Abstract
Endogenous levels and signaling of gibberellin plant hormones such as gibberellic acid (GA) have been genetically down-regulated to create semi-dwarf varieties of poplar. The potential benefits of semi-dwarf stature include reduced risk of wind damage, improved stress tolerance, and improved wood quality. Despite these benefits, modification of growth traits may have consequences for nontarget traits that confer defense against insect herbivores. According to the growth-differentiation balance hypothesis, reductions in growth may shift allocation of carbon from growth to chemical resistance traits, thereby altering plant defense. To date, host-plant suitability and pest response have not been comprehensively evaluated in GA down-regulated plants. We quantified chemical resistance and nitrogen (an index of protein) in GA down-regulated and wild-type poplar (Populus alba × P. tremula) genotypes. We also evaluated the performance of both generalist (Lymantria dispar) and specialist (Chrysomela scripta) insect pests reared on these genotypes. Our evaluation of resistance traits in four GA down-regulated genotypes revealed increased phenolic glycosides in one modified genotype and reduced lignin in two modified genotypes relative to the non-transgenic wild type. Nitrogen levels did not vary significantly among the experimental genotypes. Generalists reared on the four GA down-regulated genotypes exhibited reduced performance on only one modified genotype relative to the wild type. Specialists, however, performed similarly across all genotypes. Results from this study indicate that although some nontarget traits varied among GA down-regulated genotypes, the differences in poplar pest susceptibility were modest and highly genotype-specific.
Similar content being viewed by others
References
Abreu IN, Ahnlund MA, Moritz T, Albrectsen BR (2011) UHPLC-ESI/TOFMS determination of salicylate-like phenolic glycosides in Populus tremula leaves. J Chem Ecol 37:857–870
Alvim PDT (1960) Net assimilation rate and growth behavior of beans as affected by gibberellic acid urea and sugar sprays. Plant Physiol 35:285
Appel HM, Maines LW (1995) The influence of host plant on gut conditions of gypsy moth (Lymantria dispar) caterpillars. J Insect Physiol 41:241–246
Barbehenn RV, Constabel CP (2011) Tannins in plant-herbivore interactions. Phytochemistry 72:1551–1565
Bidart-Bouzat MG, Kliebenstein D (2011) An ecological genomic approach challenging the paradigm of differential plant responses to specialist versus generalist insect herbivores. Oecologia 167:677–689
Biemelt S, Tschiersch H, Sonnewald U (2004) Impact of altered gibberellin metabolism on biomass accumulation, lignin biosynthesis, and photosynthesis in transgenic tobacco plants. Plant Physiol 135:254–265
Bingaman BR, Hart ER (1993) Clonal and leaf age variation in Populus phenolic glycosides: implications for host selection by Chrysomela scripta (Coleoptera: Chrysomelidae). Environ Entomol 22:397–403
Boeckler A, Gershenzon J, Unsicker S (2011) Phenolic glycosides of the Salicaceae and their role as anti-herbivore defenses. Phytochemisrty 72:1497–1509
Bowers DM, Puttick GM (1988) Response of generalist and specialist insects to qualitative allelochemical variation. J Chem Ecol 14:319–334
Bryant JP, Chapin SF III, Klein D (1983) Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40:357–368
Buhl C (2013) Effects of genetic modification on non-target traits that confer defense in hybrid poplar (Populus tremula × Populus alba). Dissertation, University of Wisconsin-Madison
Burkot TR, Benjamin DM (1977) The bionomics of the cottonwood leaf beetle, Chrysomela scripta Fab., on tissue culture hybrid poplars. In: Proceedings of the thirteenth lake states forest tree improvement conference; General Technical Report NC-50. US Department of Agriculture Forest Service, Minnesota, 131–135
