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2Ministry of Education Key Laboratory for Biodiversity and Ecological Engineering, Institute of Biodiversity Science, Fudan University, Handan Road 220, Shanghai 200433 China; 3Department of Evolution, Ecology, & Organismal Biology, Ohio State University, Columbus, Ohio 43210-1293 USA; 4Fujian Province Key Laboratory of Genetic Engineering for Agriculture, Fujian Academy of Agricultural Sciences, Fuzhou 350003 China
Received for publication May 18, 2005. Accepted for publication October 17, 2005.
ABSTRACT
Understanding the balance between yield benefits and possible underlying yield costs that are associated with transgenic cultivars is useful for evaluating crop performance and the fitness of crop-wild hybrid progeny, but few researchers have tested for such costs under rigorous experimental conditions. We examined shifts in net costs and benefits of insect-resistance transgenes in cultivated rice (Oryza sativa) using two levels of insect pressure (low vs. moderate) and two types of competition (pure vs. mixed lines). We compared the growth and fecundity of potted rice plants from three transgenic lines, Bt, CpTI, and Bt/CpTI, relative to isogenic control plants at outdoor locations in Fuzhou, China. Net yield costs were detected, but only in Bt/CpTI plants in mixed-line competition with low insect pressure. These plants produced 16% fewer tillers, 6% smaller seeds, and 30% fewer seeds than competing control plants. Under moderate insect pressure, Bt and Bt/CpTI plants produced 36–65% more seeds than controls, but the net benefit for Bt/CpTI plants disappeared in mixed-line competition pots. To our knowledge, this is the first report of yield costs in cultivars with transgenic insect resistance. Our results suggest that these costs may be negligible in monotypic rice fields, especially when target insects are abundant.
Key Words: fecundity • fitness • gene flow • genetically modified • insect resistant • Oryza sativa • transgene • yield cost
Many types of genetically modified (GM) crops have transgenic resistance to insects, herbicides, and diseases, and it is widely assumed that these transgenes do not reduce plant performance (e.g., Raymer and Grey, 2003
; Monjardino et al., 2005
). However, few studies have tested explicitly for underlying yield costs in transgenic cultivars by using appropriate control lines and an absence of relevant selective pressures. It is more common to observe yield costs in early generation transformants (e.g., Tu et al., 2000
) than in those that are candidates for large-scale field release because the latter are tested extensively for high performance under a variety of field conditions. Also, small negative effects of transgenes on the growth and yield of GM crops may remain undetected in farmers' fields because the crops are often grown under conditions that demonstrate clear benefits of having transgenic traits. For the purpose of discussion, we refer to such yield costs and benefits as net effects of specific transgenes because they represent the combined effects of any inherent costs and the benefits that accrue from exposure to transgene-specific selective pressures in the field (Fig. 1).
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The frequency of a transgene that introgresses into wild or weedy populations will be influenced by the net effects of any fitness costs and benefits under field conditions, as well as effects of nontransgenic crop traits that are linked to the transgene. It is noteworthy that transgenes are inherited as dominant Mendelian traits that perform their expected function in wild relatives of the crop (e.g., Snow et al., 1999
, 2003
). Because field conditions are variable, it is useful to test for costs of transgenic traits in the absence of other selective pressures that favor transgene persistence. In sunflower (Helianthus annuus), for example, a Bt transgene that was backcrossed into populations of wild sunflower (H. annuus) did not confer any detectable fitness costs when plants were grown in the absence of herbivores, while a strong benefit was seen when target herbivores were abundant (Snow et al., 2003
). Also in sunflower, a transgene coding for resistance to a fungal disease did not decrease the fecundity of wild plants in the absence of disease pressure (Burke and Rieseberg, 2003
). Other studies also found no costs of transgenes coding for herbicide resistance on the growth or seed production of weedy relatives of oilseed rape (Snow et al., 1999
) or rice (Oard et al., 2000
; Zavala et al., 2004
) in the absence of herbicides. In contrast, a transgene for virus resistance was associated with lower biomass in sugar beet and sugar beet–swiss chard hybrids that were not exposed to the disease (Bartsch et al., 1996
, 2001
).
