Abstract
Four successive reciprocal backcrosses between F1 (obtained from wild Brassica juncea as maternal plants and transgenic glyphosate- or glufosinate-tolerant oilseed rape, B. napus, as paternal plants) or subsequent herbicide-tolerant backcross progenies and wild B. juncea were achieved by hand pollination to assess potential transgene flow. The third and forth reciprocal backcrosses produced a number of seeds per silique similar to that of self-pollinated wild B. juncea, except in plants with glufosinate-tolerant backcross progeny used as maternal plants and wild B. juncea as paternal plants, which produced fewer seeds per silique than did self-pollinated wild B. juncea. Germination percentages of reciprocal backcross progenies were high and equivalent to those of wild B. juncea. The herbicide-tolerant first reciprocal backcross progenies produced fewer siliques per plant than did wild B. juncea, but the herbicide-tolerant second or third reciprocal backcross progenies did not differ from the wild B. juncea in siliques per plant. The herbicide-tolerant second and third reciprocal backcross progenies produced an amount of seeds per silique similar to that of wild B. juncea except for with the glufosinate-tolerant first and second backcross progeny used as maternal plants and wild B. juncea as paternal plants. In the presence of herbicide selection pressure, inheritance of the glyphosate-tolerant transgene was stable across the second and third backcross generation, whereas the glufosinate-tolerant transgene was maintained, despite a lack of stabilized introgression. The occurrence of fertile, transgenic weed-like plants after only three crosses (F1, first backcross, second backcross) suggests a potential rapid spread of transgenes from oilseed rape into its wild relative wild B. juncea. Transgene flow from glyphosate-tolerant oilseed rape might be easier than that from glufosinate-tolerant oilseed rape to wild B. juncea. The original insertion site of the transgene could affect introgression.
Similar content being viewed by others
References
Ahloowalia BS (1971) Frequency, origin, and survival of aneuploids in tetraploid ryegrass. Genetica 42:129–138
Al Mouemar A, Darmency H (2004) Lack of stable inheritance of introgressed transgene from oilseed rape in wild radish. Environ Biosaf Res 3:209–214
Ammitzbøll H, Mikkelsen TN, Jørgensen RB (2005) Transgene expression and fitness of hybrids between GM oilseed rape and Brassica rapa. Environ Biosaf Res 4:3–12
Aono M, Wakiyama S, Nagatsu M, Nakajima N, Tamaoki M, Kubo A, Saji H (2006) Detection of feral transgenic oilseed rape with multiple-herbicide resistance in Japan. Environ Biosaf Res 5:77–87
Benabdelmouna A, Guèritaine G, Abirached-Darmency M, Darmency H (2003) Genome discrimination in progeny of interspecific hybrids between Brassica napus and Raphanus raphanistrum. Genome 46:469–472
Bing DJ, Downey RK, Rakow GFW (1991) Potential of gene transfer among oilseed Brassica and their weedy relatives. In: Proceedings of GCIRC 8th international rapeseed congress, Saskatoon, Canada, pp 1022–1027
Bing DJ, Downey RK, Rakow GFW (1996) Hybridization among Brassica napus, B. rapa and B. juncea and their two weedy relatives B. nigra and Sinapis arvensis under open pollination conditions in the field. Plant Breed 115:470–473
Campbell LG, Snow AA (2007) Competition alters life history and increase the relative fecundity of crop-wild radish hybrids (Raphanus spp.). New Phytol 173:648–660
Campbell DR, Waser NM (2001) Genotype-by-environment interaction and the fitness of plant hybrids in the wild. Evolution 55:669–676
Chapman MA, Burke JM (2006) Letting the gene out of the bottle: the population genetics of genetically modified crops. New Phytol 170:429–443
