Insect Herbivory on Low-Lignin Transgenic Aspen

Environmental Entomology, Dec 2006

Ecological effects of genetically modified plants cannot always be predicted based on knowledge of the plant species or transgene. We studied the effects of transgenic aspen (Populus tremuloides Michaux) with reduced lignin and altered growth phenotypes on the feeding performance of gypsy moth larvae (Lymantria dispar L.) and forest tent caterpillars (Malacosoma disstria Hübner). Developmental trials were conducted using one control line and four separate transgenic lines of aspen. Gypsy moth larvae showed a significant reduction in survival on one high-lignin reduction transgenic tree line relative to all other lines, but weights of surviving larvae were similar across tree lines. Forest tent caterpillars showed similar survival and weights on all tree lines. Trials were also conducted to evaluate whether gypsy moth larvae preferred feeding on high-lignin reduction transgenic aspen lines or control trees. While gypsy moth larvae showed no significant preference between the control line and the transgenic line that caused significant reductions in larval survival during developmental trials, they did strongly prefer transgenic leaves causing no such reductions in larval survival. Because effects on feeding larvae varied among tree lines, we concluded that any potential phytochemical alterations in the transgenic lines could not be directly linked to lignin reduction. Because only one transgenic tree line had a negative effect on the herbivores, we propose that this may be an indirect consequence of transgenic manipulation resulting from the insertion point of the antisense Pt4CL gene in the genome, rather than 4CL suppression or lignin reduction.

A PDF file should load here. If you do not see its contents the file may be temporarily unavailable at the journal website or you do not have a PDF plug-in installed and enabled in your browser.

Alternatively, you can download the file locally and open with any standalone PDF reader:

https://academic.oup.com/ee/article-pdf/35/6/1696/18302293/ee35-1696.pdf

Insect Herbivory on Low-Lignin Transgenic Aspen

Environ. Entomol. Insect Herbivory on Low-Lignin Transgenic Aspen 0 Department of Evolution , Ecology , and Organismal Biology, Ohio State University , Columbus, OH 43210 , USA 1 School of Forest Resources and Environmental Science, Michigan Technological University , 1400 Townsend Dr. Houghton, MI 49931 , USA Ecological effects of genetically modiÞed plants cannot always be predicted based on knowledge of the plant species or transgene. We studied the effects of transgenic aspen (Populus tremuloides Michaux) with reduced lignin and altered growth phenotypes on the feeding performance of gypsy moth larvae (Lymantria dispar L.) and forest tent caterpillars (Malacosoma disstria Hu¨ bner). Developmental trials were conducted using one control line and four separate transgenic lines of aspen. Gypsy moth larvae showed a signiÞcant reduction in survival on one high-lignin reduction transgenic tree line relative to all other lines, but weights of surviving larvae were similar across tree lines. Forest tent caterpillars showed similar survival and weights on all tree lines. Trials were also conducted to evaluate whether gypsy moth larvae preferred feeding on high-lignin reduction transgenic aspen lines or control trees. While gypsy moth larvae showed no signiÞcant preference between the control line and the transgenic line that caused signiÞcant reductions in larval survival during developmental trials, they did strongly prefer transgenic leaves causing no such reductions in larval survival. Because effects on feeding larvae varied among tree lines, we concluded that any potential phytochemical alterations in the transgenic lines could not be directly linked to lignin reduction. Because only one transgenic tree line had a negative effect on the herbivores, we propose that this may be an indirect consequence of transgenic manipulation resulting from the insertion point of the antisense Pt4CL gene in the genome, rather than 4CL suppression or lignin reduction. plantÐinsect interactions; Populus tremuloides; Lymantria dispar; Malacosoma disstria; transgenic lignin reduction - Separating lignin from cellulose during pulping of wood entails signiÞcant energetic and chemical expenses and signiÞcant environmental costs (Chiang 2002, Pilate et al. 2002) . Lignin separation costs the paper and pulp industry 20 billion dollars per year (Mann and Plummer 2002) . For these reasons, transgenic aspen (Populus tremuloides Michaux) with reduced lignin has been generated, using antisense down-regulation of a Pt4CL1 (4-coumarate: CoA ligase) gene, controlled by a Caulißower Mosaic Virus 35S constitutive promoter (Hu et al.1999). 4CL is involved in phenylpropanoid metabolism (Fig. 1), catalyzing the activation of hydroxycinnamic acids into high-energy CoA-intermediates for lignin and ßavonoid synthesis. Therefore, transgenic alterations of 4CL could impact tree metabolism, growth, and defense allocation of nonlignin phenolics in addition to reducing lignin content. Analysis of these transgenic aspen trees revealed increased cellulose and hemicellulose deposition in the xylem, substantially increased root growth, leaf size, and overall growth rates (Hu et al. 1999) . Additional tests found that the transgenic aspen stem wood contained increased wall-bound ferulic, sinapic, and 4-coumaric acids (Hu et al. 1999) . Within the leaves, cell wall esterÞed 4-coumaric and ferulic acids were decreased (Harding et al. 2002) . Alterations in both leaf growth rates and phenolic proÞles in the transgenic aspen could potentially impact ecological relationships between plants and herbivores. Increased plant growth is often associated with reduced defenses against herbivores (Hwang and Lindroth 1997) . However, phenolic compounds are important and widely distributed plant allelochemicals (Schowalter 2000). They make up the majority of the defense compounds found in aspen, especially in the forms of phenolic glycosides and condensed tannins (Arteel and Lindroth 1992) . Therefore, changes in either plant growth rates or phenolic proÞles could impact which insects feed on lignin-reduced transgenic aspen. The digestive and assimilative capabilities, development time, and survival of feeding insects could also be altered. Changes in fundamental aspects of the plantÐ herbivore relationship could be either positive or negative for herbivorous insects, depending on which chemicals are altered; feeding on such plants could be easier because of lower or otherwise altered defensive compounds or more difÞcult because of increased or otherwise altered defensive compounds. Changes in feeding capabilities may also not be uniform across all insect species and may depend on the characteristics of individual species. Some insect species could respond positively to phenolic changes, whereas other species respond negatively to the same changes. Trembling aspen has many associated insect herbivores, including gypsy moth larvae (Lymantria dispar L.; L (...truncated)


This is a preview of a remote PDF: https://academic.oup.com/ee/article-pdf/35/6/1696/18302293/ee35-1696.pdf

Brodeur-Campbell, Sarah E., Vucetich, John A., Richter, Dana L., Waite, Thomas A., Rosemier, Justin N., Tsai, Chung-Jui. Insect Herbivory on Low-Lignin Transgenic Aspen, Environmental Entomology, 2006, pp. 1696-1701, Volume 35, Issue 6, DOI: 10.1093/ee/35.6.1696