen content of leaf litter and alters decomposition. Oecologia 123: 99-107.
46. Dudareva N, Pichersky E, Gershenzon J. 2004. Biochemistry of plant volatiles. Plant Physiology 135: 1893-1902.
47. Emerson SE, Brown JS, Whelan CJ, Schmidt KA. 2012. Scale-dependent neighborhood effects: shared doom and associational refuge. Oecologia 168: 659-670.
48. Endara MJ, Coley PD. 2011. The resource availability hypothesis revisited: a meta-analysis. Functional Ecology 25: 389-398.
49. Engelberth J, Alborn HT, Schmelz EA, Tumlinson JH. 2004. Airborne signals prime plants against insect herbivore attack. Proceedings of the National Academy of Sciences, USA 101: 1781-1785.
50. Erb M, Meldau S, Howe GA. 2012. Role of phytohormones in insect-specific plant reactions. Trends in Plant Science 17: 250-259.
51. Feller A, Martens S. 2012. Identification and characterization of early pathway genes of ellagitannin biosynthesis in strawberry (Fragaria vesca). 6th Rosaceous Genomics Conference (RGC6).
52. Felton AM, Felton A, Raubenheimer D, Simpson SJ, Foley WJ, Wood JT, Wallis IR, Lindenmayer DB. 2009. Protein content of diets dictates the daily energy intake of a free-ranging primate. Behavioral Ecology 20: 685-690.
53. Feys BJF, Benedetti CE, Penfold CN, Turner JG. 1994. Arabadopsis mutants selected for resistance to the phytotoxin coronatine are male-sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. The Plant Cell 6: 751-759.
54. Fraenkel GS. 1959. Raison d'être of secondary plant substances. Science 129: 1466-1470.
55. Franks SJ, Wheeler GS, Goodnight C. 2012. Genetic variation and evolution of secondary compounds in native and introduced poulations of the invasive plant Melaleuca quinquenervia. Evolution 66: 1398-1412.
56. Fraser CM, Chapple C. 2011. The phenylpropanoid pathway in Arabidopsis. Arabidopsis Book 9: e0152.
57. Garcia-Gonzalez F, Simmons LW, Tomkins JL, Kotiaho JS, Evans JP. 2012. Comparing evolvabilities: common errors surrounding the calculation and use of coefficients of additive genetic variation. Evolution 66: 2341-2349.
58. Gavrilets S. 1999. A dynamical theory of speciation on holey adaptive landscapes. American Naturalist 154: 1-22.
59. Geber MA, Griffen LR. 2003. Inheritance and natural selection on functional traits. International Journal of Plant Sciences 164: S21-S42.
60. Gleadow RM, Vecchies AC, Woodrow IE. 2003. Cyanogenic Eucalyptus nobilis is polymorphic for both prunasin and specific beta-glucosidases. Phytochemistry 63: 699-704.
61. Halkier BA, Gershenzon J. 2006. Biology and biochemistry of glucosinolates. Annual Review of Plant Biology 57: 303-333.
62. Halkier BA, Möller BL. 1989. Biosynthesis of the cyanogenic glucoside dhurrin in seedlings of Sorghum bicolor (L.) Moench and partial purification of the enzyme system Involved. Plant Physiology 90: 1552-1559.
63. Hall DE, Robert JA, Keeling CI, Domanski D, Quesada AL, Jancsik S, Kuzyk MA, Hamberger B, Borchers CH, 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 Journal 65: 936-948.
64. Hall MC, Dworkin I, Ungerer MC, Purugganan M. 2007. Genetics of microenvironmental canalization in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 104: 13717-13722.
65. Hamberger B, Ohnishi T, Seguin A, Bohlmann J. 2011. Evolution of diterpene metabolism: Sitka Spruce CYP720B4 catalyzes multiple oxidations in resin acid biosynthesis of conifer defense against insects. Plant Physiology 157: 1677-1695.
66. Hamilton JG, Zangerl AR, DeLucia EH, Berenbaum MR. 2001. The carbon-nutrient balance hypothesis: its rise and fall. Ecology Letters 4: 86-95.
67. Hamilton WD, Brown SP. 2001. Autumn tree colours as a handicap signal. Proceedings of the Royal Society B: Biological Sciences 268: 1489-1493.
