title: Plants on early alert: glandular trichomes as sensors for insect herbivores.
abstract: The ability of caterpillar or moth 'footsteps' to elicit defenses in the tomato (Solanum lycopersicum) plant was examined. Although touch responses frequently have been observed in plants, the role of herbivore 'touch' in eliciting antiherbivore defenses has not been adequately examined. A combination of methods, including in situ hybridization, reverse transcriptase-polymerase chain reaction, quantitative real-time polymerase chain reaction and gas chromatography-mass spectrometry, was used to determine the role of trichomes in mediating these touch responses. Mutants compromised in jasmonic acid and glandular trichomes were used to test whether both of these were required for these touch responses. We demonstrated that the rupture of foliar glandular trichomes by caterpillar or moth contact induced the expression of defense transcripts (e.g. proteinase inhibitor 2, or PIN2) regulated by jasmonic acid. Neither chewing nor the release of salivary components was required to initiate this induced response. Jasmonic acid and the genes encoding proteins involved in its biosynthesis were identified in the trichomes. Using mutants, we showed that both jasmonic acid and trichomes were required for the contact-induced expression of PIN2. In addition, hydrogen peroxide, formed on the leaf surface, was required for PIN2 expression. Because these defenses would be activated before egg hatch, this early detection system for herbivores may be of considerable ecological significance.
authors.affiliation: Department of Entomology and Center for Chemical Ecology, The Pennsylvania State University, University Park, PA 16802, USA.
authors.forename: Michelle
authors.initials: M
authors.lastname: Peiffer
authors.affiliation: Department of Entomology and Center for Chemical Ecology, The Pennsylvania State University, University Park, PA 16802, USA.
authors.forename: John F
authors.initials: JF
authors.lastname: Tooker
authors.affiliation: Department of Crop and Soil Science and Center for Chemical Ecology, The Pennsylvania State University, University Park, PA 16802, USA.
authors.forename: Dawn S
authors.initials: DS
authors.lastname: Luthe
authors.affiliation: Department of Entomology and Center for Chemical Ecology, The Pennsylvania State University, University Park, PA 16802, USA.
authors.forename: Gary W
authors.initials: GW
authors.lastname: Felton
mesh_terms: D000818:Animals; D001483:Base Sequence; D003517:Cyclopentanes / Q000378:metabolism / Q000494:pharmacology; D017931:DNA Primers / Q000235:genetics; D018744:DNA, Plant / Q000235:genetics; D018506:Gene Expression Regulation, Plant / Q000187:drug effects; D017343:Genes, Plant; D054884:Host-Pathogen Interactions / Q000235:genetics / Q000502:physiology*; D006861:Hydrogen Peroxide / Q000378:metabolism; D018551:Solanum lycopersicum / Q000187:drug effects / Q000235:genetics / Q000502:physiology*; D009036:Moths / Q000502:physiology*; D009154:Mutation; D054883:Oxylipins / Q000378:metabolism / Q000494:pharmacology; D019441:Plant Epidermis / Q000502:physiology; D010940:Plant Proteins / Q000235:genetics / Q000502:physiology; D015398:Signal Transduction; D014110:Touch / Q000502:physiology
chemical_list: D003517:Cyclopentanes; D017931:DNA Primers; D018744:DNA, Plant; D054883:Oxylipins; D010940:Plant Proteins; C034104:proteinase inhibitor II protein, plant; C011006:jasmonic acid; D006861:Hydrogen Peroxide
references.citation: Abdala-Roberts L, Parra-Tabla V. 2005. Artificial defoliation induces trichome production in the tropical shrub Cnidoscolus aconitifolius (Euphorbiaceae). Biotropica 37: 251-257.
references.citation: Agrawal AA, Conner JK, Johnson MTG, Wallsgrove R. 2002. Ecological genetics of an induced plant defense against herbivores: additive genetic variance and costs of phenotypic plasticity. Evolution 56: 2206-2213.
references.citation: Amme S, Rutten T, Melzer M, Sonsmann G, Vissers JPC, Schlesier B, Mock HP. 2005. A proteome approach defines protective functions of tobacco leaf trichomes. Proteomics 5: 2508-2518.
references.citation: De Azevedo SM, Faria MV, Maluf WR, De Oliveira ACB, De Freitas JA. 2003. Zingiberene-mediated resistance to the South American tomato pinworm derived from Lycopersicon hirsutum var. hirsutum. Euphytica 134: 347-351.