Busov VB, Meilan R, Pearce DW, Ma C, Rood SB, Strauss SH (2003) Activation tagging of a dominant gibberellin catabolism gene (GA 2-oxidase) from poplar that regulates tree stature. Plant Physiol 132:1283–1291
Busov VR, Meilan D, Pearce W, Rood SB, Ma C, Tschaplinski TJ, Strauss SH (2006) Transgenic modification of gai or rgl1 causes dwarfing and alters gibberellins, root growth and metabolite profiles in Populus. Planta 224:288–299
Caldbeck ES, McNabb HS, Hart ER (1978) Poplar clonal preferences of cottonwood leaf beetle. J Econ Entomol 71:518–520
Chen F, Liu CJ, Tschaplinski TJ, Zhao N (2009) Genomics of secondary metabolism in Populus: interactions with biotic and abiotic environments. Crit Rev Plant Sci 28:375–392
Couture JJ, Meehan TD, Lindroth RL (2012) Atmospheric change alters foliar quality of host trees and performance of two outbreak insect species. Oecologia 168:863–876
Coyle DR, Nebeker TE, Hart ER, Mattson WJ (2005) Biology and management of insect pests in North American intensively managed hardwood forest systems. Annu Rev Entomol 50:1–29
Coyle DR, Allred AM, Kosola KR, Raffa KF (2011) Altered GAI activity of hybrid aspen has minimal effects on the performance of a polyphagous weevil, Polydrusus sericeus. Entomol Exp Appl 138:104–109
de Lucas M, Davière J-M, Rodríguez-Falcón M, Pontin M, Iglesias-Pedraz JM, Lorrain S, Fankhauser C, Blázquez MA, Titarenko E, Prat S (2008) A molecular framework for light and gibberellin control of cell elongation. Nature 451:480–484
Dickmann DI, Stuart KW (1983) The culture of poplars in eastern North America. Michigan State University, Michigan
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
Edwards PB, Wanjura WJ, Brown WV (1993) Selective herbivory by Christmas beetles in response to intraspecific variation in Eucalyptus terpenoids. Oecologia 95:551–557
Elias AA, Busov VB, Kosola KR, Ma C, Etherington E, Shevchenko O, Gandhi H, Pearce DW, Rood SB, Strauss SH (2012) Green revolution trees: semidwarfism transgenes modify gibberellins, promote root growth, enhance morphological diversity and reduce competitiveness in hybrid poplar. Plant Physiol 160:1130–1144
Etherington E, Gandhdhi H, Busov V, Meilan R, Ma C, Kosolala K, Strauss SH (2007) Dwarfism genes for modifying the stature of woody plants: a case study in poplar. Landsc Plant News 18:3–6
Gou J, Strauss SH, Tsai CJ, Fang K, Chen Y, Jiang X, Busov VB (2010) Gibberellins regulate lateral root formation in Populus through interactions with auxin and other hormones. Plant Cell 22:623–639
Haber AH, Tolbert NE (1957) Photosynthesis in gibberellin-treated leaves. Plant Physiol 32:152
Hagerman AE, Butler JG (1980) Condensed tannin purification and characterization of tannin-associated proteins. J Agr Food Chem 28:947–952
Han KM, Dharmawardhana P, Arias RS, Ma C, Busov V, Strauss SH (2010) Gibberellin-associated cisgenes modify growth, stature and wood properties in Populus. Plant Biotech J 9:162–178
Hemming JDC, Lindroth RL (1995) Intraspecific variation in aspen phytochemistry—effects on performance of gypsy moths and forest tent caterpillars. Oecologia 103:79–88
Hemming JDC, Lindroth RL (2000) Effects of phenolic glycosides and protein on gypsy moth (Lepidoptera: Lymantriidae) and forest tent caterpillar (Lepidoptera: Lasiocampidae) performance and detoxication activities. Environ Entomol 29:1108–1115
Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335
Hjältén J, Lindau A, Wennström A, Blomberg P, Witzell J, Hurry V, Ericson L (2007) Unintentional changes of defence traits in GM trees can influence plant-herbivore interactions. Basic Appl Ecol 8:434–443