We used rice (Oryza sativa) as a model system to examine underlying costs that may be associated with novel transgenic traits. Many experimental GM rice lines have been engineered to tolerate insects, disease, herbicides, harsh conditions, and other economically important traits (e.g., Shimamoto et al., 1989
; Alam et al., 1998
; Datta et al., 1998
; Giri and Laxmi, 2000
; Wu et al., 2002
; Jiang et al., 2004
). Currently, scientists in China, the United States, and other countries have developed several types of transgenic rice that will be considered for wide-scale use within the next few years (Huang et al., 2002
; Jia, 2004
). Transgenes that confer resistance to insects have been introduced into pre-commercial lines of rice, raising the possibility that these genes could spread to sexually compatible feral, weedy, or wild rice plants that occur nearby (Song et al., 2003
; Chen et al., 2004
; Lu and Snow, 2005
). Insect pests often cause serious damage to rice crops, causing estimated losses of 10–30% of the total yield in Southeast Asia (Khush and Toenniessen, 1991
; Yambao et al., 1993
). Insect-resistant rice cultivars offer advantages to farmers because they can alleviate the need for insecticidal sprays and they deter stem-boring insects that are difficult to control with insecticide applications (e.g., Tu et al., 2000
; Maqbool et al., 1998
; Shu et al., 2002
; Huang et al., 2005
).
The current study was not intended to quantify possible yield costs or expected yield benefits of GM insect-resistant rice in large-scale agricultural fields. Instead, we investigated the biology of GM rice plants to test for subtle, underlying costs that may be associated with transgenes that confer resistance to target pests. We compared the growth and fecundity of GM lines with that of non-GM control plants grown outdoors in pots with low vs. moderate insect pressure. This method for investigating costs is especially useful in situations in which it is not possible to completely prevent insects from damaging non-GM control plants. Figure 1 shows that differences in the magnitude of expected yield benefits for insect-resistant GM plants are affected by both intrinsic costs and the extent to which the plants are exposed to target insect damage. The slope of this relationship, which may or may not be linear, represents the fecundity benefit of the transgene irrespective of associated costs. Transgenes with no effect on fecundity would result in a slope of zero. The magnitude of possible fitness costs may vary with environmental conditions, such as drought stress. Also, direct competition between GM and non-GM lines may have the effect of exacerbating yield costs in the absence of exposure to insect damage and enhancing the net benefit of no-cost transgenes at higher levels of exposure to insects.
We tested for effects of three transgenic events that were engineered for insect resistance: two single-transgene events, Bt (from Bacillus thuringiensis) and CpTI (cowpea trypsin inhibitor), and one double-transgene event, Bt/CpTI, in which the two transgenes were tightly linked. These lines were developed to deter lepidopteran pests, including three types of rice stem borers (yellow, Scirpophaga incertulas; striped, Chilo suppressalis; and pink, Sesamia inferens) and the rice leaf-folder (Cnaphalocrocis medinalis). In field trials approved by the Biosafety Office of Ministry of Agriculture of China, the GM rice lines used in this study exhibited significant yield increases relative to nontransgenic controls when lepidopteran pests were common (F. Wang, unpublished data). Therefore, these transgenic events are being considered for commercial release in China in the near future.
