Abstract
The genus Populus is ideally suited for applying the tools of genomics to plant-herbivore interactions and secondary metabolism. Populus is rich in phenolic secondary metabolites including condensed tannins and salicylate-based glycosides; these and related-compounds strongly shape the interactions of Populus with a host of invertebrate and vertebrate herbivores in diverse natural environments and commercial plantations. Microarray studies have been instrumental in delineating the induced defense response to herbivore damage and in identifying defense-related genes in Populus. These can now be functionally tested in vitro as recombinant proteins as well as in vivo in transgenic plants. Analysis of the P. trichocarpa genome has provided access to candidate genes likely to be important for the synthesis of phenolic secondary metabolites, thereby accelerating progress in understanding the ecological functions of these compounds. Combining genomics with improved metabolite profiling will lead to a deeper understanding of how the substantial variation in phenolics among Populus species and genotypes is generated, as well as the ecological consequences of this variation.
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References
Adler FR, Karban R (1994) Defended fortresses or moving targets – another model of inducible defenses inspired by military metaphors. Am Nat 144:813–832.
Arimura G, Huber DPW, Bohlmann J (2004) Forest tent caterpillars (Malacosoma disstria) induce local and systemic diurnal emissions of terpenoid volatiles in hybrid poplar (Populus trichocarpa x deltoides): cDNA cloning, functional characterization, and patterns of gene expression of (-)-germacrene D synthase, PtdTPS1. Plant J 37:603–616.
Arnold T, Appel H, Patel V et al. (2004) Carbohydrate translocation determines the phenolic content of Populus foliage: a test of the sink-source model of plant defense. New Phytol 164:157–164.
Babst BA, Ferrieri RA, Gray DW et al. (2005) Jasmonic acid induces rapid changes in carbon transport and partitioning in Populus. New Phytol 167:63–72.
Bailey JK, Schweitzer JA, Rehill BJ et al. (2007) Rapid shifts in the chemical composition of aspen forests: an introduced herbivore as an agent of natural selection. Biol Invas 9:715–722.
Bailey JK, Schweitzer JA, Rehill BJ et al. (2004) Beavers as molecular geneticists: a genetic basis to the foraging of an ecosystem engineer. Ecology 85:603–608.
Baker WL (1972) Eastern Forest Insects. Miscellaneous publication No. 1175. U.S.D.A. Forest Service, Washington DC.
Barbehenn RV, Jones CP, Yip L et al. (2007) Limited impact of elevated levels of polyphenol oxidase on tree-feeding caterpillars: assessing individual plant defenses with transgenic poplar. Oecologia 154:129–140.
Bradshaw HD, Parsons TJ, Gordon MP (1991) Wound-responsive gene expression in poplars. For Ecol Manag 43:211–224.
Busov V, Meilan R, Pearce DW et al. (2006) Transgenic modification of gai or rgl1 causes dwarfing and alters gibberellins, root growth, and metabolite profiles in Populus. Planta 224:288–299.
Christopher ME, Miranda M, Major IT et al. (2004) Gene expression profiling of systemically wound-induced defenses in hybrid poplar. Planta 219:936–947.
Coleman HD, Park JY, Nair R et al. (2008) RNAi-mediated suppression of p-coumaroyl-CoA 3'-hydroxylase in hybrid poplar impacts lignin deposition and soluble secondary metabolism. Proc Natl Acad Sci USA 105:4501–4506.
Constabel CP, Barbehenn R (2008) Defensive roles of polyphenol oxidase in plants. In: Schaller A (ed) Induced Plant Resistance to Herbivory. Springer, The Netherland, pp 253–269.
Constabel CP, Major IT (2005) Molecular biology and biochemistry of induced insect defense in Populus. Rec Adv Phytochem 39:119–143.
Constabel CP, Ryan CA (1998) A survey of wound- and methyl jasmonate-induced leaf polyphenol oxidase in crop plants. Phytochemistry 47:507–511.
