Studying Populus Defenses Against Insect Herbivores in the Post-Genomic Era

REFERENCES

• Agrawal , A. A. 1998 . Induced responses to herbivory and increased plant performance . Science , 279 : 1201 – 1202 .
   PubMed Web of Science ®Google Scholar
• Andersson , A. , Keskitalo , J. , Sjödin , A. , Bhalerao , R. , Sterky , F. , Wissel , K. , Tandre , K. , Aspeborg , H. , Moyle , R. , Ohmiya , Y. , Bhalerao , R. , Brunner , A. , Gustafsson , P. , Karlsson , J. , Lundeberg , J. , Nilsson , O. , Sandberg , G. , Strauss , S. , Sundberg , B. , Uhlen , M. , Jansson , S. and Nilsson , P. 2004 . A transcriptional timetable of autumn senescence . Genome Biol. , 5 : R24
   PubMed Web of Science ®Google Scholar
• Arimura , G. , Matsui , K. and Takabayashi , J. 2009 . Chemical and molecular ecology of herbivore-induced plant volatiles: proximate factors and their ultimate functions . Plant Cell Physiol. , 50 : 911 – 923 .
   PubMed Web of Science ®Google Scholar
• Arimura , G. , Huber , D. P. W. and Bohlmann , J. 2004 . Forest tent caterpillars (Malacosoma disstria) induce local and systemic diurnal emissions of terpenoid volatiles in hybrid poplar (Populus trichocarpa × deltoides): cDNA cloning, functional characterization, and patterns of gene expression of (-)-germacrene D synthase, PtdTPS1 . Plant J. , 37 : 603 – 616 .
   PubMed Web of Science ®Google Scholar
• Babst , B. A. , Sjödin , A. , Jansson , S. and Orians , C. M. 2009 . Local and systemic transcriptome responses to herbivory and jasmonic acid in Populus . Tree Genet. Genom. , 5 : 459 – 474 .
   Web of Science ®Google Scholar
• Barbehenn , R. V. , Jones , C. P. , Yip , L. , Tran , L. and Constabel , C. P. 2007 . Limited impact of elevated levels of polyphenol oxidase on tree-feeding caterpillars: assessing individual plant defenses with transgenic poplars . Oecologia , 154 : 129 – 140 .
   PubMed Web of Science ®Google Scholar
• Barbehenn , R. V. , Jaros , A. , Yip , L. , Tran , L. , Kanellis , A. K. and Constabel , C. P. 2008 . Evaluating ascorbate oxidase as a plant defense against leaf-chewing insects using transgenic poplar . J. Chem. Ecol. , 34 : 1331 – 1340 .
   PubMed Web of Science ®Google Scholar
• Bradshaw , H. D. , Hollick , J. B. , Parsons , T. J. , Clarke , H. R. G. and Gordon , M. P. 1990 . Systemically wound-responsive genes in poplar trees encode proteins similar to sweet potato sporamins and legume Kunitz trypsin inhibitors . Plant Mol. Biol. , 14 : 51 – 59 .
   PubMed Web of Science ®Google Scholar
• Brosché , M. , Vinocur , B. , Alatalo , E. R. , Lamminmäki , A. , Teichmann , T. , Ottow , E. A. , Djilianov , D. , Afif , D. , Bogeat-Triboulot , M. B. , Altman , A. , Polle , A. , Dreyer , E. , Rudd , S. , Paulin , L. , Auvinen , P. and Kangasjärvi , J. 2005 . Gene expression and metabolite profiling of Populus euphratica growing in the Negev desert . Genome Biol. , 6 : R101
   PubMed Web of Science ®Google Scholar
• Brunner , A. M. , Busov , V. B. and Strauss , S. H. 2004 . Poplar genome sequence: functional genomics in an ecologically dominant species . Trends Plant Sci. , 9 : 49 – 56 .
   PubMed Web of Science ®Google Scholar
• Busov , V. B. , Meilan , R. , Pearce , D. W. , Ma , C. , Rood , S. B. and Strauss , S. H. 2003 . Activation tagging of a dominant gibberellin catabolism gene (GA 2-oxidase) from poplar that regulates tree stature . Plant Physiol. , 132 : 1283 – 1291 .
   PubMed Web of Science ®Google Scholar
• Christopher , M. E. , Miranda , M. , Major , I. T. and Constabel , C. P. 2004 . Gene expression profiling of systemically wound-induced defenses in hybrid poplar . Planta , 219 : 936 – 947 .