Hjältén J, Lindau A, Wennström A, Blomberg P, Witzell J, Hurry V, Ericson L, Moritz T, Karlsson J (2008) Vole response to unintentional changes in the chemistry of GM poplars. Chemoecology 18:227–231
Hu JJ, Tian YC, Han YF, Li L, Zhang BE (2001) Field evaluation of insect-resistant transgenic Populus nigra trees. Euphytica 121:123–127
Hwang SY, Lindroth RL (1997) Clonal variation in foliar chemistry of aspen: effects on gypsy moths and forest tent caterpillars. Oecologia 111:99–108
Ikonen A (2002) Preferences of six leaf beetle species among qualitatively different age classes of three Salicaceous host species. Chemoecol 12:23–28
Jansson S, Douglas CJ (2007) Populus: a model system for plant biology. Annu Rev Plant Biol 58:435–458
Joshi CP, Thammannagowda S, Fujino T, Gou JQ, Avci U, Haigler CH, McDonnell LM, Mansfield SD, Mengesha B, Carpita NC, Harris D, DeBolt S, Peter GF (2011) Perturbation of wood cellulose synthesis causes pleiotropic effects in transgenic aspen. Mol Plant 4:331–345
Kosonen M, Keski-Saari S, Ruuhola T, Constabel CP, Julkunen-Tiitto R (2012) Effects of overproduction of condensed tannins and elevated temperature on chemical and ecological traits of genetically modified hybrid aspens (Populus tremula × P. tremuloides). J Chem Ecol 38:1235–1246
Lindroth RL, Hwang S-H (1996) Phytochemical diversity and redundancy in ecological interactions. In: Thirty-fifth annual meeting of the phytochemical society of North America on phytochemical diversity and redundancy in ecological interactions. Plenum Press, Ontario
Lindroth RL, St. Clair SB (2013) Adaptations of quaking aspen (Populus tremuloides Michx.) for defense against herbivores. For Ecol Manag 299:14–21
Little CHA, Loach K (1975) Effect of gibberellic acid on growth and photosynthesis in Abies balsamea. Can J Bot 53:1805–1810
Loomis WE (1932) Growth-differentiation balance vs. carbohydrate-nitrogen ratio. Proc Am Soc Hortic Sci 29:240–245
Luis AG, Guardiola JL (1981) Effect of gibberellic acid on ion uptake selectivity in pea seedlings. Planta 153:494–496
Marth PC, Audia WV, Mitchell JW (1956) Effect of gibberellic acid on growth and development of various species of plants. Bot Gaz 118:106–111
Mattson WJ (1980) Herbivory in relation to plant nitrogen-content. Annu Rev Ecol Syst 11:119–161
Mishiba K, Nakatsuka T, Abe Y, Hirano H, Yokoi T, Kikuchi A, Yamamura S (2005) Consistent transcriptional silencing of 35S-driven transgenes in gentian. Plant J 44:541–556
Montgomery ME (1986) Gypsy moth host plant relationships and population dynamics. In: Proceedings of the 18th International Union of Forest Research Organizations World Congress. Division 2, Vol II. Forest plants and forest protection, Yugoslavia
Oerke E-C (2006) Crop losses to pests. J Agr Sci 144:31
Ohkuma M (2003) Termite symbiotic systems: efficient bio-recycling of lignocellulose. Appl Microbiol Biotech 61:1–9
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, Hwang S-Y, Lindroth RL (2000) Effects of phytochemical variation in quaking aspen Populus tremuloides clones on gypsy moth Lymantria dispar performance in the field and laboratory. Ecol Entomol 25:197–207
Paspatis EA (1990) Effects of external application of gibberellic acid (GA3) on yield and nitrate content of spinach. Zizaniology 2:161–166
Pasteels JM, Rowell-Rahier M, Braekman JC, Dupont A (1983) Salicin from host plant as a precursor of salicyaldehyde in defensive secretion of Chrysomeline larvae. Physiol Entomol 8:307–314
Peng J, Carol P, Richards DE, King KE, Cowling RJ, Murphy GP, Harberd NP (1997) The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. Genes Dev 11:3194–3205
Philippe RN, Bohlmann J (2007) Poplar defense against insect herbivores. Can J Bot 85:1111–1126