Chen LH, Wang XW, Zhang WJ, Zhang XD, Hu DF, Liu GT (1999) Transformation of common wheat (Triticum aestivum L.) with herbicide-resistant EPSPs gene. Acta Genet Sin 26:239–243
Chèvre AM, Eber F, Baranger A, Renard M (1997) Gene flow from transgenic crops. Nature 389:924
Chèvre AM, Eber F, Baranger A, Hureau G, Barret P, Picault H, Renard M (1998) Characterization of backcross generations obtained under field conditions from oilseed rape-wild radish F1 interspecific hybrids: an assessment of transgene dispersal. Theor Appl Genet 97:90–98
Chèvre AM, Adamczyk K, Eber F, Huteau V, Coriton O, Letanneur JC, Laredo C, Jenczewski E, Monod H (2007) Modelling gene flow between oilseed rape and wild radish. I. Evolution of chromosome structure. Theor Appl Genet 114:209–221
Dale PJ (1992) Spread of engineered genes to wild relatives. Plant Physiol 100:13–15
Darmency H, Fleury A (2000) Mating system in Hirschfeldia incana and hybridization to oilseed rape. Weed Res 40:231–238
Agbios GM database (2008) AGBIOS Canadian Company. http://www.agbios.com/dbase.php. Accessed 22 Sept 2008
FitzJohn RG, Armstrong TT, Newstrom-Lloyd LE, Wilton AD, Cochrane M (2007) Hybridisation within Brassica and allied genera: evaluation of potential for transgene escape. Euphytica 158:209–230
Frello SK, Hansen R, Jensen J, Jørgensen RB (1995) Inheritance of rapeseed (Brassica napus)-specific RAPD markers and a transgene in the cross B. juncea × (B. juncea × B. napus). Theor Appl Genet 91:236–241
Ge HX, Li ZY (2007) Intra- and intergenomic homology of B-genome chromosomes in trigenomic combinations of the cultivated Brassica species revealed by GISH analysis. Chromosome Res 15:849–861
Guan CY (1996) Comparative studies of inheritable character in Xinjiang wild rape and Sinapis arvensis L. Acta Agro Sin 22:214–219
Guan CY (2005) Transgenic breeding of oilseed rape. Chin J Oil Crop Sci 27:97–103
Guan CY, Li X (1997) Research and application of transgenic oilseed rape. J Cell Biol 19:18–23
Guèritaine G, Sester M, Eber F, Chèvre AM, Darmency H (2002) Fitness of backcross six of hybrids between transgenic oilseed rape (Brassica napus) and wild radish (Raphanus raphanistrum). Mol Ecol 11:1419–1426
Guo QY, Tu HL, Qiu XL, Xin Y (1998) Research on occurrence pattern and control technology of wild mustard. Sci Tech Qinghai Agric For 4:38–41
Hansen LB, Siegismund HR, Jørgensen RB (2001) Introgression between oilseed rape (Brassica napus L.) and its weedy relative B. rapa L. in a natural population. Genet Resour Crop Evol 48:621–627
Hansen LB, Siegismund HR, Jørgensen RB (2003) Progressive introgression between Brassica napus (oilseed rape) and B. rapa. Heredity 91:276–283
Hasterok R, Wolny E, Kulak S, Zdziechiewicz A, Maluszynska J, Heneen WK (2005) Molecular cytogenetic analysis of Brassica rapa–Brassica oleracea var. alboglabra monosomic addition lines. Theor Appl Genet 111:196–205
Hauser TP, Jørgensen RB, Ø stergard H (1998) Fitness of backcross and F2 hybrids between weedy Brassica rapa and oilseed rape (B. napus). Heredity 81:436–443
Hauser TP, Damgaard C, Jørgensen RB (2003) Frequency-dependent fitness of hybrids between oilseed rape (Brassica napus) and weedy B. rapa (Brassicaceae). Am J Bot 90:571–578
Hosaka K, Kianian SF, McGrath JM, Quiros CF (1990) Development and chromosomal localization of genome-specific DNA markers of Brassica and the evolution of amphidiploids and n = 9 diploid species. Genome 33(1):131–142
Huangfu CH, Song XL, Sheng Qiang, Zhang HJ (2007) Response of wild Brassica juncea populations to glyphosate. Pest Manage Sci 63:1133–1140
Jenczewski E, Ronfort J, Chèvre AM (2003) Crop-to-wild gene flow, introgression and possible fitness effects of transgenes. Environ Biosaf Res 2:9–24
