Commercialization of transgenic rice in China: potential environmental biosafety issues

doi:10.3724/SP.J.1003.2008.08159

Abstract

Abstract:

The development and commercialization of transgenic rice with novel traits in China may offer more opportunities for promoting rice productivity. Owing to the significance of rice as a major food crop in China, the enhancement of rice production is important for national food security. If left unaddressed, the potential biosafety concerns over the extensive release and commercial cultivation of transgenic rice may hamper the development and application of this technology in rice improvement. Biosafety issues include: (1) effects of toxic transgenes on non-target organisms; (2) transgene escape to crops or wild relatives through gene flow and its potential ecological consequences; (3) interactions and influences of transgenes and transgenic plants on biodiversity, ecosystem functions, and soil microbes; and (4) the development of resistance to insect- or disease-resistant transgenes in target organisms. In order to safely and sustainably utilize transgenic biotechnology in rice, it is very important to assess biosafety consequences, including environmental risks, from transgenic rice. This paper presents a rational analysis of potential environmental biosafety problems based on the principles of risk assessment, provided that transgenic rice will be released for commercialization. We hope these analyses will provide useful information for the decision-making on commercialization of transgenic rice and serve as a framework for the assessment of relevant environmental biosafety risks.

Key words: transgenic rice, ecological risk, non-target organism, gene flow, biodiversity, soil microbe, resistance evolution

Bao-Rong Lu, Qiang Fu, Zhicheng Shen. Commercialization of transgenic rice in China: potential environmental biosafety issues[J]. Biodiv Sci, 2008, 16(5): 426-436.

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URL: https://www.biodiversity-science.net/EN/10.3724/SP.J.1003.2008.08159

