Stacked Bt maize and arthropod predators: exposure to insecticidal Cry proteins and potential hazards
Jazyk angličtina Země Velká Británie, Anglie Médium print
Typ dokumentu časopisecké články
PubMed
28724730
PubMed Central
PMC5543214
DOI
10.1098/rspb.2017.0440
PII: rspb.2017.0440
Knihovny.cz E-zdroje
- Klíčová slova
- Bt maize, Cry proteins, arthropod foodweb, environmental risk assessment, genetically modified crops, natural enemies,
- MeSH
- Bacillus thuringiensis MeSH
- bakteriální proteiny genetika MeSH
- členovci * MeSH
- endotoxiny genetika MeSH
- geneticky modifikované rostliny genetika MeSH
- hemolyziny genetika MeSH
- kukuřice setá genetika MeSH
- larva MeSH
- potravní řetězec * MeSH
- toxiny Bacillus thuringensis MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- bakteriální proteiny MeSH
- endotoxiny MeSH
- hemolyziny MeSH
- insecticidal crystal protein, Bacillus Thuringiensis MeSH Prohlížeč
- toxiny Bacillus thuringensis MeSH
Genetically engineered (GE) crops with stacked insecticidal traits expose arthropods to multiple Cry proteins from Bacillus thuringiensis (Bt). One concern is that the different Cry proteins may interact and lead to unexpected adverse effects on non-target species. Bi- and tri-trophic experiments with SmartStax maize, herbivorous spider mites (Tetranychus urticae), aphids (Rhopalosiphum padi), predatory spiders (Phylloneta impressa), ladybeetles (Harmonia axyridis) and lacewings (Chrysoperla carnea) were conducted. Cry1A.105, Cry1F, Cry3Bb1 and Cry34Ab1 moved in a similar pattern through the arthropod food chain. By contrast, Cry2Ab2 had highest concentrations in maize leaves, but lowest in pollen, and lowest acquisition rates by herbivores and predators. While spider mites contained Cry protein concentrations exceeding the values in leaves (except Cry2Ab2), aphids contained only traces of some Cry protein. Predators contained lower concentrations than their food. Among the different predators, ladybeetle larvae showed higher concentrations than lacewing larvae and juvenile spiders. Acute effects of SmartStax maize on predator survival, development and weight were not observed. The study thus provides evidence that the different Cry proteins do not interact in a way that poses a risk to the investigated non-target species under controlled laboratory conditions.
Faculty of Science University of South Bohemia Branišovská 31 České Budějovice 37005 Czech Republic
Institute of Ecology and Evolution University of Bern Baltzerstrasse 6 Bern 3012 Switzerland
Institute of Entomology Biology Centre CAS Branišovská 31 České Budějovice 37005 Czech Republic
Zobrazit více v PubMed
Romeis J, Meissle M, Bigler F. 2006. Transgenic crops expressing Bacillus thuringiensis toxins and biological control. Nat. Biotechnol. 24, 63–71. (10.1038/nbt1180) PubMed DOI
Sanvido O, Romeis J, Gathmann A, Gielkens M, Raybould A, Bigler F. 2012. Evaluating environmental risks of genetically modified crops—ecological harm criteria for regulatory decision-making. Environ. Sci. Policy 15, 82–91. (10.1016/j.envsci.2011.08.006) DOI
Romeis J, et al. 2008. Assessment of risk of insect-resistant transgenic crops to nontarget arthropods. Nat. Biotechnol. 26, 203–208. (10.1038/nbt1381) PubMed DOI
Wolfenbarger LL, Naranjo SE, Lundgren JG, Bitzer RJ, Watrud LS. 2008. Bt crop effects on functional guilds of non-target arthropods: a meta-analysis. PLoS ONE 3, e2118 (10.1371/journal.pone.0002118) PubMed DOI PMC
Naranjo SE. 2009. Impacts of Bt crops on non-target invertebrates and insecticide use patterns. CAB Rev.: Perspect. Agric., Vet. Sci., Nutrit. Nat. Resour. 4, 11 (10.1079/PAVSNNR20094011) DOI
Comas C, Lumbierres B, Pons X, Albajes R. 2014. No effects of Bacillus thuringiensis maize on nontarget organisms in the field in southern Europe: a meta-analysis of 26 arthropod taxa. Transgenic Res. 23, 135–143. (10.1007/s11248-013-9737-0) PubMed DOI
Torres JB, Ruberson JR, Adang MJ. 2006. Expression of Bacillus thuringiensis Cry1Ac protein in cotton plants, acquisition by pests and predators: a tritrophic analysis. Agric. Forest Entomol. 8, 191–202. (10.1111/j.1461-9563.2006.00298.x) DOI
Romeis J, Meissle M, Raybould A, Hellmich RL. 2009. Impact of insect-resistant transgenic crops on above-ground non-target arthropods. In Environmental impact of genetically modified crops (eds Ferry N, Gatehouse AMR), pp. 165–198. Wallingford, UK: CAB International.