   PubMed Web of Science ®Google Scholar
• Confalonieri , M. , Allegro , G. , Balestrazzi , A. , Fogher , C. and Delledonne , M. 1998 . Regeneration of Populus nigra transgenic plants expressing a Kunitz proteinase inhibitor (KTi 3) gene . Mol. Breed. , 4 : 137 – 145 .
   Web of Science ®Google Scholar
• Constabel , C. P. and Major , I. T. 2005 . “ Molecular biology and biochemistry of induced insect defense in Populus ” . In Recent Advances in Phytochemistry. Vol. 39. Chemical Ecology and Phytochemistry of Forest Ecosystems , Edited by: Romeo , J. 119 – 143 . Amsterdam, , Netherlands : Elsevier Academic Press .
   Google Scholar
• Constabel , C. P. , Yip , L. , Patton , J. J. and Christopher , M. E. 2000 . Polyphenol oxidase from hybrid poplar. Cloning and expression in response to wounding and herbivory . Plant Physiol. , 124 : 285 – 295 .
   PubMed Web of Science ®Google Scholar
• Coyle , D. R. , Nebeker , T. E. , Hart , E. R. and Mattson , W. J. 2005 . Biology and management of insect pests in North American intensively managed hardwood forest systems . Ann. Rev. Entomol. , 50 : 1 – 29 .
   PubMed Web of Science ®Google Scholar
• Cronk , Q. C. B. 2005 . Plant eco-devo: the potential of poplar as a model organism . New Phytol. , 166 : 39 – 48 .
   PubMed Web of Science ®Google Scholar
• Davis , J. M. , Clarke , H. R. G. , Bradshaw , H. D. and Gordon , M. P. 1991 . Populus chitinase genes: structure, organization, and similarity of translated sequences to herbaceous plant chitinases . Plant Mol. Biol. , 17 : 631 – 639 .
   PubMed Web of Science ®Google Scholar
• Davis , J. M. , Egelkrout , E. E. , Coleman , G. D. , Chen , T. H. H. , Haissig , B. E. , Riemenschneider , D. E. and Gordon , M. P. 1993 . A family of wound-induced genes in Populus shares common features with genes encoding vegetative storage proteins . Plant Mol. Biol. , 23 : 135 – 143 .
   PubMed Web of Science ®Google Scholar
• Delledonne , M. , Allegro , G. , Belenghi , B. , Balestrazzi , A. , Picco , F. , Levine , A. , Zelasco , S. , Calligari , P. and Confalonieri , M. 2001 . Transformation of white poplar (Populus alba L.) with a novel Arabidopsis thaliana cysteine proteinase inhibitor and analysis of insect pest resistance . Mol. Breed. , 7 : 35 – 42 .
   Web of Science ®Google Scholar
• Dicke , M. 2009 . Behavioral and community ecology of plants that cry for help . Plant Cell Environ. , 32 : 654 – 665 .
   PubMed Web of Science ®Google Scholar
• Donaldson , J. R. and Lindroth , R. L. 2007 . Genetics, environment, and their interaction determine efficacy of chemical defense in trembling aspen . Ecology , 88 : 729 – 739 .
   PubMed Web of Science ®Google Scholar
• Donaldson , J. R. , Stevens , M. T. , Barnhill , H. R. and Lindroth , R. L. 2006 . Age-related shifts in leaf chemistry of clonal aspen (Populus tremuloides) . J. Chem. Ecol. , 32 : 1415 – 1429 .
   PubMed Web of Science ®Google Scholar
• Fitzgerald , T. D. 1995 . The Tent Caterpillars , 303 Ithaca, New York : Cornell University Press .
