Research Paper

Transgene Flow from Glufosinate-Resistant Rice to Improved and Weedy Rice in China

Expand
  • 1Center of Rice Cultivation Technology Research, China National Rice Research Institute, Hangzhou 310006, China; 2Department of Crop, Soil and Environmental Sciences, University of Arkansas, Fayetteville 72704, AR, USA

Online published: 2014-07-26

Supported by

The study was funded by the China Agriculture Research System (Grant No. CARS-01) and Zhejiang Science and Technology Project of China (Grant No. 2008C22086).

Abstract

The development of transgenic rice with novel traits in China can increase rice productivity, but transgene flow to improved or weedy rice has become a major concern. We aimed to evaluate the potential maximum frequencies of transgene flow from glufosinate-resistant rice to improved rice cultivars and weedy rice. Treatments were arranged in randomized complete blocks with three replicates. Experiments were conducted between 2009 and 2010 at the Center for Environmental Safety Supervision and Inspection for Genetically Modified Plants, China National Rice Research Institute, Hangzhou, China. Glufosinate-resistant japonica rice 99-1 was the pollen donor. The pollen recipients were two inbred japonica rice (Chunjiang 016 and Xiushui 09), two inbred indica rice (Zhongzu 14 and Zhongzao 22), two indica hybrid rice (Zhongzheyou 1 and Guodao 1), and one weedy indica rice (Taizhou weedy rice). The offspring of recipients were planted in the field and sprayed with a commercial dose of glufosinate. Leaf tissues of survivors were analyzed by polymerase chain reaction to detect the presence of the transgene. The frequency of gene flow ranged from 0 to 0.488%. In 2009, the order of gene flow frequency was as follows: weedy rice > Chunjiang 016 > Xiushui 09 and Zhongzu 14 > Guodao 1, Zhongzheyou 1 and Zhongzao 22. Gene flow frequencies were generally higher in 2009 than in 2010, but did not differ significantly among rice materials. Gene flow frequency was the highest in weedy rice followed by the inbred japonica rice. The risk of gene flow differed significantly between years and year-to-year variance could mask risk differences among pollen recipients. Gene flow was generally lesser in taller pollen recipients than in shorter ones, but plant height only accounted for about 30% of variation in gene flow. When flowering synchrony was maximized, as in this study, low frequencies of gene flow occurred from herbicide-resistant japonica rice to other cultivars and weedy rice. Averaged across years, the risk of gene flow to weedy rice was higher than that of improved rice and hybrids. Greater resources must be dedicated to the management of remnant weedy rice in fields planted with herbicide-resistant rice, and to prevent the evolution of resistant weedy rice populations.

Cite this article

LU Yong-liang, Nilda R. BURGOS, WANG Wei-xia, YU Liu-qing . Transgene Flow from Glufosinate-Resistant Rice to Improved and Weedy Rice in China[J]. Rice Science, 2014 , 21(5) : 271 -281 . DOI: 10.1016/S1672-6308(13)60197-3