references.citation: Aziz N, Paiva NL, May GD, Dixon RA. 2005. Transcriptome analysis of alfalfa glandular trichomes. Planta 221: 28-38.
references.citation: Besser K, Harper A, Welsby N, Schauvinhold I, Slocombe S, Li Y, Dixon RA, Broun P. 2009. Divergent regulation of terpenoid metabolism in the trichomes of wild and cultivated tomato species. Plant Physiology 149: 499-514.
references.citation: Boughton AJ, Hoover K, Felton GW. 2005. Methyl jasmonate application induces increased densities of glandular trichomes on tomato, Lycopersicon esculentum. Journal of Chemical Ecology 31: 2211-2216.
references.citation: Bown AW, Hall DE, MacGregor KB. 2002. Insect footsteps on leaves stimulate the accumulation of 4-aminobutyrate and can be visualized through increased chlorophyll fluorescence and superoxide production. Plant Physiology 129: 1430-1434.
references.citation: Braam J. 2005. In touch: plant responses to mechanical stimuli. New Phytologist 165: 373-389.
references.citation: Cahill JF, Castelli JP, Casper BB. 2001. The herbivory uncertainty principle: visiting plants can alter herbivory. Ecology 82: 307-312.
references.citation: Calo L, Garcia I, Gotor C, Romero LC. 2006. Leaf hairs influence phytopathogenic fungus infection and confer an increased resistance when expressing a Trichoderma alpha-1,3-glucanase. Journal of Experimental Botany 57: 3911-3920.
references.citation: Chippendale GM. 1970. Metamorphic changes in fat body proteins of Southwestern corn-borer, Diatraea grandiosella. Journal of Insect Physiology 16: 1057-1068.
references.citation: Choi Y-E, Harada E, Kim G-H, Yoon E-S, Sano H. 2004. Distribution of elements on tobacco trichomes and leaves under cadmium and sodium stresses. Journal of Plant Biology 47: 75-82.
references.citation: Chu CC, Natwick ET, Chen TY, Henneberry TJ. 2003. Analyses of cotton leaf characteristics effect on Bemisia tabaci (Homoptera: Aleyrodidae) biotype B colonization on cotton in Arizona and California. Southwestern Entomologist 28: 235-240.
references.citation: Clauss MJ, Dietel S, Schubert G, Mitchell-Olds T. 2006. Glucosinolate and trichome defenses in a natural Arabidopsis lyrata population. Journal of Chemical Ecology 32: 2351-2373.
references.citation: Conrath U, Beckers GJM, Flors V, Garcia-Agustin P, Jakab G, Mauch F, Newman MA, Pieterse CMJ, Poinssot B, Pozo MJ et al. 2006. Priming: getting ready for battle. Molecular Plant-Microbe Interactions 19: 1062-1071.
references.citation: Dalin P, Bjorkman C. 2003. Adult beetle grazing induces willow trichome defence against subsequent larval feeding. Oecologia 134: 112-118.
references.citation: 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.
references.citation: Depege N, Varenne M, Boyer N. 2000. Induction of oxidative stress and GPX-like protein activation in tomato plants after mechanical stimulation. Physiologia Plantarum 110: 209-214.
references.citation: Duffey SS. 1986. Plant glandular trichomes: their partial role in defence against insects. In: Juniper BE, Southwood TE, eds. Insects and the plant surface. London, UK: Arnold, 151-172.
references.citation: Duffey SS, Isman MB. 1981. Inhibition of insect larval growth by phenolics in glandular trichomes of tomato leaves. Cellular and Molecular Life Sciences (CMLS) 37: 574-576.
references.citation: Engelberth J, Alborn HT, Schmelz EA, Tumlinson JH. 2004. Airborne signals prime plants against insect herbivore attack. Proceedings of the National Academy of Science, USA 101: 1781-1785.
references.citation: English-Loeb G, Norton A. 2006. Lack of trade-off between direct and indirect defence against grape powdery mildew in riverbank grape. Ecological Entomology 31: 415-422.
references.citation: Farrar RR, Kennedy G. 1991. Inhibition of Telenomus sphingis an egg parasitoid of Manduca spp by trichome 2-tridecanone-based host plant-resistance in tomato. Entomologia Experimentalis et Applicata 60: 157-166.
references.citation: Forterre Y, Skotheim JM, Dumais J, Mahadevan L. 2005. How the Venus flytrap snaps. Nature 433: 421-425.