https://www.biodiversity-science.net/EN/Y2008/V16/I5/426

References 73

[1]	Ammann K (2005) Effects of biotechnology on biodiversity: herbicide-tolerant and insect-resistant GM crops. Trends in Biotechnology, 23,388-394. DOI URL PMID
[2]	Andow DA, Zwahlen C (2006) Assessing environmental risks of transgenic plants. Ecology Letters, 9,196-214, 12. DOI URL PMID
[3]	Bai YY (白耀宇), Jiang MX (蒋明星), Cheng JA (程家安) (2005) Impacts of transgenic Cry1Ab rice on two collembolan species and predation of Microvelia horvathi (Hemiptera: Veliidae). Acta Entomologica Sinica (昆虫学报), 48,42-47. (in Chinese with English abstract)
[4]	Bates SL, Zhao JZ, Roush RT, Shelton AM (2005) Insect resistance management in GM crops: past, present and future. Nature Biotechnology, 23,57-62. DOI URL PMID
[5]	Cao QJ, Lu B-R, Xia H, Rong J, Sala F, Spada A, Grassi F (2006) Genetic diversity and origin of weedy rice ( Oryza sativa f. spontanea) populations found in northeastern China revealed by simple sequence repeat (SSR) markers. Annals of Botany, 98,1241-1252. DOI URL PMID
[6]	Chen LJ, Lee DS, Song ZP, Suh HS, Lu B-R (2004) Gene flow from cultivated rice ( Oryza sativa) to its weedy and wild relatives. Annals of Botany, 93,67-73. DOI URL PMID
[7]	Chen M, Zhao JZ, Ye GY, Fu Q, Shelton AM (2006a) Impact of insect-resistant transgenic rice on target insect pests and non-target arthropods in China. Insect Science, 13,409-420. DOI URL
[8]	Chen M, Ye GY, Liu ZC, Yao HW, Chen XX, Sheng ZC, Hu C, Datta SK (2006b) Field assessment of the effects of transgenic rice expressing a fused gene of CryIAb and CryIAc from Bacillus thuringiensis Berliner on non-target planthoppers and leafhoppers. Environmental Entomology, 35,127-134.
[9]	Chen WB (陈文滨), Liu FJ (刘丰静), Lin S (林胜), You MS (尤民生) (2007) Effects of insect-resistant hybrid rice on bionomical characteristics of Tetragnatha nitens. Entomological Journal of East China (华东昆虫学报), 16,13-17. (in Chinese with English abstract)
[10]	Cohen MB, Arpaia S, Lan LP, Chau LM, Snow AA (2008) Shared flowering phenology, insect pests, and pathogens among wild, weedy, and cultivated rice in the Mekong Delta, Vietnam: implications for transgenic rice. Environmental Biosafety Research, 7,73-85. DOI URL PMID
[11]	Conner AJ, Glare TR, Nap JP (2003) The release of genetically modified crops into the environment. Part II. Overview of ecological risk assessment. Plant Journal, 33,19-46.
[12]	Dale PJ, Clarke B, Fontes EMG (2002) Potential for the environmental impact of transgenic crops. Nature Biotechnology, 20,567-574. DOI URL PMID
[13]	Dalecky A, Bourguet D, Ponsard S (2007) Does the European corn borer disperse enough for a sustainable control of resistance to Bt maize via the High Dose/Refuge strategy? Cahiers Agricultures, 16,171-176.
[14]	Devare MH, Jones CM, Thies JE (2004) Effect of Cry3Bb transgenic corn and tefluthrin on the soil microbial community: biomass, activity and diversity. Journal of Environmental Quality, 33,837-843. DOI URL PMID
[15]	Ellstrand NC (2003) Current knowledge of gene flow in plants: implications for transgene flow. Philosophical Transactions of the Royal Society B: Biological Sciences, 358,1163-1170.
[16]	Fu Q (傅强), Wang F (王锋), Li DH (李冬虎), Yao Q (姚青), Lai FX (赖凤香), Zhang ZT (张志涛) (2003) Effects of insect-resistant transgenic rice lines MSA and MSB on non-target pests Nilaparvata lugens and Sogatella fucifera. Acta Entomologica Sinica(昆虫学报), 46,697-704. (in Chinese with English abstract)
[17]	Giovannetti M, Sbrana C, Turrini A (2005) The impact of genetically modified crops on soil microbial communities. Rivista di Biologia/Biology Forum, 98,393-417. URL PMID
[18]	Heinemann JA (2007) A typology of the effects of (trans)gene flow on the conservation and sustainable use of genetic resources. http://www.fao.org/ag/cgrfa/cgrfa11.htm.