References

Akhtar Z R, Tian J C, Chen Y, Fang Q, Hu C, Peng Y F, Ye G Y. 2013. Impact of six transgenic Bacillus thuringiensis rice lines on four nontarget thrips species attacking rice panicles in the paddy field. Environ Entom, 42(1): 173–180.
Caemmerer S V, Quick W P, Furbank R T. 2012. The development of C4 rice: Current progress and future challenges. Science, 336: 1671–1672.
CAST (Council for Agricultural Science and Technology). 2007. Implications of Gene Flow in the Scale-up and Commercial Use of Biotechnology-Derived Crops: Economic and Policy Considerations. Stuttart, Arkansas: OSDA-Agricultural Research Service: 37.
Chen L J, Lee D S, Song Z P, Suh H S, Lu B R. 2004. Gene flow from cultivated rice (Oryza sativa) to its weedy and wild relatives. Ann Bot, 93(1): 67–73.
Cheng S H, Li J. 2007. Modern Chinese Rice. Beijing, China: Jindun Publisher: 90–93. (in Chinese)
de Block M, Botterman J, Vandewiele M, Dockx J, Thoen C, Gosselé V, Rao Movva N, Thompson C, van Montagu M, Leemans J. 1987. Engineering herbicide resistance in plants by expression of a detoxifying enzyme. EMBO J, 6(9): 2513–2518.
Fang Z M, Xia K F, Yang X, Grotemeyer M S, Meier S, Rentsch D, Xu X L, Zhang M Y. 2013. Altered expression of the PTR/NRT1 homologue OsPTR9 affects nitrogen utilization efficiency, growth and grain yield of rice. Plant Biotechnol J, 11(4): 446–458.
Gao J H, Zhang Y E, Zhao Q C, Lin C Y, Xu X L, Shen Z C. 2011. Transgenic rice expressing a fusion protein of Cry1Ab and Cry9Aa confers resistance to a broad spectrum of lepidopteran pests. Crop Sci, 51(6): 2535–2543.
Gealy D R. 2005. Gene movement between rice (Oryza sativa) and weedy rice (Oryza sativa): A U.S. temperate rice perspective. In: Gressel J. Crop Ferality and Volunteerism. Boca Raton: CRC Press: 323–354.
Helliwell E E, Wang Q, Yang Y N. 2013. Transgenic rice with inducible ethylene production exhibits broad-spectrum disease resistance to the fungal pathogens Magnaporthe oryzae and Rhizoctonia solani. Plant Biotechnol J, 11(1): 33–42.
Hosoi N. 1992. Comparison of the flowering and fertility under cool temperature and low radiation condition between tolerant and susceptible varieties to cool temperature at flowering and heading stages in japonica rice (Oryza sativa L.). Jpn J Breeding, 42(3): 615–630.
Hu G C, Xiao H, Yu Y H, Zhu Z G, Si H M, Fu Y P, Sun Z X. 2000. Agrobacterium-mediated transformation of the restorer lines of two-line hybrid rice with Bar gene. Chin J Appl Environ Biol, 6(6): 511–515. (in Chinese with English abstract)
Hu T Z, Qu X X, Xiao G S, Huang X Y. 2009. Enhanced tolerance to herbicide of rice plants by over-expression of a glutathione S-transferase. Mol Breeding, 24(4): 409–418.
Huang D N, Wang H Z, Guo L B. 2006. Rice Transgene Research and Breeding. Beijing, China: Chinese Agriculture Science and Technology: 154. (in Chinese)
Huang J K, Rozelle S, Pray C, Wang Q F. 2002. Plant biotechnology in China. Science, 295: 674–676.
Inui H, Shiola N, Ido Y, Inoue T, Hirose S, Kawahigashi H, Ohkawa Y, Okawa H. 2001. Herbicide metabolism and tolerance in the transgenic rice plants expressing human CYP2C9 and CYP2C19. Pest Biochem Physiol, 71(3): 156–169.
James C. 2011. Global Status of Commercialized Biotech/GM Crops: 2011. Ithaca, NY, USA: International Service for the Acquisition of Agri-Biotech Applications: 43.
James C. 2012. Global Status of Commercialized Biotech/GM Crops: 2012. Ithaca, NY, USA: International Service for the Acquisition of Agri-Biotech Applications: 44.