Meissle M, Romeis J. 2012. No accumulation of Bt protein in Phylloneta impressa (Araneae: Theridiidae) and prey arthropods in Bt maize. Environ. Entomol. 41, 1037–1042. (10.1603/EN11321) DOI
Harwood JD, Wallin WG, Obrycki JJ. 2005. Uptake of Bt endotoxins by nontarget herbivores and higher order arthropod predators: molecular evidence from a transgenic corn agroecosystem. Mol. Ecol. 14, 2815–2823. (10.1111/j.1365-294X.2005.02611.x) PubMed DOI
Obrist LB, Dutton A, Albajes R, Bigler F. 2006. Exposure of arthropod predators to Cry1Ab toxin in Bt maize fields. Ecol. Entomol. 31, 143–154. (10.1111/j.0307-6946.2006.00762.x) DOI
Meissle M, Romeis J. 2009. The web-building spider Theridion impressum (Araneae: Theridiidae) is not adversely affected by Bt maize resistant to corn rootworms. Plant Biotechnol. J. 7, 645–656. (10.1111/j.1467-7652.2009.00431.x) DOI
Yu H, Romeis J, Li Y, Li X, Wu K. 2014. Acquisition of Cry1Ac protein by non-target arthropods in Bt soybean fields. PLoS ONE 9, e103973 (10.1371/journal.pone.0103973) PubMed DOI PMC
Li Y, et al. 2017. Bt rice in China—focusing the non-target risk assessment. Plant Biotechnol. J. (10.1111/pbi.12720) PubMed DOI PMC
Que Q, Chilton MDM, de Fontes CM, He C, Nuccio M, Zhu T, Wu Y, Chen JS, Shi L. 2010. Trait stacking in transgenic crops: challenges and opportunities. GM Crops 1, 220–229. (10.4161/gmcr.1.4.13439) PubMed DOI
ISAAA. 2016. Global status of commercialized biotech/GM crops: 2016. ISAAA Brief No. 52 Ithaca, NY: ISAAA.
Hilbeck A, Otto M. 2015. Specificity and combinatorial effects of Bacillus thuringiensis Cry toxins in the context of GMO environmental risk assessment. Front. Environ. Sci. 3, 71 (10.3389/fenvs.2015.00071) DOI
Marra MC, Piggott NE, Goodwin BK. 2010. The anticipated value of SmartStax™ for US corn growers. AgBioForum 13, 1–12.
Head G, Carroll M, Clark T, Galvan T, Huckaba RM, Price P, Samuel L, Storer NP. 2014. Efficacy of SmartStax® insect-protected corn hybrids against corn rootworm: the value of pyramiding the Cry3Bb1 and Cry34/35Ab1 proteins. Crop Prot. 57, 38–47. (10.1016/j.cropro.2013.11.025) DOI
Meissle M, Zünd J, Walderburger M, Romeis J. 2014. Development of Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae) on pollen from Bt-transgenic and conventional maize. Sci. Rep. 4, 5900 (10.1038/srep05900) PubMed DOI PMC
Dutton A, Klein H, Romeis J, Bigler F. 2002. Uptake of Bt-toxin by herbivores feeding on transgenic maize and consequences for the predator Chrysoperla carnea. Ecol. Entomol. 27, 441–447. (10.1046/j.1365-2311.2002.00436.x) DOI
Romeis J, Dutton A, Bigler F. 2004. Bacillus thuringiensis toxin (Cry1Ab) has no direct effect on larvae of the green lacewing Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae). J. Insect Physiol. 50, 175–183. (10.1016/j.jinsphys.2003.11.004) PubMed DOI
2009. BPPD review of SmartStax plant-incorporated protectant (PIP) (Decision No: 394799; DP Barcode: 355689; Submission 830991; MRID No's 474449–01 thr 07). Washington, DC: United States Environmental Protection Agency; See https://archive.epa.gov/pesticides/chemicalsearch/chemical/foia/web/pdf/Bacillus-thuringiensisCry1A105-2009-03-13a.pdf (accessed 29 June 2017).
