Please wait a minute...
Journal of Integrative Agriculture  2019, Vol. 18 Issue (12): 2793-2805    DOI: 10.1016/S2095-3119(19)62662-6
Special Issue: 杂草合辑Weed
Plant Protection Advanced Online Publication | Current Issue | Archive | Adv Search |
Fitness of F1 hybrids between stacked transgenic rice T1c-19 with cry1C*/bar genes and weedy rice
HUANG Yao*, WANG Yuan-yuan*, QIANG Sheng, SONG Xiao-ling, DAI Wei-min
Weed Research Laboratory, College of Life Sciences, Nanjing Agricultural University, Nanjing 210095, P.R.China
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
Compared to single-trait transgenic crops, stacked transgenic plants may be more prone to become weedy, and transgene flow from stacked transgenic plants to weedy relatives may pose a potential environmental risk because these hybrids could be more advantageous under specific environmental conditions.  Evaluation of the potential environmental risk caused by stacked transgenes is essential for assessing the environmental consequences caused by crop-weed transgene flow.  The agronomic performance of fitness-related traits was assessed in F1+ (transgene positive) hybrids (using the transgenic line T1c-19 as the paternal parent) in monoculture and mixed planting under presence or absence glufosinate pressure in the presence or absence of natural insect pressure and then compared with the performance of F1– (transgene negative) hybrids (using the non-transgenic line Minghui 63 (MH63) as the paternal parent) and their weedy rice counterparts.  The results demonstrated that compared with the F1– hybrids and weedy rice counterparts, the F1+ hybrid presented higher performance (P<0.05) or non-significant changes (P>0.05) under natural insect pressure, respectively, lower performance (P<0.05) or non-significant changes (P>0.05) in the absence of insect pressure in monoculture planting, respectively.  And compared to weedy rice counterparts, the F1+ hybrid presented higher performance (P<0.05) or non-significant changes (P>0.05) in the presence or absence of insect pressure in mixed planting, respectively.  The F1+ hybrids presented non-significant changes (P>0.05) under the presence or absence glufosinate pressure under insect or non-insect pressure in monoculture planting.  The all F1+ hybrids and two of three F1– hybrids had significantly lower (P<0.05) seed shattering than the weedy rice counterparts.  The potential risk of gene flow from T1c-19 to weedy rice should be prevented due to the greater fitness advantage of F1 hybrids in the majority of cases. 
Keywords:  weedy rice        hybrids        stacked transgenes        safety assessment        fitness  
Received: 02 November 2018   Accepted:
Fund: This research was financially supported by the China Transgenic Organism Research and Commercialization Project (2016ZX08011-001).
Corresponding Authors:  Correspondence SONG Xiao-ling, E-mail:; DAI Wei-min, E-mail:    
About author:  * These authors contributed equally to this study.

Cite this article: 

HUANG Yao, WANG Yuan-yuan, QIANG Sheng, SONG Xiao-ling, DAI Wei-min. 2019. Fitness of F1 hybrids between stacked transgenic rice T1c-19 with cry1C*/bar genes and weedy rice. Journal of Integrative Agriculture, 18(12): 2793-2805.

Arrieta-Espinoza G, Sánchez E, Vargas S, Lobo J, Quesada T, Espinoza A M. 2005. The weedy rice complex in Costa Rica. I. Morphological study of relationships between commercial rice varieties, wild Oryza relatives and weedy types. Genetic Resources and Crop Evolution, 52, 575–587.
Burgos N R, Norman R J, Gealy D R, Black H. 2006. Competitive N uptake between rice and weedy rice. Field Crops Research, 99, 96–105.
Cao Q J, Xia H, Yang X, Lu B R. 2009. Performance of hybrids between weedy rice and insect-resistant transgenic rice under field experiments: Implication for environmental biosafety assessment. Journal of Integrative Plant Biology, 51, 1138–1148.
Chen 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. Annals of Botany, 93, 67–73.
Chun Y J, Kim D I, Park K W, Jeong H J, An J H, Cho K H, Back K, Kim H M, Kim C G. 2011. Gene flow from herbicide-tolerant GM rice and the heterosis of GM rice-weed F2 progeny. Planta, 233, 807–815.
Cui R R, Wei Y, Meng P P, Ma Y L, Jin Y, Li Q R, Qiang S, Dai W M, Song X L. 2012. Assessment on potential weediness of transgenic glufosinate-resistant rice Minghui 86B. Rice Science, 26, 467–475. (in Chiense)
Dai L, Dai W M, Song X L, Lu B R, Qiang S. 2014. A comparative study of competitiveness between different genotypes of weedy rice (Oryza sativa) and cultivated rice. Pest Management Science, 70, 113–122.