68. Hansen TF, Pélabon C, Houle D. 2011. Heritability is not evolvability. Evolutionary Biology 38: 258-277.
69. Hare JF, Eisner T. 1993. Pyrrolizidine alkaloid deters ant predators of Utetheisa ornatrix eggs - effects of alkaloid concentration, oxidation state and prior exposure of ants to alkaloid-laden prey. Oecologia 96: 9-18.
70. Hartl M, Giri AP, Kaur H, Baldwin IT. 2010. Serine protease inhibitors specifically defend Solanum nigrum against generalist herbivores but do not influence plant growth and development. The Plant Cell 22: 4158-4175.
71. Haslam E. 1986. Secondary metabolism - facts and fiction. Natural Product Reports 3: 217-249
72. Haviola S, Neuvonen S, Rantala MJ, Saikkonen K, Salminen JP, Saloniemi I, Yang SY, Ruuhola T. 2012. Genetic and environmental factors behind foliar chemistry of the mature mountain birch. Journal of Chemical Ecology 38: 902-913.
73. Hereford J. 2009. A quantitative survey of local adaptation and fitness trade-offs. American Naturalist 173: 579-588.
74. Hill WG, Mulder HA. 2010. Genetic analysis of environmental variation. Genetics Research 92: 381-395.
75. Hill WG, Zhang X-S. 2004. Effects on phenotypic variability of directional selection arising through genetic differences in residual variability. Genetics Research 83: 121-132.
76. Hinman VF, Davidson EH. 2007. Evolutionary plasticity of developmental gene regulatory network architecture. Proceedings of the National Academy of Sciences, USA 104: 19404-19409.
77. Hjalten J, Danell K, Lundberg P. 1993. Herbivore avoidance by association: vole and hare utilization of woody plants. Oikos 68: 125-131.
78. Holeski LM, Hillstrom ML, Whitham TG, Lindroth RL. 2012a. Relative importance of genetic, ontogenetic, induction, and seasonal variation in producing a multivariate defense phenotype in a foundation tree species. Oecologia 170: 695-707.
79. Holeski LM, Jander G, Agrawal AA. 2012b. Transgenerational defense induction and epigenetic inheritance in plants. Trends in Ecology & Evolution 27: 618-626.
80. Holton TA, Cornish EC. 1995. Genetics and biochemistry of anthocyanin biosynthesis. The Plant Cell 7: 1071-1083.
81. Houle D. 1992. Comparing evolvability and variability of quantitative traits. Genetics 130: 195-204.
82. Hughes AR, Stachowicz JJ. 2004. Genetic diversity enhances the resistance of a seagrass ecosystem to disturbance. Proceedings of the National Academy of Sciences, USA 101: 8998-9002.
83. Hughes MA. 1991. The cyanogenic polymorphism in Trifolium repens L. (white clover). Heredity 66: 105-115.
84. Hyatt LA, Rosenberg MS, Howard TG, Bole G, Fang W, Anastasia J, Brown K, Grella R, Hinman K, Kurdziel JP et al. 2003. The distance dependence prediction of the Janzen-Connell hypothesis: a meta-analysis. Oikos 103: 590-602.
85. Iason GR, Lennon JJ, Pakeman RJ, Thoss V, Beaton JK, Sim DA, Elston DA. 2005. Does chemical composition of individual Scots pine trees determine the biodiversity of their associated ground vegetation? Ecology Letters 8: 364-369.
86. Iason GR, O'Reilly-Wapstra JM, Brewer MJ, Summers RW, Moore B. 2011. Do multiple herbivores maintain chemical diversity of Scots pine monoterpenes? Philosophical Transactions of the Royal Society of London, Series B-Biological Sciences 366: 1337-1345.
87. Irmisch S, Krause ST, Kunert G, Gershenzon J, Degenhardt J, Köllner TG. 2012. The organ-specific expression of terpene synthase genes contributes to the terpene hydrocarbon composition of chamomile essential oils. BMC Plant Biology 12: 84.
88. Irwin RE, Adler LS, Brody AK. 2004. The dual role of floral traits: pollinator attraction and plant defense. Ecology 85: 1503-1511.