Álvarez-Alfageme F, Ferry N, Castañera P, Ortego F, Gatehouse AMR. 2008. Prey mediated effects of Bt maize on fitness and digestive physiology of the red spider mite predator Stethorus punctillum Weise (Coleoptera: Coccinellidae). Transgenic Res. 17, 943–954. (10.1007/s11248-008-9177-4) PubMed DOI
Álvarez-Alfageme F, Bigler F, Romeis J. 2011. Laboratory toxicity studies demonstrate no adverse effects of Cry1Ab and Cry3Bb1 to larvae of Adalia bipunctata (Coleoptera: Coccinellidae): the importance of study design. Transgenic Res. 20, 467–479. (10.1007/s11248-010-9430-5) PubMed DOI PMC
Li Y, Romeis J. 2010. Bt maize expressing Cry3Bb1 does not harm the spider mite, Tetranychus urticae, or its ladybird beetle predator, Stethorus punctillum. Biol. Control 53, 337–344. (10.1016/j.biocontrol.2009.12.003) DOI
Meissle M, Romeis J. 2017. Transfer of Cry1Ac and Cry2A proteins from genetically engineered Bt cotton to herbivores and predators. Insect Sci. (10.1111/1744-7917.12468) PubMed DOI
Torres JB, Ruberson JR. 2008. Interactions of Bacillus thuringiensis Cry1Ac toxin in genetically engineered cotton with predatory heteropterans. Transgenic Res. 17, 345–354. (10.1007/s11248-007-9109-8) PubMed DOI
Filho AB Esteves, de Oliveira JV, Torres JB, Gondim MGC Jr. 2010. Compared biology and behavior of Tetranychus urticae Koch (Acari: Tetranychidae) and Phytoseiulus macropilis (Banks) (Acari: Phytoseiidae) on BollgardTM and non-transgenic isoline cotton. Neotrop. Entomol. 39, 338–344. (10.1590/S1519-566X2010000300005) PubMed DOI
Dutton A, Obrist L, D’ Alessandro M, Diener L, Müller M, Romeis J, Bigler F. 2004. Tracking Bt-toxin in transgenic maize to assess the risks on non-target arthropods. IOBC–WPRS Bull. 27(3), 57–63.
Romeis J, Meissle M. 2011. Non-target risk assessment of Bt crops—Cry protein uptake by aphids. J. Appl. Entomol. 135, 1–6. (10.1111/j.1439-0418.2010.01546.x) DOI
Raps A, Kehr J, Gugerli P, Moar WJ, Bigler F, Hilbeck A. 2001. Immunological analysis of phloem sap of Bacillus thuringiensis corn and of the nontarget herbivore Rhopalosiphum padi (Homoptera: Aphididae) for the presence of Cry1Ab. Mol. Ecol. 10, 525–533. (10.1046/j.1365-294X.2001.01236.x) PubMed DOI
Paula DP, Andow DA. 2016. Uptake and bioaccumulation of Cry toxins by an aphidophagous predator. Environ. Poll. 209, 164–168. (10.1016/j.envpol.2015.11.036) PubMed DOI
Foelix RF. 1996. Biology of spiders, 2nd edn Oxford, NY: Oxford University Press, Georg Thieme Verlag.
Yazlovetsky IG. 2001. Features of the nutrition of Chrysopidae larvae and larval artificial diets. In Lacewings in the crop environment (eds McEwen PK, New TR, Whittington AE), pp. 320–337. Cambridge, UK: Cambridge University Press.