David Y L, Eric P W, Zhang W, Steve D L. 2003. Response of glufosinate-resistant rice (Oryza sativa) to glufosinate application timings. Weed Technology, 17, 157–160.
Delouche J C, Burgos N R, Gealy D R, Zorrilla D S M G, Labrada R, Larinde M. 2007. Weedy Rices: Origin, Biology, Ecology and Control (vol. 188). Food & Agriculture Organic Plant Production and Protection Paper, Rome.
Ellstrand N C, Meirmans P, Rong J, Bartsch D, Ghosh A, de Jong T J, Haccou P, Lu B L, Snow A A, Stewart Jr N, Strasburg J L, Van Tienderen P H, Vrieling K, Hooftman D. 2013. Introgression of crop alleles into wild or weedy populations. Annual Review of Ecology, Evolution, and Systematics, 44, 325–345.
Fan B L, Tang X J, Tian H, Sun Z F, Yang W X, Xie Y J, Li X L, Song Y, Xu S Y, Liu J F. 2014. Chronic toxicity of Huahui no. 1 rice toward rats. Scientia Sinica (Vitae), 44, 911–919. (in Chinese)
Feurtey A, Cornille A, Shykoff J A, Snirc A, Giraud T. 2017. Crop-to-wild gene flow and its fitness consequences for a wild fruit tree: Towards a comprehensive conservation strategy of the wild apple in Europe. Evolutionary Applications, 10, 180–188.
Gressel J, Valverde B E. 2009. A strategy to provide long-term control of weedy rice while mitigating herbicide resistance transgene flow, and its potential use for other crops with related weeds. Pest Management Science, 65, 723–731.
Guèritaine G, Sester M, Eber F, Chevre A M , Darmency H. 2002. Fitness of backcross six of hybrids between transgenic oilseed rape (Brassica napus) and wild radish (Raphanus raphanistrum). Molecular Ecology, 11, 419–1426.
Huang J, Rozelle S, Pray C, Wang Q. 2002. Plant biotechnology in China. Science, 295, 377–378 .
Huang Y, Li J K, Qiang S, Dai W M, Song X L. 2016. Transgenic restorer rice line T1c-19 with stacked cry1C*/bar genes has low weediness potential without selection pressure. Journal of Integrative Agriculture, 15, 5–7.
Huang Y, Li J K, Qiang S, Luo T P, Song X L. 2015. Gene flow from transgenic rice T1c-19 with stacked cry1C*/bar genes to weedy and cultivated rice species. Chinese Journal of Applied and Environmental Biology, 21, 1112–1119. (in Chinese)
Jenczewski E, Ronfort J, Chèvre A M. 2003. Crop-to-wild gene flow, introgression and possible fitness effects of transgenes. Environmental Biosafety Research, 2, 9–24.
Jia S, Peng Y. 2002. GMO biosafety research in China. Environmental Biosafety Research, 1, 5–8.
Jongsma M A, Gould F, Legros M, Yang L, Loon J J A, Dicke M. 2010. Insect oviposition behavior affects the evolution of adaptation to Bt crops: Consequences for refuge policies. Evolutionary Ecology, 24, 1017–1030.
Li X Q, Chen F J, Liu M Q, Chen X Y, Hu F. 2012. Effects of two years planting transgenic Bt rice (Bt SY63) on soil nematode community. Chinese Journal of Applied Ecology, 23, 3065–3071. (in Chinese)
Liang Y Y, Liu F, Li J S, Cheng Z X, Chen H F, Wang X M, Xiao N W, Liu Y B. 2018. Coexistence of Bt-transgenic and conventional rice affects insect abundance and plant fitness in fields. Pest Management Science, 74, 1646–1653.
Liu S N, Song X L, Hu Y H, Dai W M, Qiang S. 2016. Fitness of hybrids between two types of transgenic rice and six japonica and indica weed rice accessions. Crop Science, 56, 2751–2765.
Liu Y B, Ge F, Liang Y Y, Wu G, Li J S. 2015. Characterization of competitive interactions in the coexistence of Bt-transgenic and conventional rice. BMC Biotechnology, 15, 27.
Londo J P, Bautista N S, Sagers C L, Lee E, Watrud L S. 2010. Glyphosate drift promotes changes in fitness and transgene gene flow in canola (Brassica napus) and hybrids. Annuals of Botany, 106, 957–965.