Constabel CP, Yip L, Patton JJ et al. (2000) Polyphenol oxidase from hybrid poplar. Cloning and expression in response to wounding and herbivory. Plant Physiol 124:285–295.
Curtis MD, Grossniklaus U (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol 133:462–469.
Dafoe NJ, Zamani A, Ekramoddoullah AKM et al. (2009) Analysis of the poplar phloem proteome and its response to leaf wounding. J Proteome Res 8:2341–2350.
Davis JM, Gordon MP, Smit BA (1991) Assimilate movement dictates remote sites of wound-induced gene expression in poplar leaves. Proc Natl Acad Sci USA 88:2393–2396.
De Vos M, Van Oosten VR, Van Poecke RMP et al. (2005) Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol Plant-Micr Interact 18:923–937.
Dgany O, Gonzalez A, Sofer O et al. (2004) The structural basis of the thermostability of SP1, a novel plant (Populus tremula) boiling stable protein. J Biol Chem 279:51516–51523.
Dickmann DI, Stuart KW (1983) The Culture of Poplars in Eastern North America. Michigan State University, East Lansing, MI.
Diner B, Berteaux D, Fyles J et al. (2009) Behavioral archives link the chemistry and clonal structure of trembling aspen to the food choice of North American porcupine. Oecologia 160:687–695.
Ding XF, Gopalakrishnan B, Johnson LB et al. (1998) Insect resistance of transgenic tobacco expressing an insect chitinase gene. Trans Res 7:77–84.
Donaldson JR, Lindroth RL (2004) Cottonwood leaf beetle (Coleoptera: Chrysomelidae) performance in relation to variable phytochemistry in juvenile aspen (Populus tremuloides Michx.). Environ Entomol 33:1505–1511.
Donaldson JR, Lindroth RL (2007) Genetics, environment, and their interaction determine efficacy of chemical defense in trembling aspen. Ecology 88:729–739.
Donaldson JR, Lindroth RL (2008) Effects of variable phytochemistry and budbreak phenology on defoliation of aspen during a forest tent caterpillar outbreak. Agric For Entomol 10:399–410.
Donaldson JR, Stevens MT, Barnhill HR et al. (2006) Age-related shifts in leaf chemistry of clonal aspen (Populus tremuloides). J Chem Ecol 32:1415–1429.
Ellison AM, Bank MS, Clinton BD et al. (2005) Loss of foundation species: consequences for the structure and dynamics of forested ecosystems. Front Ecol Environ 3:479–486.
English S, Greenaway W, Whatley FR (1991) Analysis of phenolics of Populus-trichocarpa bud dxudate by GC-MS. Phytochemistry 30:531–533.
Felton GW, Tumlinson JH (2008) Plant-insect dialogs: complex interactions at the plant-insect interface. Curr Opin Plant Biol 11:457–463.
Fernandez MP, Breuil C, Watson PA (2002) Natural clonal variation of wood extractives in Populus tremuloides. Can J For Res 32:1192–1199.
Frost CJ, Appel M, Carlson JE et al. (2007) Within-plant signalling via volatiles overcomes vascular constraints on systemic signalling and primes responses against herbivores. Ecol Lett 10:490–498.
Furniss RL, Carolin VM (1977) Western Forest Insects. Miscellaneous Publication no. 1339. U.S.D.A. Forest Service, Washington D.C.
Greenaway W, Whatley FR (1990) Resolution of complex mixtures of phenolics in poplar bud exudate by analysis of gas chromatography mass mpectrometry data. J Chrom 519:145–158.
Greenaway W, Whatley FR (1991) Analysis of phenolics of bud exudate of Populus ciliata by GC-MS. Phytochemistry 30:1887–1889.
Hale BK, Herms DA, Hansen RC et al. (2005) Effects of drought stress and nutrient availability on dry matter allocation, phenolic glycosides, and rapid induced resistance of poplar to two lymantriid defoliators. J Chem Ecol 31:2601–2620.
