Biosafety risk assessment approaches for insect-resistant genetically modified crops

Inaam Ullah, Muhammad Asif, Mazhar Hussain Ranjha, Romana Iftikhar, Midrar Ullah, Nasir Mehmood Khan, Muhammad Ashfaq

Abstract


Background: Environmental risk assessment (ERA) is imperative for commercial release of insect resistant, genetically modified crops (IR-GMCs).An insect specific, spider venom peptideω-HXTX-Hv1a (Hvt) was successfully expressed in cotton plants. The cotton plants producing Hvt protein have demonstrated resistance against economically important insect pest species. The study was performed to assess the effects of Hvt producing cotton plants on Honey bees (Apis mellifera).

Methods: Three approaches were used to evaluate the effects of Hvt protein on adults of honeybees; whole plant assays in flight cages, in vitro assays with pollen of Hvt-cotton, and assays with elevated levels of purified Hvt protein. Pollens of Bt cotton or purified Bt proteins were used as control.

Results: The field experiments did not yield any meaningful data due to high rate of mortality in all treatments including the control. However, the laboratory experiments provided conclusive results in which Hvt, purified or in pollens, did not affect the survival or longevity of the bees compared to the control. During the course of study we were able to compare the quality, effectiveness and economics of different experiments.

Conclusions: We conclude that Hvt either purified or produced in cotton plants do not affect the survival or longevity of honey bees. We are also of the view that starting at laboratory level assays not only gives meaningful data but also saves a lot of time and money that can be spent on other important questions regarding safety of a particular transgenic crop. Hence, a purpose-based, tiered approach could be the best choice for pre-release ERA of IR-GMCs. 


Full Text:

PDF

References


Ferry N, Edwards MG, Gatehouse J, Capell T, Christou PAMR, et al. Transgenic plants for insect pest control: a forward looking scientific perspective. Transgenic Research, (2006); 15(1): 13-19.

James C. 20th Anniversary (1996 to 2015) of the Global Commercialization of Biotech Crops and Biotech Crop Highlights in 2015. ISAAA Brief, (2015); (51).

Thubru D, Firake D, Behere G. Assessing risks of pesticides targeting lepidopteran pests in cruciferous ecosystems to eggs parasitoid, Trichogramma brassicae (Bezdenko). Saudi Journal of Biological Sciences, (2016).

Ronlels J, Meissle M, Raybould A (2009) Ground Non-target Arthropods. Environmental impact of genetically modified crops. Wallingford: CABI. pp. 165.

Shahid AA, Bano S, Khalid S, Samiullah TR, Bajwa KS, et al. Biosafety assessment of transgenic Bt cotton on model animals. Advancements in Life Sciences, (2016); 3(3): 97-108.

Tabashnik BE, Brévault T, Carrière Y. Insect resistance to Bt crops: lessons from the first billion acres. Nature Biotechnology, (2013); 31(6): 510-521.

Nair R, Kamath SP, Mohan KS, Head G, Sumerford DV. Inheritance of field‐relevant resistance to the Bacillus thuringiensis protein Cry1Ac in Pectinophora gossypiella (Lepidoptera: Gelechiidae) collected from India. Pest Management Science, (2016); 72(3): 558-565.

Khan SA, Zafar Y, Briddon RW, Malik KA, Mukhtar Z. Spider venom toxin protects plants from insect attack. Transgenic Research, (2006); 15(3): 349-357.

Ullah I, Hagenbucher S, Álvarez‐Alfageme F, Ashfaq M, Romeis J. Target and non‐target effects of a spider venom toxin produced in transgenic cotton and tobacco plants. Journal of Applied Entomology, (2015); 139321–332.

Fletcher JI, Smith R, O'Donoghue SI, Nilges M, Connor M, et al. The structure of a novel insecticidal neurotoxin, ω-atracotoxin-HV1, from the venom of an Australian funnel web spider. Nature Structural Biology, (1997); 4(7): 559-566.

Mukherjee AK, Sollod BL, Wikel SK, King GF. Orally active acaricidal peptide toxins from spider venom. Toxicon, (2006); 47(2): 182-187.

