Abstract
Expression of the Bacillus thuringiensis beetle-specific toxin Cry3Aa, which renders a genetically modified potato cultivar resistant to the Colorado potato beetle Leptinotarsa decemlineata, exerts a deleterious effect on the polyphagous moth Spodoptera littoralis. The caterpillars of S. littoralis feed less and produce smaller pupae on the genetically modified cultivar (NewLeaf Superior) than on the parental nontransgenic cultivar (Superior). The conversion efficiencies of total dry matter, combustion heat, carbon, and nitrogen from leaves to insect biomass are similar on both cultivars. In spite of similar food utilization and a relatively small difference in the body mass at pupation, female adults that developed from caterpillars fed on NewLeaf Superior lay a mean of 309 eggs compared to a mean of 713 eggs deposited by females that developed from caterpillars fed on Superior. Because of this difference and a simultaneous reduction in fertility (egg hatchability) from 78 to 48%, a pair of adults that fed as larvae on NewLeaf Superior produces only 148 larvae, whereas a pair of adults that fed as larvae on Superior produces 556 larvae. We suggest that small amounts of Cry3Aa that accumulate in insect tissue and persist until the adult stage are responsible for the decline in reproduction.

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S. Arpaia L. Marzo ParticleDe G. M. Leo ParticleDi M. E. Santoro G. Mennella J. J. A. Loon ParticleVan (2000) ArticleTitleFeeding behaviour and reproductive biology of Colorado potato beetle adults fed transgenic potatoes expressing the Bacillus thuringiensis Cry3B endotoxin Entomol. Exp. Appl. 95 31–37 Occurrence Handle10.1023/A:1003961817187 Occurrence Handle1:CAS:528:DC%2BD3cXjvVWjtb4%3D
R. Deml T. Meise K. Dettner (1999) ArticleTitleEffects of Bacillus thuringiensis δ-endotoxins on food utilization, growth, and survival of selected phytophagous insects J. Appl. Entomol. 123 55–64 Occurrence Handle10.1046/j.1439-0418.1999.00312.x Occurrence Handle1:CAS:528:DyaK1MXhvVGns7w%3D
J. J. Duan G. Head A. Jensen G. Reed (2004) ArticleTitleEffects of transgenic Bacillus thuringiensis potato and conventional insecticides for Colorado potato beetle (Coleoptera: Chrysomelidae) management on the abundance of ground-dwelling arthropods in Oregon potato ecosystems Environ. Entomol. 33 275–281 Occurrence Handle1:CAS:528:DC%2BD2cXjvFyls7o%3D
A. Dutton J. Romeis F. Bigler (2003) ArticleTitleAssessing the risks of insect resistant transgenic plants on entomophagous arthropods: Bt-maize expressing Cry1Ab as a case of study Biocontrol 48 611–636 Occurrence Handle10.1023/A:1026313719424 Occurrence Handle1:CAS:528:DC%2BD3sXosFWqu70%3D
E. Gazit D. Bach I. D. Kerr M. S. P. Sansom N. Chejanovsky Y. Shai (1994) ArticleTitleThe alpha-5 segment of Bacillus thuringiensis delta-endotoxin: in vitro activity, ion channel formation and molecular modeling Biochem. J. 304 895–902 Occurrence Handle1:CAS:528:DyaK2MXisVagtr8%3D Occurrence Handle7529493
P. Grochulski L. Masson S. Borisova M. Pusztai-Carey J. L. Schwartz R. Brousseau M. Cygler (1995) ArticleTitleBacillus thuringiensis CrylA(a) insecticidal toxin—crystal-structure and channel formation J. Mol. Biol. 254 447–464 Occurrence Handle10.1006/jmbi.1995.0630 Occurrence Handle1:CAS:528:DyaK2MXpvVCmsrw%3D Occurrence Handle7490762
A. M. Heimpel (1967) ArticleTitleA critical review of Bacillus thuringiensis var. thuringiensis Berliner and other crystalliferous bacteria Annu. Rev. Entomol. 12 287–322 Occurrence Handle10.1146/annurev.en.12.010167.001443 Occurrence Handle1:STN:280:CCiB3M3it10%3D Occurrence Handle5340721
A. Hilbeck M. Baumgartner P. M. Fried F. Bigler (1998a) ArticleTitleEffects of transgenic Bacillus thuringiensis corn-fed prey on mortality and development time of immature Chrysoperla carnea (Neuroptera: Chrysopidae) Environ. Entomol. 27 480–487
A. Hilbeck W. J. Moar M. Pusztai-Carey A. Filippini F. Bigler (1998b) ArticleTitleToxicity of Bacillus thuringiensis Cry1Ab toxin to the predator Chrysoperla carnea (Neuroptera: Chrysopidae) Environ. Entomol. 27 1255–1263 Occurrence Handle1:CAS:528:DyaK1cXnt12ktbg%3D
A. Hilbeck W. J. Moar M. Pusztai-Carey A. Filippini F. Bigler (1999) ArticleTitlePrey-mediated effects of Cry1Ab toxin and protoxin and Cry2A protoxin on the predator Chrysoperla carnea Entomol. Exp. Appl. 91 305–316 Occurrence Handle10.1023/A:1003678630661 Occurrence Handle1:CAS:528:DyaK1MXmsFyisbo%3D
H. M. Hussein O. Habuštová F. Sehnal (2005) ArticleTitleBeetle-specific Bacillus thuringiensis Cry3Aa toxin reduces larval growth and curbs reproduction in Spodoptera littoralis (Boisd) Pest. Manag. Sci 61 1186–1192 Occurrence Handle10.1002/ps.1112 Occurrence Handle1:CAS:528:DC%2BD2MXht1ehtLzO Occurrence Handle16152673