   Google Scholar
• Giaever , G. , Chu , A. M. , Ni , L. , Connelly , C. , Riles , L. , Véronneau , S. , Dow , S. , Lucau-Danila , A. , Anderson , K. , André , B. , Arkin , A. P. , Astromoff , A. , Bakkoury , M. E. , Bangham , R. , Benito , R. , Brachat , S. , Campanaro , S. , Curtiss , M. , Davis , K. , Deutschbauer , A. , Entian , K.-D. , Flaherty , P. , Foury , F. , Garfinkel , D. J. , Gerstein , M. , Gotte , D. , Güldener , D. , Hegemann , J. H. , Hempel , S. , Herman , Z. , Jaramillo , D. F. , Kelly , D. E. , Kelly , S. L. , Kötter , P. , LaBonte , D. , Lamb , D. C. , Lan , N. , Liang , H. , Liao , H. , Liu , L. , Luo , C. , Lussier , M. , Mao , R. , Menard , P. , Ooi , S. L. , Revuelta , J. L. , Roberts , C. J. , Rose , M. , Ross-Macdonald , P. , Scherens , B. , Schimmack , G. , Shafer , B. , Shoemaker , D. D. , Sookhai-Mahadeo , S. , Storms , R. K. , Strathern , J. N. , Valle , G. , Voet , M. , Volckaert , G. , Wang , C.-Y. , Ward , T. R. , Wilhelmy , J. , Winzeler , E. A. , Yang , Y. , Yen , G. , Youngman , E. , Yu , K. , Bussey , H. , Boeke , J. D. , Snyder , M. , Philippsen , P. , Davis , R. W. and Johnston , M. 2002 . Functional profiling of the Saccharomyces cerevisiae genome . Nature , 418 : 387 – 391 .
   PubMed Web of Science ®Google Scholar
• Gigolashvili , T. , Berger , B. , Mock , H. P. , Müller , C. , Weisshaar , B. and Flügge , U. I. 2007 . The transcription factor HIG1/MYB51 regulates indolic glucosinolate biosynthesis in Arabidopsis thaliana . Plant J. , 50 : 886 – 901 .
   PubMed Web of Science ®Google Scholar
• Gill , R. I. , Ellis , B. E. and Isman , M. B. 2003 . Tryptamine-induced resistance in tryptophan decarboxylase transgenic poplar and tobacco plants against their specific herbivores . J. Chem. Ecol. , 29 : 779 – 793 .
   PubMed Web of Science ®Google Scholar
• Hale , B. K. , Herms , D. A. , Hansen , R. C. , Clausen , T. P. and Arnold , D. 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 .
   PubMed Web of Science ®Google Scholar
• Harding , S. A. , Jiang , H. , Jeong , M. L. , Casado , F. L. , Lin , H. W. and Tsai , C. J. 2005 . Functional genomics analysis of foliar condensed tannin and phenolic glycoside regulation in natural cottonwood hybrids . Tree Physiol. , 25 : 1475 – 1486 .
   PubMed Web of Science ®Google Scholar
• Harrison , E. J. , Bush , M. , Plett , J. M. , McPhee , D. P. , Vitez , R. , O'Malley , B. , Sharma , V. , Bosnich , W. , Séguin , A. , MacKay , J. and Regan , S. 2007 . Diverse developmental mutants revealed in an activation tagged population of poplar . Can. J. Bot. , 85 : 1071 – 1081 .
   Google Scholar
• Haruta , M. , Major , I. T. , Christopher , M. E. , Patton , J. J. and Constabel , C. P. 2001b . 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 .
   PubMed Web of Science ®Google Scholar
• Haruta , M. , Pedersen , J. A. and Constabel , C. P. 2001a . Polyphenol oxidase and herbivore defense in trembling aspen (Populus tremuloides): cDNA cloning, expression, and potential substrates . Physiol. Plant. , 112 : 552 – 558 .
   PubMed Web of Science ®Google Scholar
• Heil , M. 2008 . Indirect defense via tritrophic interactions . New. Phytol. , 178 : 41 – 61 .
   PubMed Web of Science ®Google Scholar
• Hogg , E. H. , Brandt , J. P. and Kochtubajda , B. 2002 . Growth and dieback of aspen forests in northwestern Alberta, Canada, in relation to climate and insects . Can. J. For. Res. , 32 : 823 – 832 .
   Web of Science ®Google Scholar
• Hollick , J. B. and Gordon , M. P. 1993 . A poplar tree proteinase inhibitor-like gene promoter is responsive to wounding in transgenic tobacco . Plant Mol. Biol. , 22 : 561 – 572 .
   PubMed Web of Science ®Google Scholar
• Howe , G. A. and Jander , G. 2008 . Plant immunity to insect herbivores . Ann. Rev. Plant Biol. , 59 : 41 – 66 .
   PubMed Web of Science ®Google Scholar
• Hwang , S. Y. and Lindroth , R. L. 1997 . Clonal variation in foliar chemistry of aspen: effects on gypsy moths and forest tent caterpillars . Oecologia , 111 : 99 – 108 .