Smith JJ, Herzig V, King GF, Alewood PF. The insecticidal potential of venom peptides. Cellular and Molecular Life Sciences, (2013); 70(19): 3665-3693.

Pal N, Yamamoto T, King GF, Waine C, Bonning B. Aphicidal efficacy of scorpion and spider derived neurotoxins. Toxicon, (2013); 70; 114-122.

King GF, Hardy MC. Spider-Venom Peptides for Control of Insect Pests. Annual Review of Entomology, (2013); 58(1): 475–496.

Windley MJ, Herzig V, Dziemborowicz SA, Hardy MC, King GF, et al. Spider-venom peptides as bioinsecticides. Toxins, (2012); 4(3): 191-227.

Romeis J, Bartsch D, Bigler F, Candolfi MP, Gielkens MMC, et al. Assessment of risk of insect-resistant transgenic crops to non-target arthropods. Nature Biotechnology, (2008); 26(2): 203-208.

Sanvido O, Romeis J, Bigler F (2007) Ecological impacts of genetically modified crops: ten years of field research and commercial cultivation. Green Gene Technology. pp. 235-278.

Dutton A, Romeis J, Bigler F. Assessing the risks of insect resistant transgenic plants on entomophagous arthropods Bt-maize expressing Cry1Ab as a case study. BioControl, (2003); 48(6): 611-636.

Caro TM, O'Doherty G. On the use of surrogate species in conservation biology. Conservation Biology, (1999); 13(4): 805-814.

Partap U (2011) The pollination role of honeybees. Honeybees of Asia: Springer. pp. 227-255.

Liu B, Xu CR, Yan F, Gong R. The impacts of the pollen of insect-resistant transgenic cotton on honey bees. Biodiversity and Conservation, (2005); 14(14): 3487-3496.

Decourtye A, Devillers J, Cluzeau S, Charreton M, Pham-Delègue M-H. Effects of imidacloprid and deltamethrin on associative learning in honeybees under semi-field and laboratory conditions. Ecotoxicology and Environmental Safety, (2004); 57(3): 410-419.

Ullah I, Asif M, Arslan M, Ashfaq M. Temporal expression of Cry1Ab/c protein in Bt-cotton varieties, their efficacy against Helicoverpa armigera (Lepidoptera: Noctuidae) and population dynamics of sucking arthropods on them. International Journal of Agriculture and Biology, (2014); 16(5): 579-585.

Yang L, Pan A, Zhang K, Yin C, Qian B, et al. Qualitative and quantitative PCR methods for event-specific detection of genetically modified cotton Mon1445 and Mon531. Transgenic research, (2005); 14(6): 817-831.

Gray A. Problem formulation in environmental risk assessment for genetically modified crops: a practitioner’s approach. Collection of Biosafety Reviews, (2012); 610-65.

Romeis J, Hellmich RL, Candolfi MP, Carstens K, De Schrijver A, et al. Recommendations for the design of laboratory studies on non-target arthropods for risk assessment of genetically engineered plants. Transgenic Research, (2011); 20(1): 1-22.

Garcia-Alonso M, Jacobs E, Raybould A, Nickson TE, Sowig P, et al. A tiered system for assessing the risk of genetically modified plants to non-target organisms. Environmental Biosafety Research, (2006); 5(2): 57-65.

Raybould A. Ecological versus ecotoxicological methods for assessing the environmental risks of transgenic crops. Plant Science, (2007); 173(6): 589-602.

Kranthi KR, Naidu S, Dhawad CS, Tatwawadi A, Mate K, et al. Temporal and intra-plant variability of Cry1Ac expression in Bt-cotton and its influence on the survival of the cotton bollworm, Helicoverpa armigera (Hubner) (Noctuidae: Lepidoptera). Current Science, (2005); 89(2): 291.

Adamczyk JJ, Adams LC, Hardee DD, Dugger P, Richter D. Quantification of Cry1A (c) δ-endotoxin in transgenic Bt cotton: correlating insect survival to different protein levels among plant parts and varieties; 2000 4-8 January; San Antonio, USA. National Cotton Council. pp. 929-932.