Hamberger B, Ellis M, Friedmann M et al. (2007) Genome-wide analyses of phenylpropanoid-related genes in Populus trichocarpa, Arabidopsis thaliana, and Oryza sativa: the Populus lignin toolbox and conservation and diversification of angiosperm gene families. Can J Bot 85:1182–1201.
Han KH, Meilan R, Ma C et al. (2000) An Agrobacterium tumefaciens transformation protocol effective on a variety of cottonwood hybrids (genus Populus). Plant Cell Rep 19:315–320.
Harborne JB, Williams CA (2000) Advances in flavonoid research since 1992. Phytochemistry 55:481–504.
Harding SA, Jiang HY, Jeong ML, et al. (2005) Functional genomics analysis of foliar condensed tannin and phenolic glycoside regulation in natural cottonwood hybrids. Tree Physiol 25:1475–1486.
Haruta M, Major IT, Christopher ME et al. (2001) A Kunitz trypsin inhibitor gene family from trembling aspen (Populus tremuloides Michx.): cloning, functional expression, and induction by wounding and herbivory. Plant Mol Biol 46:347–359.
Havill NP, Raffa KF (1999) Effects of elicitation treatment and genotypic variation on induced resistance in Populus: impacts on gypsy moth (Lepidoptera: Lymantriidae) development and feeding behavior. Oecologia 120:295–303.
Hemming JDC, Lindroth RL (1999) Effects of light and nutrient availability on aspen: growth, phytochemistry, and insect performance. J Chem Ecol 25:1687–1714.
Herms DA, Mattson WJ (1992) The dilemma of plants – To grow or defend. Q Rev Biol 67:283–335.
Hoffmann L, Maury S, Martz F et al. (2003) Purification, cloning, and properties of an acyltransferase controlling shikimate and quinate ester intermediates in phenylpropanoid metabolism. J Biol Chem 278:95–103.
Hwang S-Y, Lindroth RL (1997) Clonal variation in foliar chemistry of aspen: effects on gypsy moths and forest tent caterpillars. Oecologia 111:99–108.
Ingvarsson PK (2005) Molecular population genetics of herbivore-induced protease inhibitor genes in European Aspen (Populus tremula L., Salicaceae). Mol Biol Evol 22:1802–1812.
Jaillon O, Aury JM, Noel B et al. (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–U5.
Kao YY, Harding SA, Tsai CJ (2002) Differential expression of two distinct phenylalanine ammonia-lyase genes in condensed tannin-accumulating and lignifying cells of quaking aspen. Plant Physiol 130:796–807.
Karimi M, Bleys A, Vanderhaeghen R et al. (2007) Building blocks for plant gene assembly. Plant Physiol 145:1183–1191.
Kempema LA, Cui XP, Holzer FM et al. (2007) Arabidopsis transcriptome changes in response to phloem-feeding silverleaf whitefly nymphs. Similarities and distinctions in responses to aphids. Plant Physiol 143:849–865.
Kessler A, Halitschke R, Baldwin IT (2004) Silencing the jasmonate cascade: Induced plant defenses and insect populations. Science 305:665–668.
Kinney KK, Lindroth RL, Jung SM et al. (1997) Effects of CO2 and NO3- availability on deciduous trees: phytochemistry and insect performance. Ecology 78:215–230.
Kohler A, Rinaldi C, Duplessis S et al. (2008) Genome-wide identification of NBS resistance genes in Populus trichocarpa. Plant Mol Biol 66:619–636.
Lawrence SD, Novak NG (2001) A rapid method for the production and characterization of recombinant insecticidal proteins in plants. Mol Breed 8:139–146.
Lawrence SD, Novak NG (2006) Expression of poplar chitinase in tomato leads to inhibition of development in colorado potato beetle. Biotech Lett 28:593–599.
Lepiniec L, Debeaujon I, Routaboul JM et al. (2006) Genetics and biochemistry of seed flavonoids. Annu Rev Plant Biol 57:405–430.