   PubMed Web of Science ®Google Scholar
• Jansson , S. and Douglas , C. J. 2007 . Populus: a model system for plant biology . Ann. Rev. Plant Biol. , 58 : 435 – 458 .
   PubMed Web of Science ®Google Scholar
• Jeong , D. H. , An , S. , Kang , H. G. , Moon , S. , Han , J. J. , Park , S. , Lee , H. S. , An , K. and An , G. 2002 . T-DNA insertional mutagenesis for activation tagging in rice . Plant Physiol. , 130 : 1636 – 1644 .
   PubMed Web of Science ®Google Scholar
• Kant , M. R. and Baldwin , I. T. 2007 . The ecogenetics and ecogenomics of plant-herbivore interactions: rapid progress on a slippery road . Curr. Opin. Genet. Develop. , 17 : 519 – 524 .
   PubMed Web of Science ®Google Scholar
• Karban , R. and Baldwin , I. T. 1997 . Induced Responses to Herbivory , 319 Chicago, Illinois : University of Chicago Press .
   Google Scholar
• Kelleher , C. T. , Chiu , R. , Shin , H. , Bosdet , I. E. , Krzywinski , M. I. , Fjell , C. D. , Wilkin , J. , Yin , T. , DiFazio , S. P. , Ali , J. , Asano , J. K. , Chan , S. , Cloutier , A. , Girn , N. , Leach , S. , Lee , D. , Mathewson , C. A. , Olson , T. , O'Connor , K. , Prabhu , A. L. , Smailus , D. E. , Stott , J. M. , Tsai , M. , Wye , N. H. , Yang , G. S. , Zhuang , J. , Holt , R. A. , Putnam , N. H. , Vrebalov , J. , Giovannoni , J. J. , Grimwood , J. , Schmutz , J. , Rokhsar , D. , Jones , S. J. M. , Marra , M. A. , Tuskan , G. A. , Bohlmann , J. , Ellis , B. E. , Ritland , K. , Douglas , C. J. and Schein , J. E. 2007 . A physical map of the highly heterozygous Populus genome: integration with the genome sequence and genetic map and analysis of haplotype variation . Plant J. , 50 : 1063 – 1078 .
   PubMed Web of Science ®Google Scholar
• Kessler , A. , Halitschke , R. and Baldwin , I. T. 2004 . Silencing the jasmonate cascade: induced plant defenses and insect populations . Science , 305 : 665 – 668 .
   PubMed Web of Science ®Google Scholar
• Kessler , A. and Baldwin , I. T. 2002 . Plant responses to insect herbivory: the emerging molecular analysis . Ann. Rev. Plant Biol. , 53 : 299 – 328 .
   PubMed Web of Science ®Google Scholar
• Kirst , M. , Basten , C. J. , Myburg , A. A. , Zeng , Z.-B. and Sederoff , R. R. 2005 . Genetic architecture of transcript-level variation in differentiating xylem of a eucalyptus hybrid . Genetics , 169 : 2295 – 2303 .
   PubMed Web of Science ®Google Scholar
• Kirst , M. , Myburg , A. A. , De León , J. P. G. , Kirst , M. E. , Scott , J. and Sederoff , R. 2004 . Coordinated genetic regulation of growth and lignin revealed by quantitative trait locus analysis of cDNA microarray data in an interspecific backcross of Eucalyptus . Plant Physiol. , 135 : 2368 – 2378 .
   PubMed Web of Science ®Google Scholar
• Kleiner , K. W. , Ellis , D. D. , McCown , B. H. and Raffa , K. F. 2003 . Leaf ontogeny influences leaf phenolics and the efficacy of genetically expressed Bacillus thuringiensis cry1A(a) d-endotoxin in hybrid poplar against gypsy moth . J. Chem. Ecol. , 29 : 2585 – 2602 .
   PubMed Web of Science ®Google Scholar
• Koch , M. , Vorwerk , S. , Masur , C. , Sharifi-Sirchi , G. , Olivieri , N. and Schlaich , N. L. 2006 . A role for a flavin containing mono-oxygenase in resistance against microbial pathogens in Arabidopsis . Plant J. , 47 : 629 – 639 .
   PubMed Web of Science ®Google Scholar
• Kosola , K. R. , Parry , D. and Workmaster , B. A. A. 2006 . Responses of condensed tannins in poplar roots to fertilization and gypsy moth defoliation . Tree Physiol. , 26 : 1607 – 1611 .