MATERIALS AND METHODS
Plant materials
We used seventh generation selfed progeny (T7) of three homozygous rice lines, Bt, CpTI, and Bt/CpTI. Each line was homozygous for the transgene(s) it contained. The isogenic line Minghui-86 that was transformed with these constructs was used as the non-GM control. Plant materials were provided by one of the authors (F. Wang). The Bt gene, cryIAc, was synthesized in the laboratory and had a constitutive ubiquitin promoter derived from maize. The CpTI gene (known as sck, signal-CpTI-KDEL) was modified from Vigna unguiculata and had a constitutive ActID promoter derived from rice. A single-insertion transgene, either Bt or CpTI, was linked to a hyg (Neomycin phosphotransferase) selectable marker gene, and plants were transformed using particle bombardment. The Bt/CpTI line was obtained using Agrobacterium and the transgenes were present as a single insertion linked to the hyg selectable marker gene. Only one transgenic event was available for study for each of these lines. Therefore, our results are not generalizable to a broader spectrum of transgenic events because we cannot rule out the possibility that other factors such as somaclonal variation or position effects on plant growth could be associated with the transgenic events used in this study. Nonetheless, our study has the advantage of being directly relevant to transgenic lineages that are being considered for large-scale cultivation in China. For brevity, we refer to differences among lines as effects of these transgenes, with the caveat that some of these effects might be due to other factors that vary among transgenic events.
Experimental procedures
Differences between GM and non-GM rice lines were examined by measuring fecundity and other phenotypic characteristics in two environments, a rooftop and a field site, in 2003. On the rooftop, plants were exposed to minimal insect damage, thereby making it easier to detect fecundity costs in transgenic lines as compared to the nontransgenic control. Although it would have been preferable to exclude insect herbivores completely, we did not use a greenhouse to exclude herbivores because we did not have a greenhouse with adequate climate controls. Also, we did not attempt to cage the plants or spray them with insecticides because the former might have shaded the plants too much and the latter was not practical given the logistics of this study. As shown in Fig. 1, it is not necessary to exclude insects completely in order to test for yield costs.
At the field site, plants were exposed to local insect herbivores, and we measured the net effects of any costs and benefits of these transgenes. By using two levels of insect pressure in this study, we were able to test for subtle differences among lines in the balance between potential costs and benefits (Fig. 1). The field site was located in Fuzhou, China, at the field station for rice research of Fujian Agricultural Academy of Science, and the rooftop area was located c. 10 km away.
At both sites, rice plants were grown in large pots (40 cm diameter, 50 cm height) under two types of competition, which we refer to as the "Pure" and "Mixed" experiments, with a sample size of 20 pots in each experiment. Each Pure pot contained six rice plants of the same type (Bt, CpTI, Bt/CpTI, or non-GM controls), while the Mixed pots contained three GM rice plants (Bt, CpTI, or Bt/CpTI) growing alternately and competing with three non-GM control plants. We hypothesized that any differences between a GM line and the controls would be greater in the Mixed pots because the plants competed for soil resources during their growth and development. Competition within pots could allow small differences between lines to become more pronounced, as compared to differences between plants grown separately in the Pure pots.
On 27 June 2003, seeds from the Bt, CpTI, Bt/CpTI lines, and the non-GM control line were placed in an incubator at 27°C after being soaked in water for 24 h. After germination, the seedlings were grown temporarily in a small nursery field that was tilled and irrigated. At the five-leaf stage, young seedlings were transplanted into pots filled with soil collected from the nursery field on 27 July 2003. To avoid possible microsite effects, replicate pots (20 for each treatment) were positioned randomly within the group of 140 pots at each location. The plants were watered frequently and were not treated with insecticides. At both locations, the plants were harvested on 29 October 2003. By this time, the vast majority of plants had fully mature panicles; the few that may have been slower to develop would be expected to have reduced yield under typical field conditions.
For each plant, we measured the total number of normal seeds, total empty seeds, plant height, flag leaf length, flag leaf width, number of tillers, number of panicles, panicle length, and mass per 1000 seeds. We also measured the height and counted the tillers for each plant and at 15-d intervals until the plants were harvested. When the plants were mature, we counted the number of tillers with "blast" damage, which refers to dried, dead seed heads and stems resulting from stem borers. Earlier damage from stem borers, including occasional tiller senescence, was not recorded, nor was damage caused by leaf-folders. Therefore, our data on blasted tillers represents only a portion of the total damage caused by lepidopteran insect larvae. It is possible that a few stems senesced for other reasons, such as physiological stress, but the patchy pattern of stem mortality that we observed was typical of insect damage.