Lu B R. 2008. Transgene escape from GM crops and potential biosafety consequences: an environmental perspective. International Centre for Genetic Engineering and Biotechnology (ICGEB), Collection of Biosafety Reviews, 4, 66–144.
Lu B R, Snow A A. 2005. Gene flow from genetically modified rice and its environmental consequences. BioScience, 55, 669–678.
Lu B R, Yang C. 2009. Gene flow from genetically modified rice to its wild relatives: Assessing potential ecological consequences. Biotechnology Advances, 27, 1083–1091.
Lu B R, Yang X, Ellstrand N C. 2016. Fitness correlates of crop transgene flow into weedy populations: A case study of weedy rice in China and other examples. Evolutionary Applications, 9, 857–870.
Lu Z B, Tian J C, Han N S, Hu C, Peng Y F, Stanley D, Ye G Y. 2014. No direct effects of two transgenic Bt rice lines, T1C-19 and T2A-1, on the arthropod communities. Environmental Entomology, 43, 1453–1463.
Messeguer J, Marfa V, Catala M M, Guiderdoni E, Melé E. 2004. A field study of pollen-mediated gene flow from Mediterranean GM rice to conventional rice and the red rice weed. Molecular Breeding, 13, 103–112.
Møldrup M E, Geu-Flores F, de Vos M, Olsen C E, Sun J, Jander G, Halkier B A. 2012. Engineering of benzylglucosinolate in tobacco provides proof-of-concept for dead-end trap crops genetically modified to attract Plutella xylostella (diamondback moth). Plant Biotechnology Journal, 10, 435–442.
Oard J, Cohn M A, Linscombe S, Gealy D, Gravois K. 2000. Field evaluation of seed production, shattering, and dormancy in hybrid populations of transgenic rice (Oryza sativa) and the weed, red rice (Oryza sativa). Plant Science (Shannon), 157, 13–22.
Ohadi S, Hodnett G, Rooney W, Bagavathiannan M. 2018. Gene flow and its consequences in Sorghum spp. Critical Reviews in Plant Sciences, 36, 367–385.
Olguin E R, Arrieta-Espinoza G, Lobo J A, Espinoza-Esquivel A M. 2009. Assessment of gene flow from a herbicide-resistant indica rice (Oryza sativa L.) to the Costa Rican weedy rice (Oryza sativa) in Tropical America, factors affecting hybridization rates and characterization of F1 hybrids. Transgenic Research, 18, 633–647.
Olsen K M, Caicedo A L, Jia Y. 2007. Evolutionary genomics of weedy rice in the USA. Journal of Integrative Plant Biology, 49, 811–816.
Rong J, Lu B R, Song Z P, Su J, Snow A A, Zhang X S, Sun S G, 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.
Rong J, Song Z, 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.
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 Protection, 26, 349–356.
Shivrain V K, Burgos N R, Gealy D R, Sales M A, Smith K L. 2009. Gene flow from weedy red rice (Oryza sativa L.) to cultivated rice and fitness of hybrids. Pest Management Science, 65, 1124–1129.
Slatkin M. 1987. Gene flow and the geographic structure of natural populations. Science, 236, 787–792.
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 Management Science, 65, 862–869.
Song X L, Wang Z, Qiang S. 2011. Agronomic performance of F1, F2 and F3 hybrids between weedy rice and transgenic glufosinate-resistant rice. Pest Management Science, 67, 921–931.
Song Z P, Lu B R, Wang B, Chen J K. 2004. Fitness estimation through performance comparison of F1 hybrids with their parental species Oryza rufipogon and O. sativa. Annals of Botany, 93, 311–316.
Sudianto 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 Protection, 49, 40–51.
Sun G H, Dai W M, Cui R R, Qiang S, Song X L. 2015. Gene flow from glufosinate-resistant transgenic hybrid rice Xiang 125S/Bar68-1 to weedy rice and cultivated rice under different experimental designs. Euphytica, 204, 211–227.
Tang W, Chen H, Xu C G, Li X H, Lin Y J, Zhang Q F. 2006. Development of insect-resistant transgenic indica rice with a synthetic cry1C* gene. Molecular Breeding, 18, 1–10.
Walsh K D, Hills M J, Martin S L, Hall L M. 2015. Pollen-mediated gene flow in Camelina sativa (L.) Crantz. Crop Science, 170, 279–286.