Jørgensen RB, Anderson B (1994) Spontaneous hybridization between oilseed rape (Brassica napus) and weedy B. campestris (Brassicaceae): a risk of growing genetically modified oilseed rape. Am J Bot 81:1620–1626
Jørgensen RB, Anderson B, Landbo L, Mikkelsen TR (1996) Spontaneous hybridization between oilseed rape (Brassica napus) and weedy relatives. Acta Hortic 407:193–200
Jørgensen RB, Andersen B, Hauser TP, Lanbo L, Mikkelsen TR, Østergård H (1998) Introgression of crop genes from oilseed rape (Brassica napus) to related wild species—an avenue for the escape of engineered genes. Acta Hortic 459:211–217
Kawata M, Murakami K, Ishikawa T (2009) Dispersal and persistence of genetically modified oilseed rape around Japanese harbors. Environ Sci Pollut Res 16(2):120–126
Kerlan MC, Chèver AM, Eber F, Renard M (1992) Risk assessment of outcrossing of transgenic rapeseed related species: interspecific hybrid production under optimal condition with emphasis on pollination and fertilization. Euphytica 62:145–153
Kerlan MC, Chèver AM, Eber F (1993) Interspecific hybrids between a transgenic rapeseed (Brassica napus) and related species: cytogenetical characterization and detection of the transgene. Genome 36:1099–1106
Kling J (1996) Could transgenic super crops one day breed super weeds? Science 274:180–181
Leflon M, Eber F, Letanneur JC, Chelysheva L, Canton O, Huteau V, Ryder CD, Barker G, Jenczewski E, Chèvre AM (2006) Pairing and recombination at meiosis of Brasscia rapa (AA) × Brassica napus (AACC) hybrids. Theor Appl Genet 113:1467–1480
Lefol E, Sèguin-Swartz G, Downey RK (1997) Sexual hybridisation in crosses of cultivated Brassica species with the crucifers Erucatrum gallicum and Raphanus raphanistrum: potential for gene introgression. Euphytica 95:127–139
Lègère A (2005) Risks and consequences of gene flow from herbicide-resistant crops: canola (Brassica napus L.) as a case study. Pest Manage Sci 61:292–300
Lu CM, Xiao L, Wu YH (2005) Ecological risk assessment of transgenic rapeseed in China. J Agric Biotechnol 13:267–275
Mercer KL, Andow DA, Wyse DL, Shaw RG (2007) Stress and domestication traits increase the relative fitness of crop-wild hybrids in sunflower. Ecol Lett 10:383–393
Metz PLJ, Nap JP, Stiekema WJ (1995) Hybridization of radish (Raphanus sativus L.) and oilseed rape (Brassica napus L.) through a flower-culture method. Euphytica 83:159–168
Metz PLJ, Jacobsen E, Nap JP, Pereira A, Stiekema WJ (1997) The impact on biosafety of the phosphinothricin-tolerant transgene in inter-specific B. rapa × B. napus hybrids and their successive backcrosses. Theor Appl Genet 95:442–450
Neve P (2007) Challenges for herbicide resistance evolution and management: 50 years after Harper. Weed Res 47:365–369
Pan LW, Chen JH, Shen YF, Hu YQ, Tao J, Han W (2001) Detection comparison of CP4 EPSP gene from genetically modified roundup ready rape seed and soybean. Lett Biotechnol 12:175–207
Pu HM (2003) Transgenetic herbicide-tolerant oilseed rape and its ecological security. Chin J Oil Crop Sci 25:89–92
Pu HM, Gao JQ, Qi CK, Zhang JF, Chen XJ, Fu SZ (2003) Inheritance of herbicide resistance in Brassica napus and its utilization. Jiangsu J Agric Sci 19:81–86
Pu HM, Qi CK, Zhang JF, Fu SZ, Gao JQ, Chen XJ, Zhao XX (2005) The studies on gene flow from GM herbicide-tolerant rapeseed to cruciferous weeds. Acta Ecol Sin 25:910–916
Rieger MA, Potter TD, Preston C, Powles SB (2001) Hybridization between Brassica napus L. and Raphanus raphanistrum L. under agronomic field conditions. Theor Appl Genet 103:555–560
Roy NN (1984) Interspecific transfer of Brassica juncea-type high blackleg resistance to Brassica napus. Euphytica 33:295–303