references.citation: Freeman JL, Zhang LH, Marcus MA, Fakra S, McGrath SP, Pilon-Smits EAH. 2006. Spatial imaging, speciation, and quantification of selenium in the hyperaccumulator plants Astragalus bisulcatus and Stanleya pinnata. Plant Physiology 142: 124-134.
references.citation: Frelichowski JE, Juvik JA. 2001. Sesquiterpene carboxylic acids from a wild tomato species affect larval feeding behavior and survival of Helicoverpa zea and Spodoptera exigua (Lepidoptera : Noctuidae). Journal of Economic Entomology 94: 1249-1259.
references.citation: Gassmann AJ, Hare JD. 2005. Indirect cost of a defensive trait: variation in trichome type affects the natural enemies of herbivorous insects on Datura wrightii. Oecologia 144: 62-71.
references.citation: Goertzen L-R, Small E. 1993. The defensive role of trichomes in black medick (Medicago lupulina, Fabaceae). Plant Systematics and Evolution 184: 101-111.
references.citation: Graham JS, Pearce G, Merryweather J, Titani K, Ericsson LH, Ryan CA. 1985. Wound-induced proteinase inhibitors from tomato leaves. II. The cDNA-deduced primary structure of pre-inhibitor II. Journal of Biological Chemistry 260: 6561-6564.
references.citation: Hall DE, MacGregor KB, Nijsse J, Bown AW. 2004. Footsteps from insect larvae damage leaf surfaces and initiate rapid responses. European Journal of Plant Pathology 110: 441-447.
references.citation: Handley R, Ekbom B, Agren J. 2005. Variation in trichome density and resistance against a specialist insect herbivore in natural populations of Arabidopsis thaliana. Ecological Entomology 30: 284-292.
references.citation: Hare JD. 2005. Biological activity of acyl glucose esters from Datura wrightii glandular trichomes against three native insect herbivores. Journal of Chemical Ecology 31: 1475-1491.
references.citation: Hare J-D, Elle E. 2002. Variable impact of diverse insect herbivores on dimorphic Datura wrightii. Ecology 83: 2711-2720.
references.citation: Hare JD, Walling LL. 2006. Constitutive and jasmonate-inducible traits of Datura wrightii. Journal of Chemical Ecology 32: 29-47.
references.citation: Hilker M, Meiners T. 2002. Induction of plant responses to oviposition and feeding by herbivorous arthropods: a comparison. Entomologia Experimentalis et Applicata 104: 181-192.
references.citation: Hilker M, Meiners T. 2006. Early herbivore alert: insect eggs induce plant defense. Journal of Chemical Ecology 32: 1379-1397.
references.citation: Howe GA, Lightner J, Browse J, Ryan CA. 1996. An octadecanoid pathway mutant (JL5) of tomato is compromised in signaling for defense against insect attack. Plant Cell 8: 2067-2077.
references.citation: Iijima Y, Gang D-R, Fridman E, Lewinsohn E, Pichersky E. 2004. Characterization of geraniol synthase from the peltate glands of sweet basil. Plant Physiology 134: 370-379.
references.citation: Kant MR, Ament K, Sabelis MW, Haring MA, Schuurink RC. 2004. Differential timing of spider mite-induced direct and indirect defenses in tomato plants. Plant Physiology 135: 483-495.
references.citation: Karban R. 2008. Plant behaviour and communication. Ecology Letters 11: 727-739.
references.citation: Kashyap RK, Kennedy GG, Farrar RR. 1991. Mortality and inhibition of Helicoverpa zea egg parasitism rates by Trichogramma in relation to trichome methyl ketone-mediated insect resistance of Lycopersicon hirsutum-F-glabratum, Accession Pi-134417. Journal of Chemical Ecology 17: 2381-2395.
references.citation: Kazama H, Dan H, Imaseki H, Wasteneys G-O. 2004. Transient exposure to ethylene stimulates cell division and alters the fate and polarity of hypocotyl epidermal cells. Plant Physiology 134: 614-1623.
references.citation: Kessler A, Halitschke R, Diezel C, Baldwin IT. 2006. Priming of plant defense responses in nature by airborne signaling between Artemisia tridentata and Nicotiana attenuata. Oecologia 148: 280-292.
references.citation: Kivimaki M, Karkkainen K, Gaudeul M, Loe G, Agren JON. 2007. Gene, phenotype and function: GLABROUS1 and resistance to herbivory in natural populations of Arabidopsis lyrata. Molecular Ecology 16: 453-462.
references.citation: Lee D, Polisensky DH, Braam J. 2005. Genome-wide identification of touch- and darkness-regulated Arabidopsis genes: a focus on calmodulin-like and XTH genes. New Phytologist 165: 429-444.