[19]	Huang JK, Hu R, Rozelle R, Pray C (2005) Insect-resistance GM rice in farmers’ fields: assessing productivity and health effects in China. Science, 308,688-690. DOI URL PMID
[20]	James C (2007) Global Status of Commercialized Biotech/GM Crops: 2007. ISAAA Brief No.37, International Service for the Acquisition of Agri-Biotech Applications, Ithaca NY, USA .
[21]	Jia SR, Wang F, Shi L, Yuan QH, Liu WG, Liao YL, Li SG, Jin WJ, Peng HP (2007) Transgene flow to hybrid rice and its male-sterile lines. Transgenic Research, 16,491-501. DOI URL PMID
[22]	Jiang YH (姜永厚), Fu Q (傅强), Cheng JA (程家安), Ye GY (叶恭银), Bai YY (白耀羽), Zhang ZT (张志涛) (2004) Effects of transgenic Bt rice on the biological characteristics of Apanteles chilonis (Munakata)(Hymenoptera: Braconidae). Acta Entomologica Sinica (昆虫学报), 47,124-129. (in Chinese with English abstract)
[23]	Jiang YH (姜永厚), Fu Q (傅强), Cheng JA (程家安), Zhu ZR (祝增荣), Jiang MX (蒋明星), Zhang ZT (张志涛) (2005) Effect of transgenic Sck+Cry1Ac rice on the survival and growth of Chilo suppressalis (Walker) (Lepidoptera: Pyralidae) and its parasitoid Apanteles chilonis (Munakata)(Hymenoptera: Braconidae). Acta Entomologica Sinica (昆虫学报), 48,554-560. (in Chinese with English abstract)
[24]	Kuk YI, Burgos NR, Shivrain VK (2008) Natural tolerance to imazethapyr in red rice (Oryza sativa). Weed Science, 56,1-11.
[25]	Li GP, Wu KM, Gould F, Wang JK, Miao J, Gao XW, Guo YY (2007) Increasing tolerance to Cry1Ac cotton from cotton bollworm,Helicoverpa armigera, was confirmed in Bt cotton farming area of China. Ecological Entomology, 32,366-375.
[26]	Lin CY, Xu XL, Zhao T, Cheng JA, Tu JM, Ye GY, Shen ZC (2008) A built-in strategy for containment of transgenic plants: creation of selectively terminable transgenic rice. PLoS ONE, 3,e1818. DOI URL PMID
[27]	Liu HC (刘洪春), Liu YW (刘耀武), Fu GY (付桂月), Guo FY (郭福英), Wei LJ (魏丽君), Wang ZM (王振梅), Tao FM (陶凤梅) (2005) New characters of pests and diseases in Bt transgenic cotton and controlling measures in Linqing County, Shandong. China Cotton (中国棉花), 32(5),25. (in Chinese)
[28]	Liu ZC (刘志诚), Ye GY (叶恭银), Hu C (胡萃), Datta SK (2002) Effects of Bt transgenic rice on population dynamics of main non-target insect pests and dominant spider species in rice paddies. Acta Phytophylacica Sinica (植物保护学报), 29,138-144. (in Chinese with English abstract)
[29]	Liu ZC (刘志诚), Ye GY (叶恭银), Hu C (胡萃), Datta SK (2003a) Impact of transgenic indica rice with a fused gene of Cry1Ab/Cry1Ac on the rice paddy arthropod community. Acta Entomologica Sinica(昆虫学报), 46,454-465. (in Chinese with English abstract)
[30]	Liu ZC (刘志诚), Ye GY (叶恭银), Fu Q (傅强), Zhang ZT (张志涛), Hu C (胡萃) (2003b) Indirect impact assessment of transgenic rice with Cry1Ab gene on predations by the wolf spider, Pirata subpiraticus. Chinese Journal of Rice Science (中国水稻科学), 17(2),175-178. (in Chinese with English abstract)
[31]	Liu ZC (刘志诚), Ye GY (叶恭银), Hu C (胡萃) (2004) Effects of Bacillus thuringiensis transgenic rice and chemical insecticides on arthropod communities in paddy-fields. Chinese Journal of Applied Ecology (应用生态学报), 15,2309-2314. (in Chinese with English abstract)
[32]	Liu YF (刘雨芳), Su J (苏军), You MS (尤民生), Wang Q (汪琼), Hu SQ (胡斯琴), Liu WH (刘文海), Zhao SX (赵士熙), Wang F (王锋) (2005) Effect of transgenic pest-resistant rice on pest insect communities in paddy fields. Acta Entomologica Sinica (昆虫学报), 48,544-553. (in Chinese with English abstract)
[33]	Liu YF (刘雨芳), He L (贺玲), Wang Q (汪琼), Hu SQ (胡斯琴), Liu WH (刘文海), Chen KG (陈康贵), You MS (尤民生) (2006) Evaluation of the effects of insect-resistant Cry1Ac/Sck transgenic rice on the parasitoid communities in paddy fields. Acta Entomologica Sinica (昆虫学报), 49,955-962. (in Chinese with English abstract)
[34]	Lu B-R (2006) Identifying possible environmental hazard from GM rice in China to inform biosafety assessment. In:Proceedings of the 9th International Symposium on the Biosafety of Genetically Modified Organisms, pp.2006. Jeju,South Korea.