89. Jander G, Clay N. 2011. New synthesis - plant defense signaling: new opportunities for studying chemical diversity. Journal of Chemical Ecology 37: 429.
90. Janz N, Bergstrom A, Johansson J. 2005. Frequency dependence of host plant choice within and between patches: a large cage experiment. Evolutionary Ecology 19: 289-302.
91. Janzen DH. 1970. Herbivores and the number of tree species in tropical forests. The American Naturalist 104: 501-528.
92. Jensen J. 1906. On the convex functions and inequalities between mean values. Acta Mathematica 30: 175-193.
93. Jiménez-Gómez J, Corwin JA, Joseph B, Maloof JN, Kliebenstein DJ. 2011. Genomic analysis of QTLs and genes altering natural variation in stochastic noise. PLOS Genetics 7: e1002295.
94. Johnson MTJ, Agrawal AA, Maron JL, Salminen JP. 2009. Heritability, covariation and natural selection on 24 traits of common evening primrose (Oenothera biennis) from a field experiment. Journal of Evolutionary Biology 22: 1295-1307.
95. Johnson MTJ, Lajeunesse MJ, Agrawal AA. 2006. Additive and interactive effects of plant genotypic diversity on arthropod communities and plant fitness. Ecology Letters 9: 24-34.
96. Jones CG, Firn RD. 1991. On the evolution of plant secondary chemical diversity. Philosophical Transactions of the Royal Society of London, Series B-Biological Sciences 333: 273-280.
97. Jones PR, Möller BL, Hoj PB. 1999. The UDP-glucose:p-hydroxymandelonitrile-O-glucosyltransferase that catalyzes the last step in synthesis of the cyanogenic glucoside dhurrin in Sorghum bicolor. Isolation, cloning, heterologous expression, and substrate specificity. Journal of Biological Chemistry 274: 35483-35491.
98. Jung V, Violle C, Mondy C, Hoffmann L, Muller S. 2010. Intraspecific variability and trait-based community assembly. Journal of Ecology 98: 1134-1140.
99. Kaltz O, Shykoff JA. 1998. Local adaptation in host-parasite systems. Heredity 81: 361-370.
100. Kampranis SC, Ioannidis D, Purvis A, Mahrez W, Ninga E, Katerelos NA, Anssour S, Dunwell JM, Degenhardt J, Makris AM et al. 2007. Rational conversion of substrate and product specificity in a Salvia monoterpene synthase: structural insights into the evolution of terpene synthase function. The Plant Cell 19: 1994-2005.
101. Karban R. 2011. The ecology and evolution of induced resistance against herbivores. Functional Ecology 25: 339-347.
102. Karban R, Agrawal AA, Mangel M. 1997. The benefits of induced defenses against herbivores. Ecology 78: 1351-1355.
103. Karban R, Baldwin IT. 1997. Induced responses to herbivory. Chicago, IL, USA: University of Chicago Press.
104. Katz A, Lifshitz Y, Bab-Dinitz E, Kapri-Pardes E, Goldshleger R, Tal DM, SJ. K. 2010. Selectivity of digitalis glycosides for isoforms of human Na, K-ATPase. Journal of Biological Chemistry 285: 19582-19592.
105. Keeling CI, Bohlmann J. 2006. Diterpene resin acids in conifers. Phytochemistry 67: 2415-2423.
106. Kessler A, Baldwin IT. 2002. Plant responses to insect herbivory: the emerging molecular analysis. Annual Review of Plant Biology 53: 299-328.
107. Kessler D, Bhattacharya S, Diezel C, Rothe E, Gase K, Schottner M, Baldwin IT. 2012. Unpredictability of nectar nicotine promotes outcrossing by hummingbirds in Nicotiana attenuata. Plant Journal 71: 529-538.
108. Kessler D, Gase K, Baldwin IT. 2008. Field experiments with transformed plants reveal the sense of floral scents. Science 321: 1200-1202.
109. Kim SG, Yon F, Gaquerel E, Gulati J, Baldwin IT. 2011. Tissue specific diurnal rhythms of metabolites and their regulation during herbivore attack in a native tobacco, Nicotiana attenuata. PLoS One 6: e26214.
