GENET archive


2-Plants: Preserving the effectiveness of Bt crops

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SOURCE: ISB News Report, USA, by Anthony Shelton
DATE:   Sep 2005

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Since their introduction in 1996, the area grown to transgenic plants
expressing insecticidal proteins from the bacterium Bacillus
thuringiensis (Bt) has grown rapidly. In 2004, Bt plants were grown on
over 13 million ha in the U.S. and 22.4 million ha worldwide1,2. Bt corn
and Bt cotton comprised about one-third and one-half, respectively, of
the U.S. corn and cotton markets in 2004. Worldwide, approximately 15
million ha of Bt corn and 7.4 million ha of Bt cotton were grown in 2004.
The economic and environmental benefits of Bt crops, compared to other
technologies, have been well-documented3. Reports from China have also
shown that fewer insecticide poisonings occur when Bt cotton is used4.

Despite the extensive use of Bt crops over an 8-year period, there have
been no reports of product failure or increased resistance in insect
pests5. To put this in perspective, Bt crops have already exceeded the
length of time that typically passes in the field before resistance is
first documented with most conventional neurotoxic pesticides, despite
undergoing what has been hailed as one of the world's largest selection
for resistance6. However, because of the demonstrated ability of two
insect species (the diamondback moth and the cabbage looper) to evolve
resistance to sprays of Bt proteins in commercial settings, there is
concern that some insects may also evolve resistance in the field to Bt
plants. To prevent or delay resistance to Bt crops, various insecticide
resistance management (IRM) strategies have been proposed. These
strategies include manipulation of the transgenic elements of the plants,
such as the genes and promoters, and the manner in which plants are
deployed in the landscape. The most widely employed tactic to delay
resistance is the use of plants expressing a high dose of a single Bt
protein throughout the life of the plant, combined with a "refuge" of
non-Bt plants nearby that can maintain an adequate supply of susceptible
alleles within the insect population. We believe this "high dose/refuge"
strategy has played a major role in the lack of resistance to date for Bt
plants, but recognize that other strategies must be developed as the use
of Bt plants continues to grow and selection for resistance intensifies.

Over the past 15 years, our cooperative program has tested various IRM
strategies using a unique system. The system is composed of different
populations of diamondback moth that have evolved resistance to one or
two Bt proteins (Cry1A and/or Cry1C) and broccoli plants that express
either one or both of these proteins. Our greenhouse and field tests are
described in a recent paper6 in a historical perspective of IRM and Bt
plants. In that paper, we describe the use of this unique system to
demonstrate the effectiveness of the "high dose/refuge" strategy and the
use of an inducible promoter as "proof of concept" by using the inducible
promoter so that the Bt protein is expressed only at a specific period of
time, thus reducing the selection pressure for resistance. Such inducible
promoters allow Bt proteins to be expressed only during specific periods
of time, and could be used in situations in which plants could withstand
some insect defoliation early in their growth, but the marketable part of
the plant must be kept clean during the later stages of growth (e.g.,

An IRM strategy outlined in a 1998 paper by Roush7 suggested that
pyramiding two dissimilar Bt proteins in the same plant could delay
resistance development compared to plants that expressed only one Bt
protein. The models contained in the paper were evaluated using our
diamondback moth/Bt broccoli system, and we found that such Bt pyramided
plants significantly delayed the evolution of resistance8.

Pyramided cotton plants ("Bollgard II") with two genes derived from Bt
(Cry1Ac and Cry2Ab2) were approved for commercial use in Australia and
the U.S. in 2002, and several companies are developing new cotton and
corn varieties with pyramided Bt genes. However, there is concern that
the optimal benefits of pyramided Bt genes for resistance management may
be lost if one-gene plants sharing similar Bt toxins continue to be
deployed. Newly developed pyramided varieties of Bt cotton and corn
currently contain the same or similar genes as one-gene (Cry1Ac for Bt
cotton, Cry1Ab for Bt corn) Bt plants already marketed. If market forces
result in a complicated landscape mix of one- and two-gene Bt plants, the
benefits of pyramided Bt plants for slowing resistance evolution could be
undermined. For example, a modeling study9 suggested that Cry2A
resistance evolution in a cotton pest was maximized when Bt cotton
varieties expressing one- and two-genes were both available, and that the
overall durability of two-gene plants would be greater if they were
deployed alone, compared to a sequential or mosaic deployment with
Bollgard (Cry1Ac alone). However, the risk of pest adaptation to
pyramided Bt plants used in conjunction with one-gene plants had not been
quantified empirically.