Jia S R, Peng Y F. 2002. GMO biosafety research in China. Environ Biosaf Res, 1: 5–8.
Jia S R, Wang F, Shi L, Yuan Q H, Liu W G, Liao Y L, Li S G, Jin W J, Peng H P. 2007. Transgene flow to hybrid rice and its male-sterile lines. Transg Res, 16: 491–501.
Jiang J D, Linscombe S D, Wang J L, Oard J H. 2000. High efficiency transformation of U.S. rice lines from mature seed-derived calli and segregation of glufosinate resistance under field conditions. Crop Sci, 40(6): 1729–1741.
Jiang Z X, Xia H B, Basso B, Lu B R. 2012. Introgression from cultivated rice influences genetic differentiation of weedy rice populations at a local spatial scale. Theor Appl Genet, 124(2): 309–322.
Jung H I, Kuk Y I, Kim H Y, Back K, Lee D J, Lee S, Burgos N R. 2010. Resistance levels and fitness of protoporphyrinogen oxidase (PROTOX) inhibitor-resistant transgenic rice in paddy fields. Field Crops Res, 115(2): 125–131.
Kajala K, Covshoff S, Karki S, Woodfield H, Tolley B J, Dionora M J A, Mogul R T, Mabilangan A E, Danila F R, Hibberd J M, Quick W P. 2011. Strategies for engineering a two-celled C4 photosynthetic pathway into rice. J Exp Bot, 62(9): 3001–3010.
Kuang H H, Tu D S. 1949. Studies on the fertile percentage in varietal crosses of rice hybrids. Agron J, 41: 195–199.
Kurai T, Wakayama M, Abiko T, Yanagisawa S, Aoki N, Ohsugi R. 2011. Introduction of the ZmDof1 gene into rice enhances carbon and nitrogen assimilation under low-nitrogen conditions. Plant Biotechnol J, 9(8): 826–837.
Li J Y, Mu J Y, Bai J T, Fu F Y, Zou T T, An F Y, Zhang J, Jing H W, Wang Q, Li Z, Yang S H, Zuo J R. 2013. PARAQUAT RESISTANT1, a golgi-localized putative transporter protein, is involved in intracellular transport of paraquat. Plant Physiol, 162(1): 470–483.
Li S R. 2004. Environmental risk assessment of GM crops: Progress in risk assessment. Sci Agric Sin, 37(2): 175–187. (in Chinese with English abstract)
Li W, Zhang J Z, Zhang G Q, Zuo Q F. 2002. Analysis of heterosis of main agronomic traits of indica-japonica lines. J Southwest Agric Univ, 24(4): 317–339. (in Chinese with English abstract)
Lu B R, Snow A A. 2005. Gene flow from genetically modified rice and its environmental consequences. BioSci, 55(8): 669–678.
Lu B R, Yang C. 2009. Gene flow from genetically modified rice to its wild relatives: Assessing potential ecological consequences. Biotechnol Adv, 27(6): 1083–1091.
Ma J, Song Y Z, Wu B, Jiang M S, Li K D, Zhu C X, Wen F J. 2011. Production of transgenic rice new germplasm with strong resistance against two isolations of rice stripe virus by RNA interference. Transg Res, 20(6): 1367–1377.
Messeguer J, Fogher C, Guiderdoni E, Marfa V, Catala M M, Baldi G, Mele E. 2001. Field assessments of gene flow from transgenic to cultivated rice (Oryza sativa L.) using a herbicide resistance gene as tracer marker. Theor Appl Genet, 103(8): 1151–1159.
Messeguer J, Marfa V, Catala M M, Guiderdoni E, Mele E. 2004. A field study of pollen-mediated gene flow from Mediterranean GM rice to conventional rice and the red rice weed. Mol Breed, 13(1): 103–112.
Ministry of Agriculture. 2002. Chinese Rice Quality Regionalism and High Quality Cultivation. Beijing, China: Chinese Agriculture Publisher: 63. (in Chinese)
Mohanty S. 2013. Trends in global rice consumption. Rice Today. Available at http://irri.org/rice-today/trends-in-global-rice-consumption.
Niruntrayakul S, Rerkasem B, Jamjod S. 2009. Crossability between cultivated rice (Oryza sativa) and common wild rice (O. rufipogon) and characterization of F1 and F2 populations. Sci Asia, 35: 161–169.