110. Kliebenstein DJ. 2008. A role for gene duplication and natural variation of gene expression in the evolution of metabolism. PLoS One 3: e1838.
111. Kliebenstein DJ, Kroymann J, Brown P, Figuth A, Pedersen D, Gershenzon J, Mitchell-Olds T. 2001a. Genetic control of natural variation in Arabidopsis glucosinolate accumulation. Plant Physiology 126: 811-825.
112. Kliebenstein DJ, Lambrix VM, Reichelt M, Gershenzon J, Mitchell-Olds T. 2001b. Gene duplication in the diversification of secondary metabolism: tandem 2-oxoglutarate-dependent dioxygenases control glucosinolate biosynthesis in Arabidopsis. The Plant Cell 13: 681-693.
113. Kliebenstein DJ, Rowe HC, Denby KJ. 2005. Secondary metabolites influence Arabidopsis/Botrytis interactions: variation in host production and pathogen susceptibility. Plant Journal 44: 25-36.
114. Kollner TG, Held M, Lenk C, Hiltpold I, Turlings TCJ, Gershenzon J, Degenhardt J. 2008. A maize (E)-beta-caryophyllene synthase implicated in indirect defense responses against herbivores is not expressed in most American maize varieties. The Plant Cell 20: 482-494.
115. Koricheva J. 1999. Interpreting phenotypic variation in plant allelochemistry: problems with the use of concentrations. Oecologia 119: 467-473.
116. Kotowska AM, Cahill JF, Keddie BA. 2010. Plant genetic diversity yields increased plant productivity and herbivore performance. Journal of Ecology 98: 237-245.
117. Kroymann J. 2011. Natural diversity and adaptation in plant secondary metabolism. Current Opinion in Plant Biology 14: 246-251.
118. Kroymann J, Donnerhacke S, Schnabelrauch D, Mitchell-Olds T. 2003. Evolutionary dynamics of an Arabidopsis insect resistance quantitative trait locus. Proceedings of the National Academy of Sciences, USA 100: 14587-14592.
119. Kroymann J, Mitchell-Olds T. 2005. Epistasis and balanced polymorphism influencing complex trait variation. Nature 435: 95-98.
120. 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.
121. Kursar TA, Dexter KG, Lokvam J, Pennington RT, Richardson JE, Weber MG, Murakami ET, Drake C, McGregor R, Coley PD. 2009. The evolution of antiherbivore defenses and their contribution to species coexistence in the tropical tree genus Inga. Proceedings of the National Academy of Sciences, USA 106: 18073-18078.
122. Lambrix V, Reichelt M, Mitchell-Olds T, Kliebenstein DJ, Gershenzon J. 2001. The Arabidopsis epithiospecifier protein promotes the hydrolysis of glucosinolates to nitriles and influences Trichoplusia ni herbivory. The Plant Cell 13: 2793-2807.
123. Lamont BB. 1993. Injury-induced cyanogenesis in vegetative and reproductive parts of 2 Grevillia species and their F1 hybrid. Annals of Botany 71: 537-542.
124. Langenheim JH, Stubblebein WH. 1983. Variation in leaf resin composition between parent tree and progeny in Hymenaea: implications for herbivory in the humid tropics. Biochemical Systematics and Ecology 11: 97-106.
125. Lankau RA. 2007. Specialist and generalist herbivores exert opposing selection on a chemical defense. New Phytologist 175: 176-184.
126. Lankau RA, Strauss SY. 2007. Mutual feedbacks maintain both genetic and species diversity in a plant community. Science 317: 1561-1563.
127. Lankau RA, Strauss SY. 2008. Community complexity drives patterns of natural selection on a chemical defense of Brassica nigra. American Naturalist 171: 150-161.
128. Lawler IR, Stapley J, Foley WJ, Eschler BM. 1999. Ecological example of conditioned flavor aversion in plant-herbivore interactions: effect of terpenes of Eucalyptus leaves on feeding by common ringtail and brushtail possums. Journal of Chemical Ecology 25: 401-415.
129. Lichtenthaler HK. 1999. The 1-deoxy-d-xylulose-5-phosphate pathway of isoprenoid biosynthesis in plants. Annual Review of Plant Physiology and Plant Molecular Biology 50: 47-65.