Koch RL. 2003. The multicolored Asian lady beetle, Harmonia axyridis: a review of its biology, uses in biological control, and non-target impacts. J. Insect Sci. 3, 32. PubMed PMC
Obrist LB, Dutton A, Romeis J, Bigler F. 2006. Biological activity of Cry1Ab toxin expressed by Bt maize following ingestion by herbivorous arthropods and exposure of the predator Chrysoperla carnea. BioControl 51, 31–48. (10.1007/s10526-005-2936-8) DOI
Meissle M, Romeis J. 2009. Insecticidal activity of Cry3Bb1 expressed in Bt maize on larvae of the Colorado potato beetle, Leptinotarsa decemlineata. Entomol. Exp. Appl. 131, 308–319. (10.1111/j.1570-7458.2009.00859.x) DOI
Wang C, Henderson G, Huang F, Gautam BK, Zhu C. 2012. Survival rate, food consumption, and tunneling of the formosan subterranean termite (Isoptera: Rhinotermitidae) feeding on Bt and non-Bt maize. Sociobiology 59, 1335–1350. (10.13102/sociobiology.v59i4.505) DOI
Hendriksma HP, Härtel S, Steffan-Dewenter I. 2011. Testing pollen of single and stacked insect-resistant Bt-maize on in vitro reared honey bee larvae. PLoS ONE 6, e28174 (10.1371/journal.pone.0028174) PubMed DOI PMC
Hendriksma HP, Küting M, Härtel S, Näther A, Dohrmann AB, Steffan-Dewenter I, Tebe CC. 2013. Effect of stacked insecticidal Cry proteins from maize pollen on nurse bees (Apis mellifera carnica) and their gut bacteria. PLoS ONE 8, e59589 (10.1371/journal.pone.0059589) PubMed DOI PMC
Schultheis E. 2011. Faunistische Umweltrisikobewertung von Bt-Mais mit multiplen Resistenzgenen und Evaluierung von Trigonotylus caelestialium (KIRKALDY) und Lumbricus terrestris LINNAEUS als Modellorganismen. PhD dissertation, RWTH Aachen University, Faculty for Mathematics, Informatics, and Natural Sciences, Germany.
Balog A, Szénási A, Szekeres D, Pálinkás Z. 2011. Analysis of soil dwelling rove beetles (Coleoptera: Staphylinidae) in cultivated maize fields containing the Bt toxins, Cry34/35Ab1 and Cry1F x Cry34/35Ab1. Biocontrol Sci. Technol. 21, 293–297. (10.1080/09583157.2010.545104) DOI
Szénási A, Pálinkás Z, Zalai M, Schmitz OJ, Balog A. 2014. Short-term effects of different genetically modified maize varieties on arthropod food web properties: an experimental field assessment. Sci. Rep. 4, 5315 (10.1038/srep05315) PubMed DOI PMC
Higgins LS, Babcock J, Neese P, Layton RJ, Moellenbeck DJ, Storer A. 2009. Three-year field monitoring of Cry1F, event DAS-Ø15Ø7–1, maize hybrids for nontarget arthropod effects. Environ. Entomol. 38, 281–292. (10.1603/022.038.0135) PubMed DOI
Svobodová Z, Habuštová O, Sehnal F, Holec M, Hussein HM. 2013. Epigeic spiders are not affected by the genetically modified maize MON 88017. J. Appl. Entomol. 137, 56–67. (10.1111/j.1439-0418.2012.01727.x) DOI
Svobodová Z, Skoková Habuštová O, Hutchison WD, Hussein HM, Sehnal F. 2015. Risk assessment of genetically engineered maize resistant to Diabrotica spp.: influence on above-ground arthropods in the Czech Republic. PLoS ONE 10, e0130656 (10.1371/journal.pone.0130656) PubMed DOI PMC
Habuštová O, Doležal P, Spitzer L, Svobodová Z, Hussein HM, Sehnal F. 2014. Impact of Cry1Ab toxin expression on the non-target insects dwelling on maize plants. J. Appl. Entomol. 138, 164–172. (10.1111/jen.12004) DOI
Romeis J, Meissle M, Naranjo SE, Li Y, Bigler F. 2014. The end of a myth—Bt (Cry1Ab) maize does not harm green lacewings. Front. Plant Sci. 5, 391 (10.3389/fpls.2014.00391) PubMed DOI PMC
Skoková Habuštová O, Svobodová Z, Spitzer L, Doležal P, Hussein HM, Sehnal F. 2015. Communities of ground-dwelling arthropods in conventional and transgenic maize: background data for the post-market environmental monitoring. J. Appl. Entomol. 139, 31–45. (10.1111/jen.12160) DOI
Svobodová Z, Shu Y, Skoková Habuštová O, Romeis J, Meissle M. 2017. Stacked Bt maize and arthropod predators: exposure to insecticidal Cry proteins and potential hazards. Dryad Digital Repository. (10.5061/dryad.51d4h) PubMed DOI PMC
Cry3Aa Toxin Is Not Suitable to Control Lepidopteran Pest Spodoptera littoralis (Boisd.)