Hendriksma HP, Küting M, Härtel S, Näther A, Dohrmann AB, et al. Effect of stacked insecticidal Cry proteins from maize pollen on nurse bees (Apis mellifera carnica) and their gut bacteria. PloS One, (2013); 8(3).

Li Y, Zhang X, Chen X, Romeis J, Yin X, et al. Consumption of Bt rice pollen containing Cry1C or Cry2A does not pose a risk to Propylea japonica (Thunberg)(Coleoptera: Coccinellidae). Scientific Reports, (2015); 5: 7679.

Li Y, Meissle M, Romeis J. Consumption of Bt maize pollen expressing Cry1Ab or Cry3Bb1 does not harm adult green lacewings, Chrysoperla carnea (Neuroptera: Chrysopidae). PloS One, (2008); 3(8): e2909.

Huang ZY, Hanley AV, Pett WL, Langenberger M, Duan JJ. Field and semifield evaluation of impacts of transgenic canola pollen on survival and development of worker honey bees. Journal of Economic Entomology, (2004); 97(5): 1517-1523.

Dai PL, Zhou W, Zhang J, Cui HJ, Wang Q, et al. Field assessment of Bt cry1Ah corn pollen on the survival, development and behavior of Apis mellifera ligustica. Ecotoxicology and Environmental Safety, (2012); 79: 232-237.

Han P, Niu CY, Biondi A, Desneux N. Does transgenic Cry1Ac+ CpTI cotton pollen affect hypopharyngeal gland development and midgut proteolytic enzyme activity in the honey bee Apis mellifera L.(Hymenoptera, Apidae)? Ecotoxicology, (2012); 21(8): 2214-2221.

Adamczyk JJ, Meredith WR. Genetic basis for variability of Cry1Ac expression among commercial transgenic Bacillus thuringiensis (Bt) cotton cultivars in the United States. Journal of Cotton Science, (2004); 817-23.

Adamczyk JJ, Sumerford DV. Potential factors impacting season-long expression of Cry1Ac in 13 commercial varieties of Bollgard® cotton. Journal of Insect Science (Tucson), (2001); 1(13): 1-6.

Dong HZ, Li WJ. Variability of endotoxin expression in Bt transgenic cotton. Journal of Agronomy and Crop Science, (2007); 193(1): 21-29.

Standifer L. Honey bee nutrition and supplemental feeding. Beekeeping in the United States Agriculture Handbook, (1980); 335: 39-45.

Somerville D. Honey bee nutrition and supplementary feeding. Agnote DAI/178 NSW Agriculture, (2000); 1034-6848.

Nakasu EYT, Williamson SM, M ME, Elaine FM, John GA, et al. Novel biopesticide based on a spider venom peptide shows no adverse effects on honeybees. Proceedings of the Royal Society of London Series B: Biological Sciences, (2014); 281: 20140619.

Dai P-L, Zhou W, Zhang J, Jiang W-Y, Wang Q, et al. The effects of Bt Cry1Ah toxin on worker honeybees (Apis mellifera ligustica and Apis cerana cerana). Apidologie, (2012); 43(4): 384-391.

Ramirez-Romero R, Chaufaux J, Pham-Delegue M. Effects of Cry1Ab protoxin, deltamethrin and imidacloprid on the foraging activity and the learning performances of the honeybee Apis mellifera, a comparative approach. Apidologie, (2005); 36(4): 601.

Hanley AV, Huang ZY, Pett WL. Effects of dietary transgenic Bt corn pollen on larvae of Apis mellifera and Galleria mellonella. Journal of Apicultural Research, (2003); 42(4): 77-81.

Alvarez-Alfageme F, Bigler F, Romeis J. Laboratory toxicity studies demonstrate no adverse effects of Cry1Ab and Cry3Bb1 to larvae of Adalia bipunctata (Coleoptera: Coccinellidae): the importance of study design. Transgenic Research, (2011); 20(3): 467-479.




DOI: http://dx.doi.org/10.62940/als.v4i2.269

Refbacks

  • There are currently no refbacks.