Li L, Li CY, Lee GI et al. (2002) Distinct roles for jasmonate synthesis and action in the systemic wound response of tomato. Proc Natl Acad Sci USA 99:6416–6421.
Lindroth RL (2001) Adaptations of quaking aspen for defense against damage by herbivores and related environmental agents. In: Shepperd WD, Binkley DB, Bartos DL, et al. (eds) Sustaining Aspen in Western Landscapes. symposium proceedings, 13–15 June 2000, Grand Junction, CO.
Lindroth RL, Hwang S-Y (1996a) Diversity, redundancy and multiplicity in chemical defense systems of aspen. Rec Adv Phytochem 30:25–56.
Lindroth RL, Hwang S-Y (1996b) Clonal variation in foliar chemistry of quaking aspen (Populus tremuloides Michx.). Biochem Syst Ecol 24:357–364.
Lindroth RL, Peterson SS (1988) Effects of plant phenols on performance of southern armyworm larvae. Oecologia 75:185–189.
Lindroth RL, Scriber JM, Hsia MTS (1988) Chemical ecology of the tiger swallowtail: mediation of host use by phenolic glycosides. Ecology 69:814–822.
Madritch M, Donaldson JR, Lindroth RL (2006) Genetic identity of Populus tremuloides litter influences decomposition and nutrient release in a mixed forest stand. Ecosystems 9:528–537.
Madritch MD, Greene SG, Lindroth RL (2009) Genetic mosaics of ecosystem functioning across aspen-dominated landscapes. Oecologia. 160: 119–127.
Major IT, Constabel CP (2006) Molular analysis of poplar defense against herbivory: comparison of wound- and insect elicitor-induced gene expression. New Phytol 172:617–635.
Major IT, Constabel CP (2007) Shoot-root defense signaling and activation of root defense by leaf damage in poplar. Can J Bot 85:1171–1181.
Major IT, Constabel CP (2007b) Insect regurgitant and wounding elicit similar defense responses in poplar leaves: not something to spit at? Plant Signal Behav 2:1–3.
Major IT, Constabel CP (2008) Functional analysis of the Kunitz trypsin inhibitor family in poplar reveals biochemical diversity and multiplicity in defense against herbivores. Plant Physiol 146:888–903.
McArthur C, Robbins CT, Hagerman AE, Hanley TA (1993) Diet selection by a ruminant generalist browser in relation to plant chemistry. Can J Zool 71:2236–2243.
Mellway RD, Constabel CP (2009) Metabolic engineering and potential functions of proanthocyanidins in poplar. Plant Signal & Behavior. 4: 790–792.
Mellway RD, Tran LT, Prouse MB et al. (2009) The wound-, pathogen-, and ultraviolet B-responsive MYB134 gene encodes an R2R3 MYB transcription factor that regulates proanthocyanidin synthesis in poplar. Plant Physiol 150:924–941.
Miranda M, Ralph SG, Mellway R et al. (2007) The transcriptional response of hybrid poplar (Populus trichocarpa x P. deltoides) to infection by Melampsora medusae leaf rust involves induction of flavonoid pathway genes leading to the accumulation of proanthocyanidins. Mol Plant-Micr Interact 20:816–831.
Mithofer A, Wanner G, Boland W (2005) Effects of feeding Spodoptera littoralis on lima bean leaves. II. Continuous mechanical wounding resembling insect feeding is sufficient to elicit herbivory-related volatile emission. Plant Physiol 137:1160–1168.
Neale DB, Savolainen O (2004) Association genetics of complex traits in conifers. Trends Plant Sci 9:325–330.
Niggeweg R, Michael AJ, Martin C (2004) Engineering plants with increased levels of the antioxidant chlorogenic acid. Nature Biotech 22:746–754.
Osier TL, Lindroth RL (2001) Effects of genotype, nutrient availability, and defoliation on aspen phytochemistry and insect performance. J Chem Ecol 27:1289–1313.
Osier TL, Lindroth RL (2004) Long-term effects of defoliation on quaking aspen in relation to genotype and nutrient availability: plant growth, phytochemistry and insect performance. Oecologia 139:55–65.