Oard J H, Linscombe S D, Braverman M P, Jodari F, Blouin D C, Leech M, Kohli A, Vain P, Cooley J C, Christou P. 1996. Development, field evaluation, and agronomic performance of transgenic herbicide resistant rice. Mol Breed, 2(4): 359–368.
OECD (Organization for Economic Co-operation and Development). 1999. Consensus document on the biology of Oryza sativa (rice). In: OECD Environmental Health and Safety Publications: Series on Harmonization of Regulatory Oversight in Biotechnology. Paris, France: OECD.
Olofsdotter M, Valverde B E, Madsen K H. 2000. Herbicide-resistant rice (Oryza sativa L.): Global implications for weedy rice and weed management. Ann Appl Biol, 137(3): 279–295.
Ortega B R. 2007. Analysis of factors affecting spikelet sterility in flooded rice under field conditions in Chile. Arch Agron Soil Sci, 53(2): 183–192.
Pusadee T, Schaal B A, Rerkasem B, Jamjod S. 2013. Populations structure of the primary gene pool of Oryza sativa in Thailand. Genet Resour Crop Evol, 60(1): 335–353.
Qi Y B, Chen L, He X L, Jin Q S, Zhang X M, He Z H. 2013. Marker-free, tissue-specific expression of Cry1Ab as a safe transgenic strategy for insect resistance in rice plants. Pest Manag Sci, 69(1): 135–141.
Robert E H, Craufurd R Q, Cochet F L. 1961. Estimation of percentage natural cross-pollination: Experiment on rice. Nature, 190: 1084–1085.
Rong J, Xia H, Zhu Y Y, Wang Y Y, Lu B R. 2004. Asymmetric gene flow between traditional and hybrid rice varieties (Oryza sativa) indicated by nuclear simple sequence repeats and implications of germplasm conservation. New Phytol, 163(2): 439–445.
Rong J, Wang F, Song Z P, Su J, Chen R, Lu B R. 2012. Scale effect on rice pollen-mediated gene flow: Implications in assessing transgene flow from genetically engineered plants. Ann Appl Biol, 161(1): 3–11.
SAS. 2011. Base SAS 9.2 Procedures Guide. Cary, NC: SAS Institute Inc.
Shah J M, Singh R, Veluthambi K. 2013. Transgenic rice lines constitutively co-expressing tlp-D34 and chi11 display enhancement of sheath blight resistance. Biol Plant, 57(2): 351–358.
Shimizu T, Ogamino T, Hiraguri A, Nakazono-Nagaoka E, Uehara- Ichiki T, Nakajima M, Akutsu K, Omura T, Sasaya T. 2013. Strong resistance against rice grassy stunt virus is induced in transgenic rice plants expressing double-stranded RNA of the viral genes for nucleocapsid or movement proteins as targets for RNA interference. Phytopathology, 103(5): 513–519.
Shivrain V K, Burgos N R, Anders M M, Rajguru S N, Moore J, Sales M A. 2007. Gene flow between ClearfieldTM rice and red rice. Crop Prot, 26(3): 349–356.
Shivrain V K, Burgos N R, Gealy D R, Moldenhauer K A K, Baquireza C J. 2008. Maximum outcrossing rate and genetic compatibility between red rice (Oryza sativa) biotypes and ClearfieldTM rice. Weed Sci, 56(6): 807–813.
Shivrain V K, Burgos N R, Sales M A, Mauromoustakos A, Gealy D R, Smith K L, Black H L, Jia M. 2009. Factors affecting the outcrossing rate between ClearfieldTM rice and red rice (Oryza sativa). Weed Sci, 57(4): 394–403.
Song X L, Liu L L, Wang Z, Qiang S. 2009. Potential gene flow from transgenic rice (Oryza sativa L.) to different weedy rice (Oryza sativa f. spontanea) accessions based on reproductive compatibility. Pest Manag Sci, 65(8): 862–869.
Song Z P, Lu B R, Chen J K. 2001. A study of pollen viability and longevity in Oryza rufipogon, O. sativa, and their hybrids. Int Rice Res Notes, 26: 31–32.
Song Z P, Lu B R, Zhu Y G, Chen J K. 2002. Pollen competition between cultivated and wild rice species (Oryza sativa and O. rufipogon). New Phytol, 153(2): 289–296.