At harvest, all panicles of each individual were cut, bagged, and transported to the laboratory to be dried and analyzed. In the Mixed experiments, where GM and non-GM individuals were planted alternately in the same pot, the three individuals of GM and non-GM lines were bagged separately. Then we counted the number of panicles per plant and measured panicle length. The seeds on each panicle were removed and separated into two groups, good seeds and empty seeds, and the total number in each group was recorded for each plant. Other variables, such as percentage seed set, average seed mass, and the percentage of tillers with blast damage were calculated from these data. In all cases, we calculated the average value of plants of the same genotype in each pot (using six plants in the Pure pots and three plants in the Mixed pots), so N = 20 pots for each dependent variable.
To test for net yield costs or benefits, we compared average values of each GM line with the appropriate non-GM control, using SPSS version 11.0 software (SPSS Inc., Chicago, USA). We used t tests for the Pure pots and paired t test for the Mixed pots at each location. Percentages were arcsine-transformed for these analyses to improve normality. Bonferroni corrections were calculated for the average number of seeds per plant, which is the main variable of interest.
RESULTS
Insect damage on final number of tillers
Plants that were grown on the rooftop experienced much lower levels of blast damage from stem borers than those at the field site, as expected (Fig. 2, Appendix 1). At the end of the study, the four groups of control plants on the rooftop had blast symptoms on 
3–7% of their tillers, while controls at the field site had blast symptoms on 20–30% of their tillers. The amount of blast damage on transgenic lines at the field site was higher than we expected, perhaps because the plants were stressed by unusually hot weather during the summer of 2003. At this site, only one transgenic group, the Bt/CpTI plants grown in the Pure experiment, had significantly lower levels of blast damage than the controls.
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For Bt/CpTI, the net yield costs and benefits varied among experiments (Table 1). At the rooftop site with low insect pressure, the fecundity of GM plants in the Pure competition pots was similar to controls, but with Mixed competition, Bt/CpTI plants produced 30% fewer seeds per plant (P = 0.022), 33% lower seed mass per plant (P = 0.010), and seeds with 6% lower mass (P = 0.023), than the non-GM controls (Fig. 2, Appendix 2). Therefore, yield costs were only detected when the GM lines competed with non-GM controls. At the field site, Bt/CpTI plants produced 60% more seeds per plant than controls in the Pure competition experiment (P = 0.001), demonstrating a net benefit, but no advantage of Bt/CpTI was detected in the Mixed competition experiment. This finding shows that fecundity costs were greater under Mixed competition than Pure competition. In the Mixed experiment, the fecundity costs associated with Bt/CpTI were large enough to offset the advantage that we observed in the Pure competition.
We applied a Bonferroni correction to determine whether the observed fecundity effects were statistically significant with more conservative assumptions (Rice, 1989
). This correction often is recommended for minimizing Type I errors when multiple statistical tests are presented together (Rice, 1989
), but it has been criticized as being too conservative, leading to a surfeit of Type II errors (e.g., Nakagawa, 2004
). Bonferroni corrections were applied to each of the four experiments shown in Fig. 3, such that a value of P < 0.017 (=0.05/3) was set as the threshold for significant differences. When this threshold for significance was used, the cost associated with Bt/CpTI in the Rooftop-Mixed experiment was not quite significant (original P value of 0.022), nor was the net benefit of Bt in the Field-Pure experiment (original P value of 0.028). The net benefits of Bt/CpTI in the Field-Pure experiment (original P value of 0.001) and of Bt in the Field-Mixed experiment remained significant with this threshold (original P value of 0.001). For brevity, we do not report Bonferroni corrections for other dependent variables that are discussed below. Instead, we note some of the differences that were only significant at P < 0.05 could be due to false discovery rates that occur with large numbers of comparisons in the same study (Rice, 1989
).