Osier TL, Lindroth RL (2006) Genotype and environment determine allocation to and costs of resistance in quaking aspen. Oecologia 148:293–303.
Owens DK, Alerding AB, Crosby KC et al. (2008) Functional analysis of a predicted flavonol synthase gene family in Arabidopsis. Plant Physiol 147:1046–1061.
Palo RT (1984) Distribution of birch (Betula spp), willow (Salix spp), and poplar (Populus spp) secondary metabolites and their potential role as chemical defense against herbivores. J Chem Ecol 10:499–520.
Parsons TJ, Bradshaw HD, Gordon MP (1989) Systemic accumulation of specific messenger-RNAs in response to wounding in poplar trees. Proc Natl Acad Sci USA 86:7895–7899.
Pearl IA, Darling SF (1968) Studies on leaves of family Salicaceae. 11. Hot water extractives of leaves of Populus balsamifera. Phytochemistry 7:1845–1849.
Perala DA (1990) Populus tremuloides Michx. Quaking Aspen. In: Burns RM, Honkala BH (eds) Silvics of North America. Volume 2. Hardwoods. U.S.D.A. Forest Service, Washington D.C.
Peters DJ, Constabel CP (2002) Molecular analysis of herbivore-induced condensed tannin synthesis: cloning and expression of dihydroflavonol reductase from trembling aspen (Populus tremuloides). Plant J 32:701–712.
Philippe RN, Bohlmann J (2007) Poplar defense against insect herbivores. Can J Bot 85:1111–1126.
Ralph S, Oddy C, Cooper D et al. (2006) Genomics of hybrid poplar (Populus trichocarpa x deltoides) interacting with forest tent caterpillars (Malacosoma disstria): normalized and full-length cDNA libraries, expressed sequence tags, and a cDNA microarray for the study of insect-induced defences in poplar. Mol Ecol 15:1275–1297.
Ralph SG, Chun HJE, Cooper D et al. (2008) Analysis of 4,664 high-quality sequence-finished poplar full-length cDNA clones and their utility for the discovery of genes responding to insect feeding. BMC Genomics 9:57.
Rehill BJ, Whitham TG, Martinsen GD et al. (2006) Developmental trajectories in cottonwood phytochemistry. J Chem Ecol 32:2269–2285.
Reymond P, Bodenhausen N, Van Poecke RMP et al. (2004) A conserved transcript pattern in response to a specialist and a generalist herbivore. Plant Cell 16:3132–3147.
Robison DJ, Raffa KF (1994) Characterization of hybrid poplar clones for resistance to the forest tent caterpillar. For Sci 40:686–714.
Robison DJ, Raffa KF (1997) Effects of constitutive and inducible traits of hybrid poplars on forest tent caterpillar feeding and population ecology. For Sci 43:252–267.
Roda A, Halitschke R, Steppuhn A et al. (2004) Individual variability in herbivore-specific elicitors from the plant’s perspective. Mol Ecol 13:2421–2433.
Ryan CA (1990) Protease inhibitors in plants – genes for improving defenses against insects and pathogens. Annu Rev Phytopath 28:425–449.
Saito K, Hirai MY, Yonekura-Sakakibara K (2008) Decoding genes with coexpression networks and metabolomics – ‘majority report by precogs’. Trends Plant Sci 13:36–43.
Schaller A, Stintzi A (2008) Jasmonate biosynthesis and signaling for induced plant defense against herbivory. In: Schaller A (ed) Induced Plant Resistance to Herbivory. Springer, Berlin, pp 349–366.
Schwachtje J, Baldwin IT (2008) Why does herbivore attack reconfigure primary metabolism? Plant Physiol 146:845–851.
Schweitzer JA, Madritch MD, Bailey JK et al. (2008) The genetic basis of condensed tannins and their role in nutrient regulation in a Populus model system. Ecosystems. 11: 1005–1020.