B. H. Knowles (1994) ArticleTitleMechanism of action of Bacillus thuringiensis insecticidal δ-endotoxins Adv. Insect Physiol. 24 275–308 Occurrence Handle1:CAS:528:DyaK2cXkt12isr0%3D
J. D. Li J. Carroll D. J. Ellar (1991) ArticleTitleCrystal-structure of insecticidal delta-endotoxin from Bacillus thuringiensis at 2.5-Å resolution Nature 353 815–821 Occurrence Handle10.1038/353815a0 Occurrence Handle1:CAS:528:DyaK3MXmslejtL8%3D Occurrence Handle1658659
F. Ortego C. Novillo J. J. Sanchez-Serrano P. Castanera (2001) ArticleTitlePhysiological response of Colorado potato beetle and beet armyworm larvae to depletion of wound-inducible proteinase inhibitors in transgenic potato plants J. Insect Physiol. 47 1291–1300 Occurrence Handle10.1016/S0022-1910(01)00118-4 Occurrence Handle1:CAS:528:DC%2BD3MXntlOrs7g%3D Occurrence Handle12770181
F. J. Perlak T. B. Stone Y. M. Muskopf L. J. Petersen G. B. Parker S. A. McPherson J. Wyman S. Love G. Reed D. Biever D. A. Fischhoff (1993) ArticleTitleGenetically improved potatoes: protection from damage by Colorado potato beetles Plant Mol. Biol. 22 313–321 Occurrence Handle10.1007/BF00014938 Occurrence Handle1:CAS:528:DyaK3sXltlGktLc%3D Occurrence Handle8507832
G. L. Reed A. S. Jensen J. Riebe G. Head J. J. Duan (2001) ArticleTitleTransgenic Bt potato and conventional insecticides for Colorado potato beetle management: Comparative efficacy and non-target impacts Entomol. Exp. Appl. 100 89–100 Occurrence Handle10.1023/A:1019250105811 Occurrence Handle1:CAS:528:DC%2BD3MXms1Oru7o%3D
E. W. Riddick P. Barbosa (1998) ArticleTitleImpact of Cry3A-intoxicated Leptinotarsa decemlineata (Coleoptera: Chrysomelidae) and pollen on consumption, development, and fecundity of Coleomegilla maculata (Coleoptera: Coccinellidae) Ann. Entomol. Soc. Am. 91 303–307
E. Schnepf N. Crickmore J. Rie ParticleVan D. Lereclus J. Baum J. Feitelson D. R. Zeigler D. H. Dean (1998) ArticleTitleBacillus thuringiensis and its pesticidal crystal proteins Microbiol. Mol. Biol. Rev. 62 775–806 Occurrence Handle1:CAS:528:DyaK1cXmtFOju7w%3D Occurrence Handle9729609
J. M. Scriber (2004) ArticleTitleNon-target impacts of forest defoliator management options: Decision for no spraying may have worse impacts on non-target Lepidoptera than Bacillus thuringiensis insecticides J. Insect Conserv. 8 241–261
F. Slansky J. M. Scriber (1985) Food consumption and utilization G. A. Kerkut L. I. Gilbert (Eds) Comprehensive Insect Physiology, Biochemistry, and Pharmacology, Vol. 4. Regulation: Digestion, Nutrition, Excretion Pergamon Press Oxford 87–163
A. Trisyono M. E. Whalon (1999) ArticleTitleToxicity of neem applied alone and in combinations with Bacillus thuringiensis to Colorado potato beetle (Coleoptera: Chrysomelidae) J. Econ. Entomol. 92 1281–1288 Occurrence Handle1:CAS:528:DC%2BD3cXhsVCksQ%3D%3D
M. E. Whalon J. M. Wierenga (1994) ArticleTitleBacillus thuringiensis resistant Colorado potato beetle and transgenic plants: Some operational and ecological implications for deployment Biocontrol Sci. Technol. 4 555–561
M. E. Whalon B. A. Wingerd (2003) ArticleTitleBt: Mode of action and use Arch. Insect Biochem. Physiol. 54 200–211 Occurrence Handle10.1002/arch.10117 Occurrence Handle1:CAS:528:DC%2BD3sXps1ers7c%3D Occurrence Handle14635181
T. Yamamoto (2001) ArticleTitleOne hundred years of Bacillus thuringiensis research and development: Discovery to transgenic crops J. Insect Biotechnol. Sericol. 70 1–23 Occurrence Handle1:CAS:528:DC%2BD3MXkt1Oju78%3D
I. A. Zalunin L. P. Revina L. I. Kostina G. G. Chestukhina (2004) ArticleTitlePeculiarities of Cry proteins to be taken into account during their in vivo and in vitro study IOBS/WPRS Bull. 27 177–185
Acknowledgments
Thanks are extended to Dr. P. Dědiě of the Potato Research Institute, Havlíčkův Brod, and Dr. S. Rakouský of the University of South Bohemia, České Budějovice, for the in vitro cultures of potatoes. Statistical evaluations were carried out with the kind help of Dr. O. Nedvěd of the University of South Bohemia. The research was performed under the auspices of Institute Research Program Z50070508 and supported by grant 522/02/1507 from the Grant Agency of the Czech Republic.
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Hussein, H.M., Habuštová, O., Turanli, F. et al. Potato Expressing Beetle-Specific Bacillus thuringiensis Cry3Aa Toxin Reduces Performance of a Moth. J Chem Ecol 32, 1–13 (2006). https://doi.org/10.1007/s10886-006-9347-x
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DOI: https://doi.org/10.1007/s10886-006-9347-x