Wang W, Xu T, Lu B R. 2010. Commercialization and environmental biosafety management of herbicide-resistant transgenic plants. Weed Science, 4, 1–9. (in Chinese)
Warwick S I, Beckie H J, Hall L M. 2009. Gene flow, invasiveness, and ecological impact of genetically modified crops. Annals of the New York Academy of Sciences, 1168, 72–99 .
Xia H, Lu B R, Xu K, Wang W, Yang X, Yang C, Luo J, Lai F X, Ye W L, Fu Q. 2011. Enhanced yield performance of Bt rice under target-insect attacks, implications for field insect management. Transgenic Research, 20, 655–664.
Yang X, Li L, Cai X X, Wang F, Su J, Lu B R. 2015. Efficacy of insect-resistance Bt/CpTI transgenes in F5–F7 generations of rice crop–weed hybrid progeny: implications for assessing ecological impact of transgene flow. Science Bulletin, 60,1563–1571.
Yang X, Wang F, Su J, Lu B R. 2012. Limited fitness advantages of crop-weed hybrid progeny containing insect-resistant transgenes (Bt/CpTI) in transgenic rice field. PLoS ONE, 7, 398–398.
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. Evolutionary Applications, 4, 672–684.
Yu G Q, Bao Y, Shi C H, Dong C Q, Ge S. 2005. Genetic diversity and population differentiation of Liaoning weedy rice detected by RAPD and SSR markers. Biochemical Genetics, 43, 261–270.
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 directions by using male sterile line as a pollen detector. Theoretical and Applied Genetics, 115, 549–560.
Zhang L J, Dai W M, Wu C, Song X L, Qiang S. 2012. Genetic diversity and origin of Japonica- and Indica-like rice biotypes of weedy rice in the Guangdong and Liaoning provinces of China. Genetic Resources and Crop Evolution, 59, 399–410.
Zhang J X, Kang Y, Valverde B E, Dai W M, Song X L, Qiang S. 2018. Feral rice from introgression of weedy rice genes into transgenic herbicide-resistant hybrid-rice progeny. Journal of Experimental Botany, 69, 3855–3865.
Zhang N Y, Linscombe S, Oard J. 2003. Out-crossing frequency and genetic analysis of hybrids between transgenic glufosinate herbicide-resistant rice and the weed, red rice. Euphytica, 130, 35–45.
Zhang W Q, Linscombe S D, Oard J H. 2008. Genetic and agronomic analyses of red rice-Clearfield hybrids and their progeny produced from natural and controlled crosses. Euphytica, 164, 659–668.
Zhang W Q, Linscombe S D, Webster E, Tan S Y, Orad J. 2006. Risk assessment of the transfer of imazethapyr herbicide tolerance from Clearfield rice to red rice (Oryza sativa). Euphytica, 152, 75–86.
Zhang X, Yang Y, Xu H, Chen H, Wang B, Lin Y, Lu Z. 2011. Resistance performances of transgenic Bt rice lines T(2A)-1 and T1c-19 against Cnaphalocrocis medinalis (Lepidoptera: Pyralidae). Journal of Economic Entomology, 104, 1730–1735.
Zuo J, Zhang L J, Song X L, Dai W, Qiang S. 2011. Innate factors causing differences in gene flow frequency from transgenic rice to different weedy rice biotypes. Pest Management Science, 67, 677–690.
[1] WANG Hao-quan, DAI Wei-min, ZHANG Zi-xu, LI Meng-shuo, MENG Ling-chao, ZHANG Zheng, LU Huan, SONG Xiao-ling, QIANG Sheng. Occurrence pattern and morphological polymorphism of weedy rice in China[J]. >Journal of Integrative Agriculture, 2023, 22(1): 149-169.
[2] LIU Yue-e, HOU Peng, HUANG Gui-rong, ZHONG Xiu-li, LI Hao-ru, ZHAO Jiu-ran, LI Shao-kun, MEI Xu-rong. Maize grain yield and water use efficiency in relation to climatic factors and plant population in northern China[J]. >Journal of Integrative Agriculture, 2021, 20(12): 3156-3169.
[3] FAN Yin-jun, LI Fen, Abd Allah A. H. Mohammed, YI Xiao-qin, ZHANG Min, Nicolas Desneux, GAO Xi-wu. The damage risk evaluation of Aphis gossypii on wheat by host shift and fitness comparison in wheat and cotton[J]. >Journal of Integrative Agriculture, 2018, 17(03): 631-639.
No Suggested Reading articles found!