   PubMed Web of Science ®Google Scholar
• Krysan , P. J. , Young , J. C. , Jester , P. J. , Monson , S. , Copenhaver , G. , Preuss , D. and Sussman , M. R. 2002 . Characterization of T-DNA insertion sites in Arabidopsis thaliana and implications for saturation mutagenesis . OMICS , 6 : 163 – 174 .
   PubMedGoogle Scholar
• Larson , P. R. and Isebrands , J. G. 1971 . The plastochron index as applied to developmental studies of cottonwood . Can. J. For. Res. , 1 : 1 – 11 .
   Google Scholar
• Lawrence , S. D. , Dervinis , C. , Novak , N. and Davis , J. M. 2006 . Wound and insect herbivory responsive genes in poplar . Biotech. Lett. , 28 : 1493 – 1501 .
   PubMed Web of Science ®Google Scholar
• Lee , H. , Suh , S. S. , Park , E. , Cho , E. , Ahn , J. H. , Kim , S. G. , Lee , J. S. , Kwon , Y. M. and Lee , I. 2000 . The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis . Genes & Devel. , 14 : 2366 – 2376 .
   PubMed Web of Science ®Google Scholar
• Leplé , J. C. , Bonadé-Bottino , M. , Augustin , S. , Pilate , G. , Dumanois LêTân , V. , Delplanque , A. , Cornu , D. and Jouanin , L. 1995 . Toxicity to Chrysomela tremulae (Coleoptera: Chrysomelidae) of transgenic poplars expressing a cysteine proteinase inhibitor . Mol. Breed. , 1 : 319 – 328 .
   Web of Science ®Google Scholar
• Levy , M. , Wang , Q. , Kaspi , R. , Parrella , M. P. and Abel , S. 2005 . Arabidopsis IQD1, a novel calmodulin-binding nuclear protein, stimulates glucosinolate accumulation and plant defense . Plant J. , 43 : 79 – 96 .
   PubMed Web of Science ®Google Scholar
• Major , I. T. and Constabel , C. P. 2006 . Molecular analysis of poplar defense against herbivory: comparison of wound- and insect elicitor-induced gene expression . New Phytol. , 172 : 617 – 635 .
   PubMed Web of Science ®Google Scholar
• Major , I. T. and Constabel , C. P. 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 .
   PubMed Web of Science ®Google Scholar
• Mathews , H. , Clendennen , S. K. , Caldwell , C. G. , Liu , X. L. , Connors , K. , Matheis , N. , Schuster , D. K. , Menasco , D. J. , Wagoner , W. , Lightner , J. and Wagner , D. R. 2003 . Activation tagging in tomato identifies a transcriptional regulator of anthocyanin biosynthesis, modification, and transport . Plant Cell , 15 : 1689 – 1703 .
   PubMed Web of Science ®Google Scholar
• Mattson , W. J. , Hart , E. R. and Volney , W. J. A. 2001 . “ Insect pests of Populus: coping with the inevitable ” . In Poplar Culture in North America , Edited by: Dickmann , D. I. , Isebrands , J. G. , Eckenwalder , J. E. and Richardson , J. 219 – 248 . Ottawa, , Canada : NRC Research Press .
   Google Scholar
• McCown , B. H. , McCabe , D. E. , Russell , D. R. , Robinson , D. J. , Barton , K. A. and Raffa , K. F. 1991 . Stable transformation of Populus and incorporation of pest resistance by electric discharge particle acceleration . Plant Cell Rep. , 9 : 590 – 594 .
   PubMed Web of Science ®Google Scholar
• Miranda , M. , Ralph , S. G. , Mellway , R. , White , R. , Heath , M. C. , Bohlmann , J. and Constabel , C. P. 2007 . The transcriptional response of hybrid poplar (Populus trichocarpa × P. deltoides) to infection by Melampsora medusae leaf rust involves induction of flavonoid pathway genes leading to the accumulation of proanthocyanidins . Mol. Plant Path. Interac. , 20 : 816 – 831 .
   PubMed Web of Science ®Google Scholar
• Osier , T. L. and Lindroth , R. L. 2001 . Effects of genotype, nutrient availability, and defoliation on aspen phytochemistry and insect performance . J. Chem. Ecol. , 27 : 1289 – 1313 .
   PubMed Web of Science ®Google Scholar
• Osier , T. L. and Lindroth , R. L. 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 .