references.citation: Li L, Zhao YF, McCaig BC, Wingerd BA, Wang JH, Whalon ME, Pichersky E, Howe GA. 2004. The tomato homolog of CORONATINE-INSENSITIVE1 is required for the maternal control of seed maturation, jasmonate-signaled defense responses, and glandular trichome development. Plant Cell 16: 126-143.
references.citation: Li C, Schilmiller AL, Liu G, Lee GI, Jayanty S, Sageman C, Vrebalov J, Giovannoni JJ, Yagi K, Kobayashi Y et al. 2005. Role of β-oxidation in jasmonate biosynthesis and systemic wound signaling in tomato. Plant Cell 17: 971-986.
references.citation: Liedl BE, Lawson DM, White KK, Shapiro JA, Cohen DE, Carson WG, Trumble JT, Mutschler MA. 1995. Acylsugars of wild tomato Lycopersicon pennellii alters settling and reduces oviposition of Bemisia argentifolii (Homoptera, Aleyrodidae). Journal of Economic Entomology 88: 742-748.
references.citation: Liu J, Xia KF, Zhu JC, Deng YG, Huang XL, Hu BL, Xu XP, Xu ZF. 2006. The nightshade proteinase inhibitor IIb gene is constitutively expressed in glandular trichomes. Plant and Cell Physiology 47: 1274-1284.
references.citation: Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔC(T) method. Methods 25: 402-408.
references.citation: Lobato-Ortiz R, Schuster DJ, Mutschler MA. 2007. Second generation of tomato acylsugar lines with reduction in S. pennellii DNA content are resistant to silverleaf whitefly and improved for fruit characters. Hortscience 42: 1015.
references.citation: Lopez L, Camas A, Shivaji R, Ankala A, Williams WP, Luthe D. 2007. Mir 1-CP, a novel defense cysteine protease accumulates in maize vascular tissue in response to herivory. Planta 226: 517-527.
references.citation: Matos CHC, Pallini A, Chaves FF, Schoereder JH, Janssen A. 2006. Do domatia mediate mutualistic interactions between coffee plants and predatory mites? Entomologia Experimentalis et Applicata 118: 185-192.
references.citation: Mauricio R, Rausher MD. 1997. Experimental manipulation of putative selective agents provides evidence for the role of natural enemies in the evolution of plant defense. Evolution 51: 1435-1444.
references.citation: McGurl B, Orozcocardenas M, Pearce G, Ryan CA. 1994. Overexpression of the prosystemin gene in transgenic tomato plants generates a systemic signal that constitutively induces proteinase-inhibitor synthesis. Proceedings of the National Academy of Sciences, USA 91: 9799-9802.
references.citation: Medeiros AH, Tingey WM. 2006. Glandular trichomes of Solanum berthaultii and its hybrids with Solanum tuberosum affect nymphal emergence, development, and survival of Empoasca fabae (Homoptera: Cicadellidae). Journal of Economic Entomology 99: 1483-1489.
references.citation: Miersch O, Neumerkel J, Dippe M, Stenzel I, Wasternack C. 2008. Hydroxylated jasmonates are commonly occurring metabolites of jasmonic acid and contribute to a partial switch-off in jasmonate signaling. New Phytologist 177: 114-127.
references.citation: Niesenbaum RA, Cahill JF, Ingersoll CM. 2006. Light, wind, and touch influence leaf chemistry and rates of herbivory in Apocynum cannabinum (Apocynaceae). International Journal of Plant Sciences 167: 969-978.
references.citation: Nihoul P. 1993. Do light-intensity, temperature and photoperiod affect the entrapment of mites on glandular hairs of cultivated tomatoes. Experimental & Applied Acarology 17: 709-718.
references.citation: Nihoul P. 1994. Phenology of glandular trichomes related to entrapment of Phytoseiulus-Ersimilis a-H in the glasshouse tomato. Journal of Horticultural Science 69: 783-789.
references.citation: 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. Plant Cell 13: 179-191.
references.citation: Peiffer M, Felton GW. 2005. The host plant as a factor in the synthesis and secretion of salivary glucose oxidase in larval Helicoverpa zea. Archives of Insect Biochemistry and Physiology 58: 106-113.
references.citation: Ranger CM, Backus EA, Winter R, Rottinghaus GE, Ellersieck MR, Johnson DW. 2004. Glandular trichome extracts from Medicago sativa deter settling by the potato leafhopper Empoasca fabae. Journal of Chemical Ecology 30: 927-943.
