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Effects of Chinese honeybee foraging on oilseed rape gene flow and honey ingredients

  • F. X. LIU (a1) (a2), C. P. BU (a1) (a2), T. TANG (a1) (a2), G. M. CHEN (a1) (a2), S. K. GU (a1) (a2) (a3), Y. N. WANG (a1) (a2) (a3) and X. X. ZHAO (a1) (a2)...


Honeybee foraging can transfer exogenous genes from genetically modified (GM) oilseed rape (Brassica napus L.) to closely related plants, which not only induces potential ecological risks but also contaminates non-GM seeds or honey products with GM ingredients. These events may lead to international trade disputes. Chinese honeybees (Apis cerana cerana Fabricius) and a herbicide (glufosinate)-resistant GM strain of B. napus (Z7B10) were studied to examine the effects of honeybee short-range foraging on oilseed rape gene flow and honey ingredients. Results showed variable frequencies of gene flow between GM and non-GM oilseed rape cultivars, with the highest frequency under nylon net isolation with artificially stocked honeybees, the lowest frequency under nylon net isolation alone, and an intermediate frequency under natural pollination, suggesting the important role of honeybee foraging in gene flow frequency. Additionally, GM pollen grains were found in honey collected from honeybees foraging on both GM and non-GM oilseed rape cultivars. The phosphinothricin acetyltransferase protein was also detected in both unbroken pollen-containing and pollen-free honey by protein testing strips, suggesting that honeybee foraging on GM oilseed rape could lead to contamination with GM ingredients. Overall, the results provide a direct scientific basis for the ecological risk assessment and safety management of GM oilseed rape.