Porter LJ, Hrstich LN, Chan BG (1986) The conversion of procyanidins and prodelphinidins to cyanidin and delphinidin. Phytochemistry 25:223–230
Post KH, Parry D (2011) Non-target effects of transgenic blight-resistant American chestnut (Fagales: Fagaceae) on insect herbivores. Environ Entomol 40:955–963
Riley JM (1987) Gibberellic acid for fruit set and seed germination. Calif Rare Fruitgrow J 19:10–12
Robinson KM, Ingvarsson PK, Jansson S, Albrectsen BR (2012) Genetic variation in functional traits influences arthropod community composition in aspen (Populus tremula L.). PLoS One 7:e37679
Roth S, Knorr C, Lindroth RL (1997) Dietary phenolics affects performance of the gypsy moth (Lepidoptera: Lymantriidae) and its parasitoid Cotesia melanoscela (Hymenoptera: Braconidae). Environ Entomol 26:668–671
Rowland AP, Roberts JD (1994) Lignin and cellulose fractionation in decomposition studies using acid-detergent fiber methods. Commun Soil Sci Plant Anal 25:269–277
Salminen J-P, Karonen M (2011) Chemical ecology of tannins and other phenolics: we need a change in approach. Funct Ecol 25:325–338
Scheirs J, De Bruyn L, Verhagen R (2001) Nutritional benefits of the leaf-mining behaviour of two grass miners: a test of the selective feeding hypothesis. Ecol Entomol 26:509–516
Taiz L, Zeiger E (2006) Plant Physiology. Sinauer, Massachusetts
Takahashi N, Kitamura H, Kawarada A, Seta Y, Takai M, Tamura S, Sumiki Y (1955) Isolation of gibberellins and their properties. Bull Agr Chem Soc Jpn 19:267–277
Vauramo S, Pasonen H-L, Pappinen A, Setälä H (2006) Decomposition of leaf litter from chitinase transgenic silver birch (Betula pendula) and effects on decomposer populations in a field trial. Appl Soil Ecol 32:338–349
Wolf EEH, Loubser JT (1992) Gibberellic acid levels and quality effects of gibberellic acid in treated table grapes. S Afr J Ecol Vitic 13:57
Ye X, Busov V, Zhao N, Meilan R, McDonnell LM, Coleman HD, Mansfield SD, Chen F, Li Y, Cheng Z-M (2012) Transgenic Populus trees for forest products, bioenergy and functional genomics. Crit Rev Plant Sci 30:415–434
Yıldırım AN, Bekir S, Koyuncu F, Yıldırım F (2010) Variability of phenolics, α-tocopherol and amygdalin contents of selected almond (Prunus amygdalus Batsch.) genotypes. J Food Agr Environ 8:76–79
Zawaski C, Kadmiel M, Pickens J, Ma C, Strauss S, Busov V (2011) Repression of gibberellin biosynthesis or signaling produces striking alterations in poplar growth, morphology and flowering. Planta 234:1285–1298
Zehnder CB, Stodola KW, Joyce BL, Egetter D, Cooper RJ, Hunter MD (2009) Elevational and seasonal variation in the foliar quality and arthropod community of Acer pensylvanicum. Environ Entomol 38:1161–1167
Acknowledgments
This work was supported by the University of Wisconsin (Hatch grant no. WIS01336 to R.L. Lindroth) and the US Department of Energy’s Poplar Genome-Based Research for Carbon Sequestration in Terrestrial Ecosystems Program (grant nos. DE–FG02–06ER64185 and DE–FG02–05ER64113 to S.H. Strauss). We thank David Coyle of the University of Georgia for providing cottonwood leaf beetles for this study. We also thank members of the Lindroth lab for assistance with fieldwork and chemical analyses (K. Rubert-Nason, N. Fons, J. Bishop) and comments on the manuscript (H. Bultman, L. Holeski, K. Rubert-Nason).
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling Editors: Guy Smagghe and Heikki Hokkanen.
Rights and permissions
About this article
Cite this article
Buhl, C., Strauss, S.H. & Lindroth, R.L. Down-regulation of gibberellic acid in poplar has negligible effects on host-plant suitability and insect pest response. Arthropod-Plant Interactions 9, 85–95 (2015). https://doi.org/10.1007/s11829-014-9351-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11829-014-9351-y