130. Lynch M, Force A. 2000. The probability of duplicate gene preservation by subfunctionalization. Genetics 154: 459-473.
131. Macel M, Klinkhamer PGL, Vrieling K, van der Meijden E. 2002. Diversity of pyrrolizidine alkaloids in Senecio species does not affect the specialist herbivore Tyria jacobaeae. Oecologia 133: 541-550.
132. Marsh KJ, Wallis IR, McLean S, Sorensen JS, Foley WJ. 2006. Conflicting demands on detoxification pathways influence how common brushtail possums choose their diets. Ecology 87: 2103-2112.
133. 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 Biology 10: 226.
134. Masel J, Siegal ML. 2009. Robustness: mechanisms and consequences. Trends in Genetics 25: 395-403.
135. Meldau S, Erb M, Baldwin IT. 2012. Defence on demand: mechanisms behind optimal defence patterns. Annals of Botany 110: 1503-1514.
136. Mewis I, Tokuhisa JG, Schultz JC, Appel HM, Ulrichs C, Gershenzon J. 2006. Gene expression and glucosinolate accumulation in Arabidopsis thaliana in response to generalist and specialist herbivores of different feeding guilds and the role of defense signaling pathways. Phytochemistry 67: 2450-2462.
137. Mithofer A, Boland W. 2012. Plant defense against herbivores: chemical aspects. In: Merchant SS, ed. Annual review of plant biology, vol 63. Palo Alto, CA, USA: Annual Reviews, 431-450.
138. Mitra S, Baldwin IT. 2008. Independently silencing two photsynthetic proteins in Nicotiana attenuata has different effects on herbivore resistance. Plant Physiology 148: 1128-1138.
139. Mizutani M, Ohta D. 2010. Diversification of P450 genes during land plant evolution. Annual Review of Plant Biology 61: 291-315.
140. Mody K, Unsicker SB, Linsenmair KE. 2007. Fitness related diet-mixing by intraspecific host-plant-switching of specialist insect herbivores. Ecology 88: 1012-1020.
141. Moore BD, Foley WJ. 2005. Tree use by koalas in a chemically complex landscape. Nature 435: 488-490.
142. Moore BD, Lawler IR, Wallis IR, Beale CM, Foley WJ. 2010. Palatability mapping: a koala's eye view of spatial variation in habitat quality. Ecology 91: 3165-3176.
143. 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.
144. Mraja A, Unsicker SB, Reichelt M, Gershenzon J, Roscher C. 2011. Plant community diversity influences allocation to direct chemical defence in Plantago lanceolata. PLoS One 6: e28055.
145. Mulder HA, Bijma P, Hill WG. 2007. Prediction of breeding values and selection responses with genetic heterogeneity of environmental variance. Genetics 175: 1895-1910.
146. Neilson EH, Goodger JQD, Woodrow IE. 2006. Novel aspects of cyanogenesis in Eucalyptus camphora subsp. humeana. Functional Plant Biology 33: 487-496.
147. Núñez-Farfán J, Fornoni J, Valverde PL. 2007. The evolution of resistance and tolerance to herbivores. Annual Review of Ecology Evolution and Systematics 38: 541-566.
148. Ober D. 2010. Gene duplications and the time thereafter - examples from plant secondary metabolism. Plant Biology 12: 570-577.
149. Olsen KM, Hsu SC, Small LL. 2008. Evidence on the molecular basis of the Ac/ac adaptive cyanogenesis polymorphism in white clover (Trifolium repens L.). Genetics 179: 517-526.
150. Olsen KM, Kooyers NJ, Small LL. 2013. Recurrent gene deletions and the evolution of adaptive cyanogenesis polymorphisms in white clover (Trifolium repens L.). Molecular Ecology. 22: 724-738.
151. Olsen KM, Sutherland BL, Small LL. 2007. Molecular evolution of the Li/li chemical defence polymorphism in white clover (Trifolium repens L.). Molecular Ecology 16: 4180-4193.
152. Ordas B, Malvar RA, Hill WG. 2008. Genetic variation and quantitative trait loci associated with developmental stability and the environmental correlation between traits in maize. Genetics Research 90: 385-395.