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Abrol, D. P. (2011). Genetically modified plants and bees. In Pollination Biology: Biodiversity Conservation and Agricultural Production (Ed. Abrol, D. P.), pp. 669708. Dordrecht, The Netherlands: Springer Science & Business Media.
Bo, C. P., Shi, B. G., Xu, J. M., Hu, C. X. & Zhao, X. X. (2012). Primary list of flower-visiting insects in Huaian rape fields. Journal of Anhui Agricultural Sciences 40, 1209212093.
Chen, M. L., Zhao, Z. J. & Xi, G. P. (2014). Positive analysis of Chinese honeybee industry and economic perspective. Acta Agriculturae Zhejiangensis 26, 825829.
Cheng, H., Jin, W., Wu, H., Wang, F., You, C., Peng, Y. & Jia, S. (2007). Isolation and PCR detection of foreign DNA sequences in bee honey raised on genetically modified Bt (Cry 1 Ac) cotton. Food and Bioproducts Processing 85, 141145.
Chevre, A. M., Eber, F., Baranger, A. & Renard, M. (1997). Gene flow from transgenic crops. Nature 389, 924.
Cresswell, J. E. (1994). A method for quantifying the gene flow that results from a single bumblebee visit using transgenic oilseed rape, Brassica napus L. cv. Westar. Transgenic Research 3, 134137.
Cresswell, J. E., Osborne, J. L. & Bell, S. A. (2002). A model of pollinator-mediated gene flow between plant populations with numerical solutions for bumblebees pollinating oilseed rape. Oikos 98, 375384.
Cresswell, J. E. & Osborne, J. L. (2004). The effect of patch size and separation on bumblebee foraging in oilseed rape: implications for gene flow. Journal of Applied Ecology 41, 539546.
Damgaard, C. & Kjellsson, G. (2005). Gene flow of oilseed rape (Brassica napus) according to isolation distance and buffer zone. Agriculture, Ecosystems & Environment 108, 291301.
Durán, X. A., Ulloa, R. B., Carrillo, J. A., Contreras, J. L. & Bastidas, M. T. (2010). Evaluation of yield component traits of honeybee pollinated (Apis mellifera L.) rapeseed canola (Brassica napus L.). Chilean Journal of Agricultural Research 70, 309314.
Enkegaard, A., Kryger, P. & Boelt, B. (2016). Determinants of nectar production in oilseed rape. Journal of Apicultural Research 55, 8999.
Gauld, I. & Bolton, B. (1989). The Hymenoptera. Oxford: Oxford University Press.
Gilbert, N. (2013). A hard look at GM crops. Nature 497, 2426.
Hagler, J. R., Mueller, S., Teuber, L. R., Machtley, S. A. & Van Deynze, A. (2011). Foraging range of honey bees, Apis mellifera, in alfalfa seed production fields. Journal of Insect Science 11, 144. doi: 10.1673/031.011.14401.
Hayter, K. E. & Cresswell, J. E. (2003). An experimental evaluation of the relative importance of pollination by insects vs. wind in oilseed rape (Brassica napus). In Proceedings of the 1st European Conference on the Co-existence of Genetically Modified Crops with Conventional and Organic Crops (Ed. Boelt, B.), p. 214. Slagelse, Denmark: Danish Institute of Agricultural Sciences.
Hoyle, M., Hayter, K. & Cresswell, J. E. (2007). Effect of pollinator abundance on self-fertilization and gene flow: application to GM canola. Ecological Applications 17, 21232135.
Hoyle, M. & Cresswell, J. E. (2007). The effect of wind direction on cross-pollination in wind-pollination GM crops. Ecological Applications 17, 12341243.
Hüsken, A. & Dietz-Pfeilstetter, A. (2007). Pollen-mediated intraspecific gene flow from herbicide resistant oilseed rape (Brassica napus L.). Transgenic Research 16, 557569.
Ji, T. (2009). Research of genetic diversity among Apis cerana in China. Ph.D. Thesis, Yangzhou University, Yangzhou, China.
Klein, A. M., Vaissiere, B. E., Cane, J. H., Steffan-Dewenter, I., Cunningham, S. A., Kremen, C. & Tscharntke, T. (2007). Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society B: Biological Sciences 274, 303313.
Li, J., Zhu, C. D., Wang, F. H., Huang, D. Y., Zhang, Y. Z., Ding, L. & Huang, H. R. (2007). Current research on the status of wild bees and their pollination roles. Biodiversity Science 15, 687692.
Malone, L. A. & Pham-Delègue, M. H. (2001). Effects of transgene products on honey bees (Apis mellifera) and bumblebees (Bombus sp.). Apidologie 32, 287304.
Malone, L. A. (2002). Literature Review on Genetically Modified Plants and Bee Products. MAFF Technical Paper no. 2002/05. Palmerston North, New Zealand: HortResearch.