references.citation: Roda AL, Oldham NJ, Svatos A, Baldwin IT. 2003. Allometric analysis of the induced flavonols on the leaf surface of wild tobacco (Nicotiana attenuata). Phytochemistry 62: 527-536.
references.citation: Romero GQ, Benson WW. 2005. Biotic interactions of mites, plants and leaf domatia. Current Opinion in Plant Biology 8: 436-440.
references.citation: Rotenberg D, Thompson TS, German TL, Willis DK. 2006. Methods for effective real-time RT-PCR analysis of virus-induced gene silencing. Journal of Virological Methods 138: 49-59.
references.citation: Sagi M, Davydov O, Orazova S, Yesbergenova Z, Ophir R, Stratmann JW, Fluhr R. 2004. Plant respiratory burst oxidase homologs impinge on wound responsiveness and development in Lycopersicon esculentum. Plant Cell 16: 616-628.
references.citation: Schilmiller AL, Howe GA. 2005. Systemic signaling in the wound response. Current Opinions in Plant Biology 8: 369-377.
references.citation: Schmelz EA, Engelberth J, Alborn HT, O’Donnell P, Sammons M, Toshima H, Tumlinson JH. 2003. Simultaneous analysis of phytohormones, phytotoxins, and volatile organic compounds in plants. Proceedings of the National Academy of Sciences, USA 100: 10552-10557.
references.citation: Schmelz EA, Engelberth J, Tumlinson JH, Block A, Alborn HT. 2004. The use of vapor phase extraction in metabolic profiling of phytohormones and other metabolites. Plant Journal 39: 790-808.
references.citation: Schnee C, Kollner TG, Held M, Turlings TCJ, Gershenzon J, Degenhardt J. 2006. The products of a single maize sesquiterpene synthase form a volatile defense signal that attracts natural enemies of maize herbivores. Proceedings of the National Academy of Sciences, USA 103: 1129-1134.
references.citation: Shepherd RW, Wagner GJ. 2007. Phylloplane proteins: emerging defenses at the aerial frontline? Trends in Plant Science 12: 51-56.
references.citation: Shepherd RW, Bass WT, Houtz RL, Wagner GJ. 2005. Phylloplanins of tobacco are defensive proteins deployed on aerial surfaces by short glandular trichomes. Plant Cell 17: 1851-1861.
references.citation: Simmons AT, Gurr GM. 2004. Trichome-based host plant resistance of Lycopersicon species and the biocontrol agent Mallada signata: are they compatible? Entomologia Experimentalis et Applicata 113: 95-101.
references.citation: Simmons AT, Gurr GM. 2005. Trichomes of Lycopersicon species and their hybrids: effects on pests and natural enemies. Agricultural and Forest Entomology 7: 265-276.
references.citation: Simmons AT, Gurr GM, McGrath D, Martin PM, Nicol HI. 2004. Entrapment of Helicoverpa armigera (Hubner) (Lepidoptera : Noctuidae) on glandular trichomes of Lycopersicon species. Australian Journal of Entomology 43: 196-200.
references.citation: Simmons AT, Nicol HI, Gurr GM. 2006. Resistance of wild Lycopersicon species to the potato moth, Phthorimaea operculella (Zeller) (Lepidoptera : Gelechiidae). Australian Journal of Entomology 45: 81-86.
references.citation: Slocombe SP, Schauvinhold I, McQuinn RP, Besser K, Welsby NA, Harper A, Aziz N, Li Y, Larson TR, Giovannoni J et al. 2008. Transcriptomic and reverse genetic analyses of branched-chain fatty acid and acyl sugar production in Solanum pennellii and Nicotiana benthamiana. Plant Physiology 148: 1830-1846.
references.citation: Snyder JC, Thacker RR, Zhang XM. 2005. Genetic transfer of a twospotted spider mite (Acari: Tetranychidae) repellent in tomato hybrids. Journal of Economic Entomology 98: 1710-1716.
references.citation: Steffens JC, Walters DS. 1991. Biochemical aspects of glandular trichome-mediated insect resistance in the Solanaceae. ACS Symposium fSeries 449: 136-149.
references.citation: Stratmann JW, Stelmach BA, Weiler EW, Ryan CA. 2000. UVB/UVA radiation activates a 48 kDa myelin basic protein kinase and potentiates wound signaling in tomato leaves. Photochemistry and Photobiology 71: 116-123.