153. Orians CM, Lower S, Fritz RS, Roche BM. 2003. The effects of plant genetic variation and soil nutrients on secondary chemistry and growth in a shrubby willow, Salix sericea: patterns and constraints on the evolution of resistance traits. Biochemical Systematics and Ecology 31: 233-247.
154. Orozco-Cardenas ML, Narvaez-Vasquez J, Ryan CA. 2001. Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate. The Plant Cell 13: 179-191.
155. Osbourn A. 1996. Saponins and plant defence - a soap story. Trends in Plant Science 1: 4-9.
156. Pasteels JM, Gregoire JC. 1984. Selective predation on chemically defended Chrysomelid larvae - a conditioning process. Journal of Chemical Ecology 10: 1693-1700.
157. Pelser PB, de Vos H, Theuring C, Beuerle T, Vrieling K, Hartmann T. 2005. Frequent gain and loss of pyrrolizidine alkaloids in the evolution of Senecio section Jacobaea (Asteraceae). Phytochemistry 66: 1285-1295.
158. Pettersson ME, Nelson RM, Carlborg Ö. 2012. Selection on variance-controlling genes: adaptability or stability. Evolution 66: 3945-3949
159. Phillips MA, Croteau RB. 1999. Resin-based defenses in conifers. Trends in Plant Science 4: 184-190.
160. Pigliucci M. 2008. Is evolvability evolvable? Nature Reviews Genetics 9: 75-82.
161. Poelman EH, van Dam NM, van Loon JJA, Vet LEM, Dicke M. 2009. Chemical diversity in Brassica oleracea affects biodiversity of insect herbivores. Ecology 90: 1863-1877.
162. Poelman EH, van Loon JJA, Dicke M. 2008. Consequences of variation in plant defense for biodiversity at higher trophic levels. Trends in Plant Science 13: 534-541.
163. Porth I, Hamberger B, White R, Ritland K. 2011. Defense mechanisms against herbivory in Picea: sequence evolution and expression regulation of gene family members in the phenylpropanoid pathway. BMC Genomics 12: 608.
164. Queitsch C, Sangster TA, Lindquist S. 2002. Hsp90 as a capacitor of phenotypic variation. Nature 417: 618-624.
165. 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.
166. Rausher MD. 2001. Coevolution and plant resistance to natural enemies. Nature 411: 857-864.
167. Reichelt M, Brown PD, Schneider B, Oldham NJ, Stauber E, Tokuhisa J, Kliebenstein DJ, Mitchell-Olds T, Gershenzon J. 2002. Benzoic acid glucosinolate esters and other glucosinolates from Arabidopsis thaliana. Phytochemistry 59: 663-671.
168. Rhoades DF, Cates RG. 1976. Toward a general theory of plant antiherbivore chemistry. Recent Advances in Phytochemistry 10: 168-213.
169. Rowe HC, Hansen BG, Halkier BA, Kliebenstein DJ. 2008. Biochemical networks and epistasis shape the Arabidopsis metabolome. The Plant Cell 20: 1199-1216.
170. Rutherford SL, Lindquist S. 1998. Hsp90 as a capacitor for morphological evolution. Nature 396: 336-342.
171. Salminen JP, Karonen M. 2011. Chemical ecology of tannins and other phenolics: we need a change in approach. Functional Ecology 25: 325-338.
172. Salminen JP, Karonen M, Sinkkonen J. 2010. Chemical ecology of tannins: recent developments in tannin chemistry reveal new structures and structure-activity patterns. Chemistry - A European Journal 17: 2806-2816.
173. Sangster TA, Bahrami A, Wilczek A, Watanabe E, Schellenberg K, McLellan C, Kelley A, Kong SW, Queitsch C, Lindquist S. 2007. Phenotypic diversity and altered environmental plasticity in Arabidopsis thaliana with reduced Hsp90 levels. PLoS One 2: e648.
174. Sangster TA, Salathia N, Undurraga S, Milo R, Schelienberg K, Lindquist S, Queitsch C. 2008. HSP90 affects the expression of genetic variation and developmental stability in quantitative traits. Proceedings of the National Academy of Sciences, USA 105: 2963-2968.