   PubMed Web of Science ®Google Scholar
• Osier , T. L. and Lindroth , R. L. 2006 . Genotype and environment determine allocation to and costs of resistance in quaking aspen . Oecologia , 148 : 293 – 303 .
   PubMed Web of Science ®Google Scholar
• Parsons , T. J. , Bradshaw , H. D. and Gordon , M. P. 1989 . Systemic accumulation of specific mRNAs in response to wounding in poplar trees . Proc. Nat. Acad. Sci. USA , 86 : 7895 – 7899 .
   PubMed Web of Science ®Google Scholar
• Peters , D. J. and Constabel , C. P. 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 .
   PubMed Web of Science ®Google Scholar
• Philippe , R. N. and Bohlmann , J. 2007 . Poplar defense against insect herbivores . Can. J. Bot. , 85 : 1111 – 1126 .
   Google Scholar
• Philippe , R. N. , Ralph , S. G. , Külheim , C. , Jancsik , S. I. and Bohlmann , J. 2009 . Poplar defense against insects: Genome analysis, full-length cDNA cloning, and transcriptome and protein analysis of the poplar Kunitz-type protease inhibitor family . New Phytol. , in press
   PubMed Web of Science ®Google Scholar
• Pilate , G. , Guiney , E. , Holt , K. , Petit-Conil , M. , Lapierre , C. , Leplé , J-C. , Pollet , B. , Mila , I. , Webster , E. A. , Marstorp , H. G. , Hopkins , D. W. , Jouanin , L. , Boerjan , W. , Schuch , W. , Cornu , D. and Halpin , C. 2002 . Field and pulping performances of transgenic trees with altered lignification . Nature Biotech. , 20 : 607 – 612 .
   PubMed Web of Science ®Google Scholar
• Ralph , S. , Oddy , C. , Cooper , D. , Yueh , H. , Jancsik , S. , Kolosova , N. , Philippe , R. N. , Aeschliman , D. , White , R. , Huber , D. , Ritland , C. E. , Benoit , F. , Rigby , T. , Nantel , A. , Butterfield , Y. S. N. , Kirkpatrick , R. , Chun , E. , Liu , J. , Palmquist , D. , Wynhoven , B. , Stott , J. , Yang , G. , Barber , S. , Holt , R. A. , Siddiqui , A. , Jones , S. J. M. , Marra , M. A. , Ellis , B. E. , Douglas , C. J. , Ritland , K. and Bohlmann , J. 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 defenses in poplar . Mol. Ecol. , 15 : 1275 – 1297 .
   PubMed Web of Science ®Google Scholar
• Ralph , S. G. , Chun , H. J. E. , Cooper , D. , Kirkpatrick , R. , Kolosova , N. , Gunter , L. , Tuskan , G. A. , Douglas , C. J. , Holt , R. A. , Jones , S. J. M. , Marra , M. A. and Bohlmann , J. 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
   PubMed Web of Science ®Google Scholar
• Ranjan , P. , Kao , Y. Y. , Jiang , H. , Joshi , C. P. , Harding , S. A. and Tsai , C. J. 2004 . Suppression subtractive hybridization-mediated transcriptome analysis from multiple tissues of aspen (Populus tremuloides) altered in phenylpropanoid metabolism . Planta , 219 : 694 – 704 .
   PubMed Web of Science ®Google Scholar
• Regan , S. , Gustafson , V. , Mallubhotla , S. , Chakravarty , B. , Bagchi , M. , Siahbazi , M. , Rothwell , C. , Sardana , R. , Goyer , C. , Audy , P. , Li , X. Q. , Wang-Pruski , G. , De Koeyer , D. and Flinn , B. 2005 . Finding the perfect potato: using functional genomics to improve disease resistance and tuber quality traits . Can. J. Plant Pathol. , 28 : s247 – s255 .
   Web of Science ®Google Scholar
• Rehill , B. J. , Whitham , T. G. , Martinsen , G. D. , Schweitzer , J. A. , Bailey , J. K. and Lindroth , R. L. 2006 . Developmental trajectories in cottonwood phytochemistry . J. Chem. Ecol. , 32 : 2269 – 2285 .
   PubMed Web of Science ®Google Scholar
• Reymond , P. , Bodenhausen , N. , Van Poecke , R. M. P. , Krishnamurthy , V. , Dicke , M. and Farmer , E. E. 2004 . A conserved transcript pattern in response to a specialist and a generalist herbivore . Plant Cell , 16 : 3132 – 3147 .