Stevens MT, Lindroth RL (2005) Induced resistance in the indeterminate growth of aspen (Populus tremuloides). Oecologia 145:298–306.
Thines B, Katsir L, Melotto M et al. (2007) JAZ repressor proteins are targets of the SCFCO11 complex during jasmonate signalling. Nature 448:661–U2.
Tohge T, Nishiyama Y, Hirai MY et al. (2005) Functional genomics by integrated analysis of metabolome and transcriptome of Arabidopsis plants over-expressing an MYB transcription factor. Plant J 42:218–235.
Tsai CJ, Harding SA, Tschaplinski TJ et al. (2006) Genome-wide analysis of the structural genes regulating defense phenylpropanoid metabolism in Populus. New Phytol 172:47–62.
Tuskan GA, DiFazio S, Jansson S et al. (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604.
U.S. D.O.E. (2006) Breaking the biological barriers to cellulosic ethanal: a joint research agenda. U.S. Department of Energy Office of Science and Office of Energy Efficiency and Renewable Energy. DOE/SC–0095
Vigue LM, Lindroth RL (2009) Effects of genotype, elevated CO2, and elevated O3 on aspen phytochemistry and aspen leaf beetle, Chrysomela crotchi, performance. Agric For Entomol. (submitted).
Wang JH, Constabel CP (2004) Polyphenol oxidase overexpression in transgenic Populus enhances resistance to herbivory by forest tent caterpillar (Malacosoma disstria). Planta 220:87–96.
Wang WX, Pelah D, Alergand T et al. (2002) Characterization of SP1, a stress-responsive, boiling-soluble, homo-oligomeric protein from aspen. Plant Physiol 130:865–875.
Warren JM, Bassman JH, Fellman JK et al. (2003) Ultraviolet-B radiation alters phenolic salicylate and flavonoid composition of Populus trichocarpa leaves. Tree Physiol 23:527–535.
Whitham TG, Bailey JK, Schweitzer JA et al. (2006) A framework for community and ecosystem genetics: from genes to ecosystems. Nat Rev Gen 7:510–523.
Whitham TG, DiFazio SP, Schweitzer JA et al. (2008) Extending genomics to natural communities and ecosystems. Science 320:492–495.
Wooley SC, Walker S, Vernon J et al. (2008) Aspen decline, aspen chemistry, and elk herbivory. are they linked? Rangelands 30:17–21.
Yonekura-Sakakibara K, Tohge T, Matsuda F et al. (2008) Comprehensive flavonol profiling and transcriptome coexpression analysis leading to decoding gene-metabolite correlations in Arabidopsis. Plant Cell 20:2160–2176.
Yonekura-Sakakibara K, Tohge T, Niida R et al. (2007) Identification of a flavonol 7-O-rhamnosyltransferase gene determining flavonoid pattern in Arabidopsis by transcriptome coexpression analysis and reverse genetics. J Biol Chem 282:14932–14941.
Zheng SJ, Dicke M (2008) Ecological genomics of plant-insect interactions: From gene to community. Plant Physiol 146:812–817.
Acknowledgments
We thank our many students and research collaborators, whose work made possible the advances reported here. We also thank Ken Keefover-Ring for creating Fig. 1. R. Lindroth’s research has been supported by funding from the U.S. Department of Agriculture (National Research Initiative), U.S. Department of Energy (Office of Biological and Environmental Research), and the National Science Foundation (particularly, grants DEB-0074427, DEB-0344019 and DEB-0425908). P. Constabel acknowledges the generous support of the Natural Sciences and Engineering Research Council of Canada (NSERC) in the form of Discovery, Genomics, and Strategic Grants.
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Constabel, C.P., L. Lindroth, R. (2010). The Impact of Genomics on Advances in Herbivore Defense and Secondary Metabolism in Populus . In: Jansson, S., Bhalerao, R., Groover, A. (eds) Genetics and Genomics of Populus. Plant Genetics and Genomics: Crops and Models, vol 8. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-1541-2_13
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