175. Sasaki K, Saito T, Lamsa M, Oksman-Caldentey KM, Suzuki M, Ohyama K, Muranaka T, Ohara K, Yazaki K. 2007. Plants utilize isoprene emission as a thermotolerance mechanism. Plant and Cell Physiology 48: 1254-1262.
176. Schultz JC, Nothnagle PJ, Baldwin IT. 1982. Seasonal and individual variation in leaf quality of 2 northern hardwood tree species. American Journal of Botany 69: 753-759.
177. Schuman M, Baldwin IT. 2012. Asking the ecosystem if herbivory-inducible plant volatiles (HIPVs) have defensive functions. In: Iason GR, Dicke M, Hartley S, eds. The ecology of plant secondary metabolites: genes to global processes. Cambridge, UK: Cambridge University Press, 287-307.
178. Schuman MC, Heinzel N, Gaquerel E, Svatos A, Baldwin IT. 2009. Polymorphism in jasmonate signaling partially accounts for the variety of volatiles produced by Nicotiana attenuata plants in a native population. New Phytologist 183: 1134-1148.
179. Schuster J, Knill T, Reichelt M, Gershenzon J, Binder S. 2006. BRANCHED-CHAIN AMINOTRANSFERASE4 is part of the chain elongation pathway in the biosynthesis of methionine-derived glucosinolates in Arabidopsis. The Plant Cell 18: 2664-2679.
180. Schwachtje J, Baldwin IT. 2008. Why does herbivore attack reconfigure primary metabolism? Plant Physiology 146: 845-851.
181. Scioneaux AN, Schmidt MA, Moore MA, Lindroth RL, Wooley SC, Hagerman AE. 2011. Qualitative variation in proanthocyanidin composition of Populus species and hybrids: genetics is the key. Journal of Chemical Ecology 37: 57-70.
182. Shelton AL. 2004. Variation in chemical defences of plants may improve the effectiveness of defence. Evolutionary Ecology Research 6: 709-726.
183. Shen X, Pettersson M, Ronnegard L, Carlborg O. 2012. Inheritance beyond plain heritability: variance-controlling genes in Arabidopsis thaliana. PLOS Genetics 8: e1002839.
184. Shinoda T, Nagao T, Nakayama M, Serizawa H, Koshioka M, Okabe H, Kawai A. 2002. Identification of a triterpenoid saponin from a crucifer, Barbarea vulgaris, as a feeding deterrent to the diamondback moth, Plutella xylostella. Journal of Chemical Ecology 28: 587-599.
185. Siemens DH, Roy BA. 2005. Tests for parasite-mediated frequency-dependent selection in natural populations of an asexual plant species. Evolutionary Ecology 19: 321-338.
186. Simons AM. 2009. Fluctuating natural selection accounts for the evolution of diversification bet hedging. Proceedings of the Royal Society B: Biological Sciences 276: 1987-1992.
187. Smithson JB, Lenne JM. 1996. Varietal mixtures: a viable strategy for sustainable productivity in subsistence agriculture. Annals of Applied Biology 128: 127-158.
188. Speed M, Ruxton G, Mappes J, Sherratt T. 2012. Why are defensive toxins so variable? An evolutionary perspective. Biological Reviews 87: 874-884.
189. Stamp N. 2003. Out of the quagmire of plant defense hypotheses. Quarterly Review of Biology 78: 23-55.
190. Starrfelt J, Kokko H. 2012. Bet-hedging - a triple tradeoff between means, variances and correlations. Biological Reviews 87: 742-755.
191. Steppuhn A, Gase K, Krock B, Halitschke R, Baldwin IT. 2004. Nicotine's defensive function in nature. Plos Biology 2: 1074-1080.
192. Strauss SY, Rudgers JA, Lau JA, Irwin RE. 2002. Direct and ecological costs of resistance to herbivory. Trends in Ecology & Evolution 17: 278-285.
193. Suomela J, Osipov V, Haukioja E. 1995. Variation among and within mountain birch trees in foliage pehnols, carbohydrates and amino acids and in growth of Epirrita autumnata larvae. Journal of Chemical Ecology 21: 1421-1446.