Song Z P, Lu B R, Zhu Y G, Chen J K. 2003. Gene flow from cultivated rice to the wild species Oryza rufipogon under experimental field conditions. New Phytol, 157(3): 657–665.
Sudiantu E, Song B K, Neik T X, Saldain N E, Scott R C, Burgos N R. 2013. Clearfield rice: Its development, success, and key challenges on a global perspective. Crop Prot, 49: 40–51.
Takakura Y, Oka N, Suzuki J, Tsukamoto H, Ishida Y. 2012. Intercellular production of tamavidin 1, a biotin-binding protein from Tamogitake mushroom, confers resistance to the blast fungus Magnaporthe oryzae in transgenic rice. Mol Biotechnol, 51(1): 9–17.
Thompson C J, Movva N R, Tizard R, Crameri R, Davies J E, Lauwereys M, Botterman J. 1987. Characterization of the herbicide-resistance gene bar from Streptomyces hygroscopicus. EMBO J, 6(9): 2519–2523.
Thomson D, Henry R. 1995. Single-step protocol for preparation of plant tissue for analysis by PCR. Biotechniques, 19(3): 394–397.
USDA-FAS. 2013. Production, Supply and Distribution. United States Department of Agriculture-Foreign Agricultural Service.
Verma V, Sharma S, Devi S V, Rajasubramaniam S, Dasgupta I. 2012. Delay in virus accumulation and low virus transmission from transgenic rice plants expressing rice tungro spherical virus RNA. Virus Genes, 45(2): 350–359.
Vermif P. 2006. EU and Japan block unapproved GM rice. Nat Biotech, 24(10): 1186.
Wakasa Y, Ozawa K, Takaiwa F. 2012. Agrobacterium-mediated co-transformation of rice using two selectable marker genes derived from rice genome components. Plant Cell Rep, 31(11): 2075–2084.
Wang J, Shen Z, Shi S. 1991. Flower behavior and genetics of indica rice, japonica rice and hybrid. Rice, 5: 39–42.
Wei Y P, Yao F Y, Zhu C X, Jiang M S, Li G X, Song Y Z, Wen F J. 2008. Breeding of transgenic rice restorer line for multiple resistance against bacterial blight, striped stem borer and herbicide. Euphytica, 163(2): 177–184.
Xiao G Y, Yuan L P, Deng X X, Tang L, Luo R L. 2003. Studies on the heterosis of indica/javanica and japonica/javanica hybrid rice: II. Analysis of the heterosis of agronomic traits. Acta Agron Sin, 29(3): 364–371. (in Chinese with English abstract)
Yang X, Xia H, Wang W, Wang F, Su J, Snow A A, Lu B R. 2011. Transgenes for insect resistance reduce herbivory and enhance fecundity in advanced generations of crop-weed hybrids of rice. Evol Appl, 4(5): 672–684.
Yu T, Zhang L, Hu Z L, Song W Z, Liu S J, Zhang Z H, Zhu Y G. 2003. Genetic analysis of floral characters in a DH population derived from an indica/japonica cross of rice. J Wuhan Bot Res, 21(6): 459–463. (in Chinese with English abstract)
Yuan Q H, Shi L, Wang F, Cao B, Qian Q, Lei X M, Liao Y L, Liu W G, Cheng L, Jia S R. 2007. Investigation of rice transgene flow in compass sectors by using male sterile line as a pollen detector. Theor Appl Genet, 115(4): 549–560.
Zeng H L, Lu K Y, He D H, Pan X X, Zhang D R, Zeng Z. 2000. Evaluation on the fertility of some indica rice hybrids under high temperature conditions. J Huazhong Agric Univ, 19(1): 1–4. (in Chinese with English abstract)
Zuo J, Zhang L J, Song X L, Dai W M, Qiang S. 2011. Innate factors causing differences in gene flow frequency from transgenic rice to different weedy rice biotypes. Pest Manag Sci, 67(6): 677–690.
Outlines

/

浙ICP备05004719号-15   公安备案号:33010302003355
Copyright © Editorial office of Rice Science
Tel: 0571-63371017 E-mail: crrn@fy.hz.zn.cn; cjrs278@gmail.com
Supported by Beijing Magtech Co., Ltd.
Total visitors:  Visitors of today:  Now online: