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)