Other reproductive traits
The three transgenic lines exhibited differences in several other reproductive traits (Table 1, Appendices 1 and 2). Differences in the numbers of panicles per plant were similar to the differences in total seed number, in that increases were seen for Bt (Field-Pure P < 0.05; Field-Mixed P < 0.01) and Bt/CpTI (Field-Pure P < 0.01) relative to controls.
A few other differences among transgenic lines are noteworthy. In several cases, average seed mass, reported as 1000-seed mass, was lower in GM lines than controls (Table 1, Appendix 2). This occurred in all of the Bt/CpTI groups (Rooftop-Pure P < 0.05; Rooftop-Mixed P < 0.05; Field-Pure P < 0.001; and Field-Mixed, P < 0.001). The consistency of this effect across all four experiments indicates a disadvantage of Bt/CpTI that may have commercial implications. Percentage seed set was higher than controls for Bt plants in two experiments, Rooftop-Pure (P < 0.05) and Field-Pure (P < 0.001), and lower than controls in Bt/CpTI in the Rooftop-Mixed experiment (P < 0.001) and CpTI in the Rooftop-Mixed experiment (P < 0.01).
Growth and development
Several positive and negative effects of the transgenes were detected on growth and development relative to control plants (Table 1, Appendices 1–4). Some of these responses were not associated with differences in fecundity, perhaps due to allocation trade-offs or the fact that they were small in magnitude. Nonetheless, these findings provide insights into differential effects of the three transgenic lines relative to the controls.
Tiller number changed during the course of the study due to the combined effects of growth and senescence (Appendix 3). Effects of the transgenes on tiller number at the end of the study explain some of the effects on seed production (Table 1). For example, Bt/CpTI plants produced fewer tillers per plant when grown on the rooftop under Mixed competition. This effect was not seen at the field site, where Bt plants produced more tillers per plant than controls during most of the season in both Pure and Mixed competition experiments. This translated into more panicles per plant and resulted in more seeds per plant for Bt plants in both competition experiments. At the field site, the CpTI line produced more tillers per plant than controls, but only in the Mixed competition experiment. This translated into more panicles per plant, but the overall effect on fecundity was not significant (Table 1, Appendix 1).
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Effects of transgenes on fecundity
The major goal of this research was to use two levels of insect pressure to examine shifts in the balance between yield costs and benefits among three transgenic rice lines relative to the nontransgenic controls. Two of the transgenic lines, Bt and CpTI, did not have any net fecundity costs relative to control plants by the end of the study. In contrast, Bt/CpTI plants in the Rooftop-Mixed experiment exhibited net costs in terms of the final number of tillers per plant, percentage seed set, number of seeds per plant, and average seed mass (Table 1, Fig. 3). These net costs were substantial, resulting in 30% fewer seeds per plant and seeds that were 5–6% smaller than controls. With the exception of lower seed mass, however, these costs were not detected in the other three experiments. In those experiments, an underlying cost can be inferred for field-grown Bt/CpTI by comparing the fecundity of plants in Pure competition with those in the Mixed competition—the net benefit of the transgene that was seen in Pure competition disappeared under Mixed competition, which suggests a greater cost in the latter.
In summary, we conclude that the Bt/CpTI line exhibited an underlying fecundity cost, but this cost was only detectable under specific sets of conditions. To our knowledge, this is the first demonstration of fecundity costs that are associated with transgenic insect resistance. Further studies are needed to determine whether such costs could ever be great enough to reduce crop yields under realistic, large-scale rice cultivation; this seems unlikely because the costs we observed were not detected in the monoculture pots. Also, the summer of 2003 was unusually hot, and it would be useful to examine these costs under a broader range of environmental conditions.
To draw broader conclusions about the transgenes in this study, we would need to know whether the observed yield cost was due to unique features of the Bt/CpTI transgene or to smaller additive effects of Bt and CpTI. Other researchers have not found evidence for inherent fecundity costs of Bt transgenes in canola or sunflower (e.g., Ramachandran et al., 2000
; Snow et al., 2003
), but similar studies have not been carried out with CpTI. In any case, as noted before, our study does not allow us to generalize about all Bt, CpTI, or Bt/CpTI events in cultivated rice because we used only one transformation event for each of the three transgenic lines. Thus, it is not possible to know whether the costs associated with Bt/CpTI are due to the transgenes themselves or whether other factors such as position effects, selectable markers, or somoclonal mutations were the cause of decreased fecundity in this line.
