Down-regulation of gibberellic acid in poplar has negligible effects on host-plant suitability and insect pest responseArthropod-Plant Interactions

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Authors
Christine Buhl, Steven H. Strauss, Richard L. Lindroth
Year
2015
DOI
10.1007/s11829-014-9351-y
Subject
Agronomy and Crop Science / Ecology, Evolution, Behavior and Systematics / Insect Science / Ecology

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ORIGINAL PAPER

Down-regulation of gibberellic acid in poplar has negligible effects on host-plant suitability and insect pest response

Christine Buhl • Steven H. Strauss •

Richard L. Lindroth

Received: 6 June 2014 / Accepted: 2 December 2014 / Published online: 6 January 2015  Springer Science+Business Media Dordrecht 2014

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 9 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 downregulated 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.

Keywords Genetically modified plants  Gibberellic acid  Nontarget plant defense  Plant–insect interactions 

Cottonwood leaf beetle  Gypsy moth

Introduction

Gibberellins are naturally occurring plant hormones that promote cell growth as well as aspects of flowering and fruiting (Paspatis 1990; Edwards et al. 1993; Yıldırım et al. 2010). Gibberellic acid (GA) is the first gibberellin to be structurally characterized (Takahashi et al. 1955) and is often utilized for crop enhancement. Exogenous application of bioactive GAs increases plant growth and improves fruit quality and yield (Marth et al. 1956; Riley 1987; Wolf and Loubser 1992). Endogenous levels of bioactive GAs, or their signal cascades, may be artificially altered via up- or down-regulation of associated biosynthetic, catabolic, or signaling genes (Ye et al. 2012).

Down-regulation of GA action has been used to create dwarf plant varieties. Such plants typically exhibit reduced biomass production but may also exhibit increased root-to-shoot ratio, altered leaf morphology and/ or canopy architecture (Busov et al. 2006; Han et al. 2010; Zawaski et al. 2011). Successful down-regulation of

GA action has been achieved in trees such as poplar, which are important forestry and biofuel crops. The

Handling Editors: Guy Smagghe and Heikki Hokkanen.

C. Buhl (&)  R. L. Lindroth

Entomology, University of Wisconsin-Madison, 1630 Linden

Drive, Madison, WI 53706, USA e-mail: buhl@uwalumni.com

S. H. Strauss

Department of Forest Ecosystems and Society, Oregon State

University, 321 Richardson Hall, Corvallis, OR 97331, USA 123

Arthropod-Plant Interactions (2015) 9:85–95

DOI 10.1007/s11829-014-9351-y benefits of dwarf tree varieties for use as forestry crops include reduced risk of lodging and reaction wood formation (Busov et al. 2003). Dwarf trees may also be cultivated more densely and harvested more easily, facilitating their use for short-rotation coppice biofuel crops (Busov et al. 2003). Despite the potential benefits of

GA down-regulation, however, there is also the potential for negative consequences for nontarget traits.

Consistent with the growth-differentiation balance hypothesis (GDBH), modification of target traits could alter resource trade-offs with nontarget traits, resulting in unanticipated changes in nontarget trait expression (Hja¨lte´n et al. 2007; Joshi et al. 2011; Kosonen et al. 2012). The

GDBH states that carbon not allocated to growth is available for other traits, such as resistance to herbivores (Loomis 1932; Herms and Mattson 1992). According to this hypothesis, if photosynthesis remains constant carbon may accumulate in plants with reduced growth requirements (e.g., GA down-regulated plants). Once carbon requirements are satisfied for growth, ‘excess’ carbon may then be shifted toward resistance traits. Net photosynthesis may be altered by exogenous application of GA, although photosynthetic rate is not altered and is thus predicted to be unchanged when GA is genetically down-regulated (Haber and Tolbert 1957; Alvim 1960; Little and Loach 1975).

The mechanism of GA action is not fully understood, but clearly involves the induction and inhibition of numerous transcription factors, thus with effects on many downstream metabolic processes (Taiz and Zeiger 2006; de

Lucas et al. 2008). The growth-differentiation balance hypothesis is supported by evidence of higher levels of phenolic resistance traits in leaves and roots of GA downregulated poplar genotypes relative to wild types (Busov et al. 2006). These phenolics confer resistance against many generalist pests, although they may serve as attractants for some specialist pests (Boeckler et al. 2011).

The primary chemical resistance traits utilized by poplar are the phenolic secondary metabolites condensed tannins and phenolic glycosides. Condensed tannins (CTs) deter vertebrate herbivory and have been correlated with reduced larval growth rate, pupal mass and survival of some invertebrate pest species (Bryant et al. 1983; Donaldson and Lindroth 2004; Salminen and Karonen 2011). Phenolic glycosides (PGs) inhibit growth, development and fecundity for many invertebrate pest species (Hemming and