[35]	Lu B-R, Snow AA (2005) Gene flow from genetically modified rice and its environmental consequences. BioScience, 55,669-678.
[36]	Lu B-R, Xia H (2008) Development of crop production in China:a case study in rice. In:Proceedings of the 5th International Weed Science Congress: Weeds - Local Problems / Global Challenge, pp. 281-284. June 23-27, 2008. Vancouver, BC,Canada.
[37]	Lu B-R, Song ZP, Chen JK (2003) Can transgenic rice cause ecological risks through transgene escape? Progress in Natural Science, 13,17-24.
[38]	Meng FX, Wu KM, Gao XW, Peng YF, Guo YY (2003) Geographic variation in susceptibility of Chilo suppressalis (Lepidoptera: Pyralidae) to Bacillus thuringiensis toxins in China. Journal of Economic Entomology, 96,1838-1842. URL PMID
[39]	Mercer KL, Andow DA, Wyse DL, Shaw RG (2007) Stress and domestication traits increase the relative fitness of crop-wild hybrids in sunflower. Ecology Letters, 10,383-393. URL PMID
[40]	Messeguer J (2004) Gene flow assessment in transgenic plants. Plant Cell, Tissue and Organ Culture, 73,201-212.
[41]	Messeguer J, Fogher C, Guiderdoni E, Marfa V, Catala MM, Baldi G, Mele E (2001) Field assessment of gene flow from transgenic to cultivated rices ( Oryza sativa L.) using a herbicide resistance genes as tracer marker. Theoretical and Applied Genetics, 103,1151-1159.
[42]	NBSC National Bureau of Statistics of China (中华人民共和国国家统计局) (2007) China Statistical Yearbook (中国统计年鉴). China Statistics Press, Beijing. (in Chinese)
[43]	O’Callaghan M, Glare TR, Burgess EPJ, Malone LA (2005) Effects of plants genetically modified for insect resistance on non-target organisms. Annual Review of Entomology, 50,271-292.
[44]	Oliveira AR, Castro TR, Capalbo DMF, Delalibera I (2007) Toxicological evaluation of genetically modified cotton (Bollgard ^®) and Dipel ^® WP on the non-target soil mite Scheloribates praeincisus (Acari: Oribatida). Experimental and Applied Acarology, 41,191-201. URL PMID
[45]	Rajguru SN, Burgos NR, Shivrain VK, Stewart JMD (2005) Mutations in the red rice ALS gene associated with resistance to imazethapyr. Weed Science, 53,567-577.
[46]	Rong J, Xia H, Zhu YY, Wang YY, Lu B-R (2004) Asymmetric gene flow between traditional and hybrid rice varieties ( Oryza sativa) estimated by nuclear SSRs and its implication in germplasm conservation. New Phytologist, 163,439-445.
[47]	Rong J, Song ZP, Su J, Xia H, Lu B-R, Wang F (2005) Low frequency of transgene flow from Bt/ CpTI rice to its nontransgenic counterparts planted at close spacing. New Phytologist, 168,559-566.
[48]	Rong J, Lu B-R, Song ZP, Su J, Snow AA, Zhang XS, Sun SG, Chen R, Wang F (2007) Dramatic reduction of crop-to-crop gene flow within a short distance from transgenic rice fields. New Phytologist, 173,346-353.
[49]	Rong J (戎俊), Song ZP (宋志平), Su J (苏军), Xia H (夏辉), Wang F (王锋), Lu B-R (卢宝荣) (2006) Low frequencies of transgene flow between Bt/CpTI rice and their non-transgenic counterparts under alternating cultivation. Biodiversity Science (生物多样性), 14,309-314. (in Chinese with English abstract)
[50]	Saxena D, Flores S, Stotzky G (1999) Insecticidal toxin in root exudates from Bt corn. Nature, 402,480. DOI URL PMID
[51]	Saxena D, Stotzky G (2001) Bacillus thuringiensis ( Bt) toxin released from root exudates and biomass of Bt corn has no apparent effect on earthworms, nematodes, protozoa, bacteria, and fungi in soil. Soil Biology and Biochemistry, 33,1225-1230.
[52]	Saxena D, Flores S, Stotzky G (2002) Bt toxin is released in root exudates from 12 transgenic corn hybrids representing three transformation events. Soil Biology and Biochemistry, 34,133-137.
[53]	Shivraina VK, Burgos NR, Andersb MM, Rajgurua SN, Moorea J, Salesa MA (2007) Gene flow between Clearfield ^TM rice and red rice. Crop Protection, 26,349-356.
[54]	Song ZP, Lu B-R, Zhu YG, Chen JK (2002) Pollen competition between cultivated and wild rice species (Oryza sativa and O. rufipogon). New Phytologist, 153,289-296.