references.citation: Telewsk FW. 2006. A unified hypothesis of mechanoperception in plants. American Journal of Botany 93: 1466-1476.
references.citation: Thaler JS, Farag MA, Pare PW, Dicke M. 2002. Jasmonate-deficient plants have reduced direct and indirect defences against herbivores. Ecology Letters 5: 764-774.
references.citation: Thipyapong P, Joel DM, Steffens JC. 1997. Differential expression and turnover of the tomato polyphenol oxidase gene family during vegetative and reproductive development. Plant Physiology 113: 707-718.
references.citation: Ton J, D’Alessandro M, Jourdie V, Jakab G, Karlen D, Held M, Mauch-Mani B, Turlings TCJ. 2007. Priming by airborne signals boosts direct and indirect resistance in maize. Plant Journal 49: 16-26.
references.citation: Tooker JF, De Moraes CM. 2005. Jasmonate in lepidopteran eggs and neonates. Journal of Chemical Ecology 31: 2753-2759.
references.citation: Tooker JF, De Moraes CM. 2009. A gall-inducing caterpillar species increases essential fatty acid content of its host plant without concomitant increases in phytohormone levels. Molecular Plant-Microbe Interactions 22: 551-559.
references.citation: Traw MB, Bergelson J. 2003. Interactive effects of jasmonic acid, salicylic acid, and gibberellin on induction of trichomes in Arabidopsis. Plant Physiology 133: 1367-1375.
references.citation: Traw MB, Dawson TE. 2002a. Differential induction of trichomes by three herbivores of black mustard. Oecologia 131: 526-532.
references.citation: Traw MB, Dawson TE. 2002b. Reduced performance of two specialist herbivores (Lepidoptera: Pieridae, Coleoptera: Chrysomelidae) on new leaves of damaged black mustard plants. Environmental Entomology 31: 714-722.
references.citation: Valkama E, Koricheva J, Ossipov V, Ossipova S, Haukioja E, Pihlaja K. 2005. Delayed induced responses of birch glandular trichomes and leaf surface lipophilic compounds to mechanical defoliation and simulated winter browsing. Oecologia 146: 385-393.
references.citation: Valkana E, Koricheva J, Salminen J-P, Helander M, Saloniemi I, Saikkonen K, Pihlaja K. 2005. Leaf surface traits: overlooked determinants of birch resistance to herbivores and foliar micro-fungi? Trees (Berlin) 19: 191-197.
references.citation: Van Dam NM, Hare JD. 1998a. Biological activity of Datura wrightii glandular trichome exudate against Manduca sexta larvae. Journal of Chemical Ecology 24: 1529-1549.
references.citation: Van Dam NM, Hare JD. 1998b. Differences in distribution and performance of two sap-sucking herbivores on glandular and non-glandular Datura wrightii. Ecological Entomology 23: 22-32.
references.citation: Van De Ven WTG, LeVesque CS, Perring TM, Walling LL. 2000. Local and systemic changes in squash gene expression in response to silverleaf whitefly feeding. Plant Cell 12: 1409-1423.
references.citation: Wagner GJ. 1991. Secreting glandular trichomes - more than just hairs. Plant Physiology 96: 675-679.
references.citation: Wang E, Hall JT, Wagner GJ. 2004. Transgenic Nicotiana tabacum L. with enhanced trichome exudate cembratrieneols has reduced aphid infestation in the field. Molecular Breeding 13: 49-57.
references.citation: Wasternack C, Stenzel I, Hause B, Hause G, Kutter C, Maucher H, Neumerkel J, Feussner I, Miersch O. 2006. The wound response in tomato - role of jasmonic acid. Journal of Plant Physiology 163: 297-306.
references.citation: Wilkens RT, Shea GO, Halbreich S, Stamp NE. 1996. Resource availability and the trichome defenses of tomato plants. Oecologia 106: 181-191.
references.citation: Williams WG, Kennedy GG, Yamamoto RT, Thacker JD, Bordner J. 1980. 2-Tridecanone - naturally-occurring insecticide from the wild tomato Lycopersicon hirsutum f-glabratum. Science 207: 888-889.
references.citation: Yerger EH, Grazzini RA, Hesk D, Coxfoster DL, Craig R, Mumma RO. 1992. A rapid method for isolating glandular trichomes. Plant Physiology 99: 1-7.
references.citation: Zhu-Salzman K, Luthe DS, Felton GW. 2008. Arthropod-inducible proteins: broad spectrum defenses against multiple herbivores. Plant Physiology 146: 852-858.