Challenges of detecting yield costs
One challenge of testing for costs of particular transgenes is the difficulty of obtaining contrasting cultivars with the same genetic background, such that differences among cultivars can be attributed to a specific transgene construct independently of other crop genes (e.g., Raymer and Grey, 2003
). Also, few such studies have tested for yield costs in competing plants that are grown under a range of environmental conditions. In the literature on transgenic crops, statements about the absence of growth or yield costs are common, but they are often anecdotal, and crop performance typically is measured in the presence of relevant selective pressures that could mask underlying costs. Crop breeders and producers are more interested in the net effects of transgenes on yield and economic value, whereas ecologists who study gene flow to wild and weedy relatives need information about both positive and negative effects on fecundity in the context of highly variable field conditions.
Our study demonstrates that mixed-genotype competition may be essential for allowing variable but potentially significant fecundity costs to be detected. Likewise, Godfree et al. (2004)
tested for fitness costs of a sunflower albumin transgene in clover (Trifolium subterraneum) and found that transgenic plants had significantly lower survivorship than nontransgenic controls when grown at high densities. However, in sugar beet (Beta vulgaris), yield costs associated with transgenic virus resistance were not affected by competition (Bartsch et al., 1996
, 2001
). These investigators detected yield costs regardless of whether sugar beet was grown in competition with a common weed (Chenopodium album). In a second study, they also found a cost of the transgene in field experiments involving hybrids between sugar beet and swiss chard (also Beta vulgaris), expressed as reduced biomass, regardless of whether the plants competed with Chenopodium album (Bartsch et al., 2001
). Several previous studies of the costs of transgenic traits have not included competition treatments (e.g., Snow et al., 1999
, 2003
; Burke and Rieseberg, 2003
).
The mechanism for the yield cost in virus-resistant sugar beet, described earlier, is not known and could be related to pleiotropic effects or a particular transgenic event. With Bt transgenes, the amount of protein that is allocated to a new plant product may be so low (e.g., parts per thousand), as to have no detectable effect on plant performance in the absence of target herbivores. In future types of transgenic crops, we expect that some transgenes will be associated with easily detected net fecundity costs, including transgenes that alter major patterns of resource allocation or plant architecture (e.g., Al-Ahmad et al., 2004
) and transgenes that have a negative effect on metabolic pathways (e.g., Bergelson et al., 1996
). In these cases, novel traits might enhance the value of the crop despite causing reductions in seed production.
Implications for crop-to-wild gene flow
We are currently investigating the effects of Bt, CpTI, or Bt/CpTI transgenes on fitness-related traits in wild and weedy relatives of the crop. The extent to which these transgenes would be favored by natural selection will depend on herbivore pressure in unmanaged populations and the net fitness effects that the transgenes confer, as well as effects of other genes that introgress from the crop following episodes of spontaneous hybridization. Although it is not possible to extrapolate results from the crop to possible effects in wild and weedy plants, the present study provides an experimental approach that can be used to test for these effects, as well as insights into which types of transgenes may be associated with net fecundity costs or benefits in other genotypes.
FOOTNOTES
The authors thank the National Natural Science Foundation of China for Distinguished Young Scholars (Grant no. 30125029) and Shanghai Commission of Science and Technology (Grant nos. 02JC14022 and 03dz19309) for support to B.-R. Lu; T. Waite and L. Campbell of Ohio State University, Drs. B. Li, Z. P. Song, and Y. P. Geng of Fudan University for help with statistical analysis; the reviewers for constructive suggestions; and Mr. S. H. Xie, J. M. Chen, and Z. Y. Xie for field assistance. 
5 Author for correspondence (e-mail: brlu{at}fudan.edu.cn
)
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