[55]	Song ZP, Lu B-R, Zhu YG, Chen JK (2003) Gene flow from cultivated rice to the wild species Oryza rufipogon under experimental field conditions. New Phytologist, 157,657-665.
[56]	Stone R (2008) China plans $3.5 billion GM crops initiative. Science, 321,1279. DOI URL PMID
[57]	Tepfer D, Garcia-Gonzales R, Mansouri H, Seruga M, Message B, Leach F, Perica MC (2003) Homology-dependent DNA transfer from plants to a soil bacterium under laboratory conditions, implications in evolution and horizontal gene transfer. Transgenic Research, 12,425-437.
[58]	Tranel PJ, Wright TR (2002) Resistance of weeds to ALS-inhibiting herbicides: what have we learned? Weed Science, 50,700-712.
[59]	Wang F, Yuan QH, Shi L, Qian Q, Liu WG, Kuang BG, Zeng DL, Liao YL, Cao B, Jia SR (2006) A large-scale field study of transgene flow from cultivated rice ( Oryza sativa) to common wild rice ( O. rufipogon) and barnyard grass (Echinochloa crusgalli). Plant Biotechnology Journal, 4,667-676. URL PMID
[60]	Wang Y, Johnston S (2007) The status of GM rice R & D in China. Nature Biotechnology, 25,717-718. DOI URL PMID
[61]	Wang ZH (王忠华) (2005) Potential effects of Bt transgenic rice on soil micro-ecosystem. Chinese Journal of Applied Ecology (应用生态学报), 16,2469-2472. (in Chinese with English abstract)
[62]	Wang ZH (王忠华), Ye QF (叶庆富), Shu QY (舒庆尧), Cui HR (崔海瑞), Xia YW (夏英武), Zhou MY (周美园) (2002) Impact of root exudates from transgenic plants on soil micro-ecosystems. Chinese Journal of Applied Ecology (应用生态学报), 13,373-375. (in Chinese with English abstract)
[63]	Watkinson AR, Freckleton RP, Robinson RA, Sutherland WJ (2000) Predictions of biodiversity response to genetically modified herbicide-tolerant crops. Science, 289,1554-1557. DOI URL PMID
[64]	Wolfenbarger LL, Pfifer PR (2000) The ecological risks and benefits of genetically engineered plants. Science, 290,2088-2093. DOI URL PMID
[65]	Wu KM (2007) Monitoring and management strategy for Helicoverpa armigera resistance to Bt cotton in China. Journal of Invertebrate Pathology, 95,220-223. URL PMID
[66]	Wu KM, Li W, Feng H, Guo Y (2002) Seasonal abundance of the mirids, Lygus lucorum and Adelphocoris spp. (Hemiptera: Miridae) on Bt cotton in North China. Crop Protection, 21,997-1002.
[67]	Wu WX, Ye QF, Min H, Duan XJ, Jin WM (2003) Bt-transgenic rice straw affects the culturable microbiota and dehydrogenase and phosphatase activities in a flooded paddy soil. Soil Biology and Biochemistry, 36,289-295.
[68]	Xiong L (2004) China could be first nation to approve sale of GM rice. Science, 306,1458-1459. DOI URL PMID
[69]	Xu WH (徐文华), Wang RM (王瑞明), Liu B (刘标) (2007) Occurring rules and sustainable control of cotton plant-bugs in transgenic Bt cotton fields. Auhui Agricultural Science Bulletin (安徽农学通报), 13(19),142-145. (in Chinese)
[70]	Xue J (薛进), Su JW (苏建伟), Li JW (黎家文), Chen QF (陈秋芳) (2007) Genetic diversity among five geographical populations of Chilo suppressalis based on RAPD. Journal of Hunan Agricultural University (Natural Sciences) (湖南农业大学学报(自然科学版)), 33,160-163. (in Chinese with English abstract)
[71]	Yuan QH, Shi L, Wang F, Cao B, Qian Q, Lei XM, Liao YL, Liu WG, Cheng L, Jia SR (2007) Investigation of rice transgene flow in compass sectors by using male sterile line as a pollen detector. Theoretical and Applied Genetics, 115,549-560. DOI URL PMID
[72]	Zheng Y (郑宇), Hu QY (胡奇勇), Li BJ (李本金), Zhang XJ (张小俊), Li YR (李钥仁) (2007) Development and risk assessment of CpTI transgenic rice resistance in Chilo suppressalis. Journal of Fujian Agriculture and Forestry University (Natural Science Edition) (福建农林大学学报(自然科学版)), 36,113-116. (in Chinese with English abstract)
[73]	Zwahlen C, Hilbeck A, Howald R, Nentwig W (2003) Effects of transgenic Bt corn litter on the earthworm Lumbricus terrestris. Molecular Ecology, 12,1077-1086. DOI URL PMID