To assess the risk of resistance evolution to pyramided plants when they
were simultaneously deployed with single gene plants containing one of
the Bt genes in the pyramided Bt plants, we used broccoli plants
transformed to express different Cry toxins (Cry1Ac, Cry1C, or both) and
populations of diamondback moth carrying resistance to each of the Bt Cry
toxins8. Three treatments were tested in separate large greenhouse cages:
(1) 45% Cry1Ac and 45% two-gene plants plus 10% refuge; (2) 45% Cry1C and
45% two-gene plants plus 10% refuge; (3) 90% two-gene plants plus 10%
refuge. Diamondback moths with a known frequency of resistance alleles to
Cry1Ac and Cry1C were then introduced into each cage. We allowed the
insect populations in each cage to reproduce normally over time. Every
few generations, we counted the number of insects produced in each cage
and determined the frequency of resistance alleles in the insect
population. The results were rather dramatic. After 24 - 26 generations
of selection in the greenhouse, the concurrent use of one- and two-gene
plants resulted in control failure of both types of Bt plants. When only
two-gene plants were used in the cage, no or few insects survived in
subsequent tests on one- or two-gene Bt plants. Overall, this clearly
indicated that the concurrent use of transgenic plants expressing a
single and two Bt genes will select for resistance to two-gene plants
more rapidly than the use of two-gene plants alone. The results of this
experiment agree with the predictions of a Mendelian deterministic
simulation model.

What does this mean for the commercial use of Bt plants? Simply put, the
concurrent use of single and two-gene Bt plants can offer exposed insect
populations a "stepping stone" to develop resistance to both toxins.
Thus, from a resistance management perspective, it appears that using
pyramided Bt plants simultaneously with single-gene plants, if they share
similar Bt toxins, will negate some of the benefits of the two-gene
plants. In Australia, pyramided Bt cotton (Bollgard II) has been
commercially available since 2002. The use of both one- and two-gene
varieties was permitted for the first two years following the
introduction of Bollgard II, but now only two-gene varieties are allowed.
The rapid phaseout of one-gene varieties was intended to minimize pest
exposure to the single Bt toxin and thus to reduce the risk of resistance
to pyramided plants. In the U.S., plants with a single Bt gene remain the
dominant Bt varieties. Our results indicate that the introduction of
pyramided plants with currently deployed single gene plants should be
examined carefully by regulatory agencies. Our data are consistent with
models and suggest that, from an IRM standpoint, it could be advantageous
for regulatory agencies to consider deregulating single gene plants as
soon as pyramided plants are available.

We recognize that economic considerations must be factored into decisions
regarding the deployment of single and pyramided gene plants. From an
industry standpoint, however, there could be distinct economic and
marketing advantages for promoting pyramided plants rather than single
gene plants. In addition to providing superior resistance management,
pyramided plants may provide improved control of some harder-to-kill
insects, and require a smaller area set aside for the refuge. The smaller
refuge size has particular relevance for IRM; models have indicated that
a 30-40% refuge for single gene plants is equivalent to a 5-10% refuge
for pyramided plants7. Thus, the two-gene strategy is especially suitable
for developing countries such as China, where farms on average are only
0.5 ha, and the practice of setting aside land for a refuge is highly


1. U.S. Department of Agriculture-NASS (2004) http://

2. James C. (2004) ISAAA Briefs No. 32. Ithaca, NY: ISAAA. 43 pp

3. Shelton AM, Zhao J-Z & Roush RT. (2002) Ann. Rev. Entomol. 47, 845-881

4. Pray CE, Ma D, Huang J & Qiao F. (2001) Impact of Bt cotton in China.
World Dev. 29, 813-825

5. Tabashnik BE, Carrière Y, Dennehy TJ, Morin S, Sisterson MS, Roush RT,
Shelton AM & Zhao J-Z. (2003) J. Econ. Entomol. 96, 1031-1038

6. Bates SL, Zhao J-Z, Roush RT & Shelton AM. (2005) Nature Biotechnol.
22, 57-62

7. Roush RT. (1998) Phil. Trans. R. Soc. Lond. B 353, 1777-1786

8. Zhao J-Z, Cao J, Li YX, Collins HL, Roush RT, Earle ED & Shelton AM.
(2003) Nature Biotechnol. 21, 1493-1497

9. U.S. Environmental Protection Agency (2002)

Anthony M. Shelton*, J-Z Zhao*, J Cao?, HL Collins*, SL Bates*, RT
Roush§, & ED Earle?
*Dept. of Entomology, Cornell Univ. / NYSAES, Geneva, NY
?Dept. of Plant Breeding and Genetics, Cornell Univ., Ithaca, NY
§Statewide IPM Program, University of California, Davis, CA


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