Abstract
Gene flow from genetically modified (GM) crops to non-GM cultivars or weedy relatives may lead to the development of more aggressive weeds. We quantified the amount of gene flow from herbicide-tolerant GM rice (Protox GM, derived from the cultivar Dongjin) to three cultivars (Dongjin, Aranghyangchal and Hwaseong) and a weedy rice line. Gene flow frequency generally decreased with increasing distance from the pollen donor. At the shortest distance (0.5 m), we observed a maximum frequency (0.039%) of gene flow. We found that the cultivar Dongjin received the greatest amount of gene flow, with the second being weedy rice. Heterosis of F2 inbred progeny was also examined between Protox GM and weedy rice. We compared growth and reproduction between F2 progeny (homozygous or hemizygous for the Protox gene) and parental rice lines (GM and weedy rice). Here, transgene-homozygous F2 progeny was significantly taller and produced more seeds than the transgene-hemizygous F2 progeny and parental lines. Although the gene flow frequency was generally low, our results suggest that F2 progeny between GM and weedy relatives may exhibit heterosis.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bajaj S, Mohanty A (2005) Recent advances in rice biotechnology-towards genetically superior transgenic rice. Plant Biotechnol J 3:275–307. doi:10.1111/j.1467-7652.2005.00130.x
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. J Integr Plant Biol 51:1138–1148. doi:10.1111/j.1744-7909.2009.00877.x
Chandler S, Dunwell JM (2008) Gene flow, risk assessment and the environmental release of transgenic plants. Crit Rev Plant Sci 27:25–49. doi:10.1080/07352680802053916
Chapman MA, Burke JM (2006) Letting the gene out of the bottle: the population genetics of genetically modified crops. New Phytol 170:429–443. doi:10.1111/j.1469-8137.2006.01710.x
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. Ann Bot 93:67–73. doi:10.1093/aob/mch006
Dale PJ, Clarke B, Fontes EMG (2002) Potential for the environmental impact of transgenic crops. Nat Biotechnol 20:567–574. doi:10.1038/nbt0602-567
Delouche JC, Burgos NR, Gealy DR, Zorilla-San MG, Labrada R, Larinde M (2007) Weedy rices—origin, biology, ecology and control. FAO of the United Nations, Rome, p 144. http://www.fao.org/docrep/010/a1023e/a1023e00.htm. Accessed 21 September 2010
Ellstrand NC (2003) Current knowledge of gene flow in plants: implications for transgene flow. Philos Trans R Soc B Biol Sci 358:1163–1170. doi:10.1098/rstb.2003.1299
Ellstrand NC, Prentice HC, Hancock JF (1999) Gene flow and introgression from domesticated plants into their wild relatives. Annu Rev Ecol Evol Syst 30:539–563. doi:10.1146/annurev.ecolsys.30.1.539
Gealy DR, Mitten DH, Rutger JN (2003) Gene flow between red rice (Oryza sativa) and herbicide-resistant rice (O. sativa): implications for weed management. Weed Technol 17:627–645. doi:10.1614/WT02-100
Gepts P, Papa R (2003) Possible effects of (trans)gene flow from crops on the genetic diversity from landraces and wild relatives. Environ Biosafety Res 2:89–103. doi:10.1051/ebr:2003009
Hoyle M, Cresswell JE (2007) The effect of wind direction on cross-pollination in wind-pollinated GM crops. Ecol Appl 17:1234–1243. doi:10.1890/06-0569
Jang I-C, Oh S-J, Seo J-S, Choi W-B, Song SI, Kim CH, Kim YS, Seo H-S, Choi YD, Nahm BH, Kim J-K (2003) Expression of a bifunctional fusion of the Eschericia coli genes for trehalose-6-phosphate synthase and trehalose-6-phosphate phosphatase in transgenic rice plants increase trehalose accumulation and abiotic stress tolerance without stunting growth. Plant Physiol 131:516–524. doi:10.1104/pp.007237
Jeong S-C, Pack IS, Cho E-Y, Youk ES, Park S, Yoon WK, Kim C-G, Choi YD, Kim J-K, Kim HM (2007) Molecular analysis and quantitative detection of a transgenic rice line expressing a bifunctional fusion TPSP. Food Control 18:1434–1442. doi:10.1016/j.foodcont.2006.10.007
Jia S, Wang F, Shi L, Yuan Q, Liu W, Liao Y, Li S, Jin W, Peng H (2007) Transgene flow to hybrid rice and its male-sterile lines. Transgenic Res 16:491–501. doi:10.1007/s11248-006-9037-z
Langevin SA, Clay K, Grace JB (1990) The incidence and effects of hybridization between cultivated rice and its related weed rice (Oryza sativa L.). Evolution 44:1000–1008. doi:10.2307/2409561
Lee K, Yang K, Kang K, Kang S, Lee N, Back K (2007) Use of Myxococcus xanthus protoporphyrinogen oxidase as a selectable marker for transformation of rice. Pest Biochem Physiol 88:31–35. doi:10.1016/j.pestbp.2006.08.011