   PubMed Web of Science ®Google Scholar
• Robinson , D. J. , McCown , B. H. and Raffa , K. F. 1994 . Responses of gypsy moth (Lepidoptera: Lymantriidae) and forest tent caterpillar (Lepidoptera: Lasiocampidae) to transgenic poplar, Populus spp., containing a Bacillus thuringiensis d-endotoxin gene . Environ. Entomol. , 23 : 1030 – 1041 .
   Web of Science ®Google Scholar
• Schmidt , D. D. , Voelckel , C. , Hartl , M. , Schmidt , S. and Baldwin , I. T. 2005 . Specificity in ecological interactions. Attack from the same Lepidopteran herbivore results in species-specific transcriptional responses in two Solanaceous host plants . Plant Physiol. , 138 : 1763 – 1773 .
   PubMed Web of Science ®Google Scholar
• Sjödin , A. , Bylesjö , M. , Skogström , O. , Eriksson , D. , Nilsson , P. , Rydén , P. , Jansson , S. and Karlsson , J. 2006 . UPSC-BASE—Populus transcriptomics online . Plant J. , 48 : 806 – 817 .
   PubMed Web of Science ®Google Scholar
• Stairs , G. R. 1972 . Pathogenic microorganisms in the regulation of forest insect populations . Ann. Rev. Entomol. , 17 : 355 – 372 .
   Web of Science ®Google Scholar
• Sterky , F. , Bhalerao , R. R. , Unneberg , P. , Segerman , B. , Nilsson , P. , Brunner , A. M. , Charbonnel-Campaa , L. , Lindvall , J. J. , Tandre , K. , Strauss , S. H. , Sundberg , B. , Gustafsson , P. , Uhlén , M. , Bhalerao , R. P. , Nilsson , O. , Sandberg , G. , Karlsson , J. , Lundeberg , J. and Jansson , S. 2004 . A Populus EST resource for plant functional genomics . Proc. Nat. Acad. Sci. USA , 101 : 13951 – 13956 .
   PubMed Web of Science ®Google Scholar
• Street , N. R. , Skogström , O. , Sjödin , A. , Tucker , J. , Rodríguez-Acosta , M. , Nilsson , P. , Jansson , S. and Taylor , G. 2006 . The genetics and genomics of the drought response in Populus . Plant J. , 48 : 321 – 341 .
   PubMed Web of Science ®Google Scholar
• Tuskan , G. A. , DiFazio , S. , Jansson , S. , Bohlmann , J. , Grigoriev , I. , Hellsten , U. , Putnam , N. , Ralph , S. , Rombauts , S. , Salamov , A. , Schein , J. , Sterck , L. , Aerts , A. , Bhalerao , R. R. , Bhalerao , R. P. , Blaudez , D. , Boerjan , W. , Brun , A. , Brunner , A. , Busov , V. , Campbell , M. , Carlson , J. , Chalot , M. , Chapman , J. , Chen , G. L. , Cooper , D. , Coutinho , P. M. , Couturier , J. , Covert , S. , Cronk , Q. , Cunningham , R. , Davis , J. , Degroeve , S. , Déjardin , A. , dePamphilis , C. , Detter , J. , Dirks , B. , Dubchak , I. , Duplessis , S. , Ehlting , J. , Ellis , B. , Gendler , K. , Goodstein , D. , Gribskov , M. , Grimwood , J. , Groover , A. , Gunter , L. , Hamberger , B. , Heinze , B. , Helariutta , Y. , Henrissat , B. , Holligan , D. , Holt , R. , Huang , W. , Islam-Faridi , N. , Jones , S. , Jones-Rhoades , M. , Jorgensen , R. , Joshi , C. , Kangasjärvi , J. , Karlsson , J. , Kelleher , C. , Kirkpatrick , R. , Kirst , M. , Kohler , A. , Kalluri , U. , Larimer , F. , Leebens-Mack , J. , Leplé , J.-C. , Locascio , P. , Lucas , S. , Martin , F. , Montanini , B. , Napoli , C. , Nelson , D. R. , Nelson , C. , Nieminen , K. , Nilsson , O. , Pereda , V. , Peter , G. , Philippe , R. , Pilate , G. , Poliakov , A. , Razumovskaya , J. , Richardson , P. , Rinaldi , C. , Ritland , K. , Rouzé , P. , Ryaboy , D. , Schmutz , J. , Schrader , J. , Segerman , B. , Shin , H. , Siddiqui , A. , Sterky , F. , Terry , A. , Tsai , C.-J. , Uberbacher , E. , Unneberg , P. , Vahala , J. , Wall , K. , Wessler , S. , Yang , G. , Yin , T. , Douglas , C. , Marra , M. , Sandberg , G. , Van de Peer , Y. and Rokhsar , D. 2006 . The genome of black cottonwood, Populus trichocarpa (Torr. & Gray) . Science , 313 : 1596 – 1604 .