Mikkelsen, T. R., Andersen, B. & Jorgensen, R. B. (1996). The risk of crop transgene spread. Nature 380, 31. doi: 10.1038/380031a0.
MOA. (2002). Regulation No. 8 of the Ministry of Agriculture Concerning the Implementation Regulations on Safety Assessment of Agricultural GMOs of China. Beijing, China: Ministry of Agriculture.
Morse, R. A. & Calderone, N. W. (2000). The value of honey bees as pollinators of U.S. crops in 2000. Bee Culture 128, 115.
Murphy, D. J. (1996). Engineering oil production in rapeseed and other oil crops. Trends in Biotechnology 14, 206213.
Pasquet, R. S., Peltier, A., Hufford, M. B., Oudin, E., Saulnier, J., Paul, L., Knudsen, J. T., Herren, H. R. & Gepts, P. (2008). Long-distance pollen flow assessment through evaluation of pollinator foraging range suggests transgene escape distances. Proceedings of the National Academy of Sciences of the USA 105, 1345613461.
Ramsay, G., Thompson, C., Neilson, S. & Mackay, G. R. (1999). Honeybees as vectors of GM oilseed rape pollen. In Gene Flow and Agriculture: Relevance for Transgenic Crops. BCPC Symposium Proceedings No 72 (Ed. Lutman, P. J. W.), pp. 209214. Farnham, UK: British Crop Protection Council.
Ramsay, G., Thompson, C. & Squire, G. (2003). Quantifying Landscape-Scale Gene Flow in Oilseed Rape. Final Report of DEFRA Project RG0216: An Experimental and Mathematical Study of the Local and Regional Scale Movement of an Oilseed Rape Transgene. London, UK: DEFRA.
Rieger, M. A., Lamond, M., Preston, C., Powles, S. B. & Roush, R. T. (2002). Pollen-mediated movement of herbicide resistance between commercial canola fields. Science 296, 23862388.
Shi, Y. Y., Guan, C., Zeng, Z. J., An, J. D. & Luo, S. D. (2009). Yield-increasing effect and mechanism of honeybee on rape pollination. Acta Agriculturae Universitatis Jiangxiensis 31, 994999.
Steffan-Dewenter, I. (2003). Seed set of male-sterile and male-fertile oilseed rape (Brassica napus) in relation to pollinator density. Apidologie 34, 227235.
Thompson, C. E., Squire, G., Mackay, G. R., Bradshaw, J. E., Crawford, J. & Ramsay, G. (1999). Regional patterns of gene flow and its consequences for GM oilseed rape. In Gene Flow and Agriculture: Relevance for Transgenic Crops (Ed. Lutman, P. J. W.), pp. 95100. Farnham, UK: British Crop Protection Council.
Timmons, A. M., O'Brien, E. T., Charters, Y. M., Dubbels, S. J. & Wilkinson, M. J. (1995). Assessing the risks of wind pollination from fields of genetically modified Brassica napus ssp oleifera. Euphytica 85, 417423.
Wang, H. Z. (2010). Review and future development of rapeseed industry in China. Chinese Journal of Oil Crop Sciences 32, 300302.
Williams, I. H., Martin, A. P. & White, R. P. (1986). The pollination requirements of oil-seed rape (Brassica napus L.). Journal of Agricultural Science, Cambridge 106, 2730.
Wu, G., Zhang, L., Wu, Y. H., Cao, Y. L. & Lu, C. M. (2010). Comparison of five endogenous reference genes for specific PCR detection and quantification of Brassica napus . Journal of Agricultural and Food Chemistry 58, 28122817.
Xiao, L. (2009). Studies on Bar-transgenic herbicide-resistant winter oilseed rape and its gene flow. Ph.D. Thesis, Nanjing Agricultural University, Nanjing, China.
Yan, Z. L. (2015). Query and discussion on ‘ripe honey’. Journal of Bee 35, 1214.
Zhao, X. X., Lu, W. P., Qi, C. K., Pu, H. M., Xia, Q. X., Lu, D. L., Liu, G. S. & Wang, Y. P. (2005). Assessment on alien herbicide-resistant gene flow among crucifers by sexual compatibility. Chinese Science Bulletin 50, 16051612.
Zhao, X. X., Xia, Q. X., Lu, D. L., Lu, W. P., Qi, C. K., Pu, H. M., Liu, G. S., Zhao, J. & Wang, Y. P. (2006). Gene flow from genetically modified herbicide-resistant rapeseed to cruciferous weeds. Progress in Natural Science 16, 936941.
Zhao, X. X., Tang, T., Chen, G. M., Liu, F. X., Wang, X. L., Bu, C. P. & Lu, C. M. (2013). Rationalizing the isolation distance needed for field trials involving genetically modified rapeseed (Brassica napus L.) in China. Chinese Science Bulletin 58, 15581567.

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Effects of Chinese honeybee foraging on oilseed rape gene flow and honey ingredients

  • F. X. LIU (a1) (a2), C. P. BU (a1) (a2), T. TANG (a1) (a2), G. M. CHEN (a1) (a2), S. K. GU (a1) (a2) (a3), Y. N. WANG (a1) (a2) (a3) and X. X. ZHAO (a1) (a2)...


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