Lippman ZB, Zamir D (2007) Heterosis: revisiting the magic. Trends Ecol Evol 23:60–66. doi:10.1016/j.tig.2006.12.006
Lu B-R, Snow AA (2005) Gene flow from genetically modified rice and its environmental consequences. Bioscience 55:669–678. doi:10.1641/0006-3568(2005)055[0669:GFFGMR]2.0.CO;2
Lu B-R, Yang C (2009) Gene flow from genetically modified rice to its wild relatives: Assessing potential ecological consequences. Biotechnol Adv 27:1083–1091. doi:10.1016/j.biotechadv.2009.05.018
Messeguer J (2003) Gene flow assessment in transgenic plants. Plant Cell Tissue Organ Cult 73:201–212. doi:10.1023/A:1023007606621
Messeguer J, Fogher C, Guiderdoni E, Marfà V, Català MM, Baldi G, Melé 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 103:1151–1159. doi:10.1007/s001220100713
Messeguer J, Marfà V, Català MM, 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. Mol Breed 13:103–112. doi:10.1023/B:MOLB.0000012285.39859.9d
Nan L, Huabang C (2009) An accurate and rapid PCR-based zygosity testing method for genetically modified maize. Mol Plant Breed 7:619–623
Oard JH, Linscombe SD, Braverman MP, Jodari F, Blouin DC, Leech M, Kohli A, Vain P, Cooley JC, Christou P (1996) Development, field evaluation, and agronomic performance of transgenic herbicide resistant rice. Mol Breed 2:359–368. doi:10.1007/BF00437914
Oard J, Cohn MA, 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 Sci 157:13–22. doi:10.1016/S0168-9452(00)00245-4
Pilson D, Prendeville HR (2004) Ecological effects of transgenic crops and the escape of transgenes into wild populations. Annu Rev Ecol Evol Syst 35:149–174. doi:10.1146/annurev.ecolsys.34.011802.132406
R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. http://www.R-project.org. Accessed 3 September 2010
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 Phytol 168:559–566. doi:10.1111/j.1469-8137.2005.01539.x
Rong J, Lu B-R, Song Z, Su J, Snow AA, Zhang X, Sun S, Chen R, Wang F (2007) Dramatic reduction of crop-to-crop gene flow within a short distance from transgenic rice fields. New Phytol 173:346–353. doi:10.1111/j.1469-8137.2006.01906.x
Sanchez Olguin ER, Arrieta-Espinoza G, Lobo JA, Espinoza-Esquivel AM (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 Res 18:633–647. doi:10.1007/s11248-009-9255-2
Stewart CN Jr, Halfhill MD, Warwick SI (2003) Transgene introgression from genetically modified crops to their wild relatives. Nat Rev Genet 4:806–817. doi:10.1038/nrg1179
Warwick SI, Beckie HJ, Hall LM (2009) Gene flow, invasiveness, and ecological impact of genetically modified crops. Ann NY Acad Sci 1168:72–99. doi:10.1111/j.1749-6632.2009.04576.x
Yang K, Jung S, Lee Y, Back K (2006) Modifying Myxococcus xanthus protoporphyrinogen oxidase to plant codon usage and high level of oxyfluorfen resistance in transgenic rice. Pest Biochem Physiol 86:186–194. doi:10.1016/j.pestbp.2006.04.003
Yao K, Hu N, Chen W, Li R, Yuan Q, Wang F, Qian Q, Jia S (2008) Establishment of a rice transgene flow model for predicting maximum distances of gene flow in southern China. New Phytol 180:217–228. doi:10.1111/j.1469-8137.2008.02555.x
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. Theor Appl Genet 115:549–560. doi:10.1007/s00122-007-0588-z
Zhang N, 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. doi:10.1023/A:1022371104679
Zhang W, Linscombe SD, Webster E, Tan S, Oard J (2006) Risk assessment of the transfer of imazethapyr herbicide tolerance from Clearfield rice to red rice (Oryza sativa). Euphytica 152:75–86. doi:10.1007/s10681-006-9180-x
Zhang W, Linscombe SD, Oard JH (2008) Genetic and agronomic analyses of red rice-Clearfield hybrids and their progeny produced from natural and controlled crosses. Euphytica 164:659–668. doi:10.1007/s10681-008-9661-1
Acknowledgments
We thank Dr. K. W. Kim at the Kyungpook National University for providing weedy rice seeds. This research was supported by grants from the KRIBB Research Initiative Program, the Crop Functional Genomics Center and the future based technology development program of the National Research Foundation (NRF) funded by the Korean government (MEST) (No. 2010-0002033).
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
About this article
Cite this article
Chun, Y.J., Kim, D.I., Park, K.W. et al. Gene flow from herbicide-tolerant GM rice and the heterosis of GM rice-weed F2 progeny. Planta 233, 807–815 (2011). https://doi.org/10.1007/s00425-010-1339-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-010-1339-y