194. Tack AJM, Johnson MTJ, Roslin T. 2012. Sizing up community genetics: it's a matter of scale. Oikos 121: 481-488.
195. Tack AJM, Roslin T. 2010. Overrun by the neighbors: landscape context affects strength and sign of local adaptation. Ecology 91: 2253-2260.
196. Tack AJM, Roslin T. 2011. The relative importance of host-plant genetic diversity in structuring the associated herbivore community. Ecology 92: 1594-1604.
197. Tanner GJ, Francki KT, Abrahams S, Watson JM, Larkin PJ, Ashton AR. 2003. Proanthocyanidin biosynthesis in plants - purification of legume leucoanthocyanidin reductase and molecular cloning of its cDNA. Journal of Biological Chemistry 278: 31647-31656.
198. Till-Bottraud I, Gouyon PH. 1992. Intraplant versus interplant Batesian mimicry - a model on cyanogenesis and herbivory in clonal plants. American Naturalist 139: 509-520.
199. Tilman D, Reich PB, Knops J, Wedin D, Mielke T, Lehman C. 2001. Diversity and productivity in a long-term grassland experiment. Science 294: 843-845.
200. Turner JG, Ellis C, Devoto A. 2002. The jasmonate signal pathway. The Plant Cell 14(Suppl 1): S153-S164.
201. Tuskan GA, DiFazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A et al. 2006. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313: 1596-1604.
202. Utsumi S, Ando Y, Craig TP, Ohgushi T. 2011. Plant genotypic diversity increases population size of a herbivorous insect. Proceedings of the Royal Society B: Biological Sciences 278: 3108-3115.
203. Vernet P, Gouyon PH, Valdeyron G. 1986. Genetic-control of the oil content in Thymus vulgaris L - a case of polymorphism in a biosynthetic chain. Genetica 69: 227-231.
204. Wagner GP, Altenberg L. 1996. Complex adaptations and the evolution of evolvability. Evolution 50: 967-976.
205. Wang LJ, Jiang YZ, Yuan L, Lu WX, Yang L, Karim A, Luo KM. 2013. Isolation and Characterization of cDNAs encoding leucoanthocyanidin reductase and anthocyanidin reductase from Populus trichocarpa. PLoS One 8: e64664.
206. Whitham TG, Bailey JK, Schweitzer JA, Shuster SM, Bangert RK, LeRoy CJ, Lonsdorf E, Allan GJ, DiFazio SP, Potts BM et al. 2006. A framework for community and ecosystem genetics: from genes to ecosystems. Nature Reviews Genetics 7: 510-523.
207. Williams G. 1975. Sex and evolution. Princeton, NJ, USA: Princeton University Press.
208. Wink M. 2008. Plant secondary metabolism: diversity, function and its evolution. Natural Product Communications 3: 1205-1216.
209. Winkel-Shirley B. 2001. Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiology 126: 485-493.
210. Woldemariam MG, Baldwin IT, Galis I. 2011. Transcriptional regulation of plant inducible defenses against herbivores: a mini-review. Journal of Plant Interactions 6: 113-119.
211. Wu JQ, Hettenhausen C, Baldwin IT. 2006. Evolution of proteinase inhibitor defenses in North American allopolyploid species of Nicotiana. Planta 224: 750-760.
212. Ye M, Luo SM, Xie JF. 2012. Silencing COI1 in rice increases susceptibility to chewing insects and impairs inducible defense. PLoS One 7: e36214.
213. Zhang J. 2003. Evolution by gene duplication: an update. Trends in Ecology and Evolution 18: 292-298.
214. Zhang Z, Ober JA, Kliebenstein DJ. 2006. The gene controlling the quantitative trait locus EPITHIOSPECIFIER MODIFIER1 alters glucosinolate hydrolysis and insect resistance in Arabidopsis. The Plant Cell 18: 1524-1536.
215. Zulak KG, Bohlmann J. 2010. Terpenoid biosynthesis and specialized vascular cells of conifer defense. Journal of Integrative Plant Biology 52: 86-97.
216. Züst T, Heichinger C, Grossniklaus U, Harrington R, Kliebenstein DJ, Turnbull LA. 2012. Natural enemies drive geographic variation in plant defenses. Science 338: 116-119.