Scheffler, Dale (1994) Opportunities for gene transfer from transgenic oilseed rape (Brassica napus) to related species. Transgenic Res 3:263–278
Snow AA, Anderson B, Jørgensen RB (1999) Costs of transgenic herbicide resistance introgressed from Brassica napus into weedy B. rapa. Mol Ecol 8:605–615
Song XL, Qiang S (2003) Sexual compatibility of three species of oilseed rape(Brassica Spp.) with wild rapes (B. juncea var. gracilis Tsen et Lee) and the fitness of F1—potential for gene transfer. Chin J Appl Environ Biol 9:357–361
Song XL, Huangpfu CH, Qiang S (2007) Gene flow from transgenic glufosinate- or glyphosate-tolerant oilseed rape to wild rape. J Plant Ecol 31:729–737
Tomiuk J, Hauser Tp, Jørgensen RB (2000) A- or C-chromosomes, does it matter for the transfer of transgenes from Brassica napus. Theor Appl Genet 100:750–754
Town CD, Cheung F, Maiti R, Crabtree J, Haas BJ, Wortman JR, Hine EE, Althoff R, Arbogast TS, Tallon LJ, Vigouroux M, Trick M, Bancroft L (2006) Comparative genomics of Brassica oleracea and Arabidopsis thaliana reveal gene loss, fragmentation, and dispersal after polyploidy. Plant Cell 18:1348–1359
Vacher C, Weis AE, Hermann D, Kossler T, Young C, Hochberg M (2004) Impact of ecological factors on the initial invasion of Bt transgenes into wild populations of birdseed rape (Brassica rapa). Theor Appl Genet 109:806–814
Wang XF, Wang HZ, Liu GH, Hu ZL, Zhen YB (2005) Transgenic hybrid parents in Brassica napus transformed with bivalent genes for resistance to Sclerotinia sclerotiorum. Chin Bull Bot 22:292–301
Warwich SI, Simard MJ, Lègère A, Beckie HJ, Braun L, Zhu B, Mason P, Sègain-swartz G, Stewart CN (2003) Hybridization between transgenic Brassica napus L. and its wild relatives: Brassica rapa L., Raphanus raphanistrum L., Sinapis arvensis L., and Erucastrum gallicum (Wild.) O. F. Schulz. Theor Appl Genet 107:528–539
Warwick SI, Legere A, Sinard MJ, James T (2008) Do escaped transgenes persist in nature? The case of an herbicide resistance transgene in a weedy Brassica rapa population. Mol Ecol 17:1387–1395
Whitney KD, Randell RA, Rieseberg LH (2006) Adaptive introgression of herbivore resistance traits in weedy sunflower Helianthus annuus. Am Nat 167:794–807
Yang TJ, Kim JS, Kwon SJ, Lim KB, Choi BS, Kim JA, Jin M, Park JY, Lim MH, Kim H, Lim YP, Kang JJ, Hong JH, Kim CB, Bhak J, Bancroft I, Park BS (2006) Sequence-level analysis of the diploidization process in the triplicated flowering locus C region of Brassica rapa. Plant Cell 18:1339–1347
Yoshimura Y, Beckie HJ, Matsuo K (2006) Transgenic oilseed rape along transportation routes and port of Vancouver in western Canada. Environ Biosaf Res 5:67–75
Zhu B, Lawrence JR, Warwick SI, Mason P, Braun L, Halfhill MD, Stewart CN (2004) Stable Bacillus thuringiensis (Bt) toxin content in interspecific F1 and backcross populations of wild Brassica rapa after Bt gene transfer. Mol Ecol 13:237–241
Acknowledgments
This research was financially supported by the National Basic Research and Development Program (2007CB109202) and the National Natural Science Foundation of China (30400059). We express our deep appreciation to Dr. Robert E. Blackshaw, Suzanne Warwick, Yong Woong Kwon and Tae Jin Yang for their valuable comments on this manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by A. Bervillé.
Rights and permissions
About this article
Cite this article
Song, X., Wang, Z., Zuo, J. et al. Potential gene flow of two herbicide-tolerant transgenes from oilseed rape to wild B. juncea var. gracilis . Theor Appl Genet 120, 1501–1510 (2010). https://doi.org/10.1007/s00122-010-1271-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-010-1271-3