   PubMed Web of Science ®Google Scholar
• Voelckel , C. and Baldwin , I. T. 2004 . Herbivore-induced plant vaccination. Part II. Array-studies reveal the transience of herbivore-specific transcriptional imprints and a distinct imprint from stress combinations . Plant J. , 38 : 650 – 663 .
   PubMed Web of Science ®Google Scholar
• Wang , J. and Constabel , C. P. 2004 . Polyphenol oxidase overexpression in transgenic Populus enhances resistance to herbivory by forest tent caterpillar (Malacosoma disstria) . Planta , 220 : 87 – 96 .
   PubMed Web of Science ®Google Scholar
• Weigel , D. , Ahn , J. H. , Blázquez , M. A. , Borevitz , J. O. , Christensen , S. K. , Fankhauser , C. , Ferrándiz , C. , Kardailsky , I. , Malancharuvil , E. J. , Neff , M. M. , Nguyen , J. T. , Sato , S. , Wang , Z. Y. , Xia , Y. , Dixon , R. A. , Harrison , M. J. , Lamb , C. J. , Yanofsky , M. F. and Chory , J. 2000 . Activation tagging in Arabidopsis . Plant Physiol. , 122 : 1003 – 1013 .
   PubMed Web of Science ®Google Scholar
• Whitham , T. G. , DiFazio , S. P. , Schweitzer , J. A. , Shuster , S. M. , Allan , G. J. , Bailey , J. K. and Woolbright , S. A. 2008 . Perspective - Extending genomics to natural communities and ecosystems . Science , 320 : 492 – 495 .
   PubMed Web of Science ®Google Scholar
• Woodward , C. , Bemis , S. M. , Hill , E. J. , Sawa , S. , Koshiba , T. and Torii , K. U. 2005 . Interaction of auxin and ERECTA in elaborating Arabidopsis inflorescence architecture revealed by the activation tagging of a new member of the YUCCA family putative flavin monooxygenases . Plant Physiol. , 139 : 192 – 203 .
   PubMed Web of Science ®Google Scholar
• Woolbright , S. A. , DiFazio , S. P. , Yin , T. , Martinsen , G. D. , Zhang , X. , Allan , G. J. , Whitham , T. G. and Keim , P. 2008 . A dense linkage map of hybrid cottonwood (Populus fremontii × P. angustifolia) contributes to long-term ecological research and comparison mapping in a model forest tree . Heredity , 100 : 59 – 70 .
   PubMed Web of Science ®Google Scholar
• Yin , T. M. , DiFazio , S. P. , Gunter , L. E. , Riemenschneider , D. and Tuskan , G. A. 2004 . Large-scale heterospecific segregation distortion in Populus revealed by a dense genetic map . Theor. App. Genet. , 109 : 451 – 463 .
   PubMed Web of Science ®Google Scholar
• Yu , H. , Chen , X. , Hong , Y. Y. , Wang , Y. , Xu , P. , Ke , S. D. , Liu , H. Y. , Zhu , J. K. , Oliver , D. J. and Xiang , C. B. 2008 . Activated expression of an Arabidopsis HD-START protein confers drought tolerance with improved root system and reduced stomatal density . Plant Cell , 20 : 1134 – 1151 .
   PubMed Web of Science ®Google Scholar
• Zhang , D. , Zhang , Z. , Yang , K. and Li , B. 2004 . Genetic mapping in (Populus tomentosa × Populus bolleana) and P. tomentosa Carr. using AFLP markers . Theor. App. Genet. , 108 : 657 – 662 .
   PubMed Web of Science ®Google Scholar
• Zhang , J. , Wrage , E. L. , Vankova , R. , Malbeck , J. and Neff , M. M. 2006 . Over-expression of SOB5 suggests the involvement of a novel plant protein in cytokinin-mediated development . Plant J. , 46 : 834 – 848 .
   PubMed Web of Science ®Google Scholar