Ecological geneticsEcological geneticsЭкологическая генетика1811-09322411-9202Eco-Vector248210.17816/ecogen132100-117ArticlesСтатьиResearch ArticleAssessment of hybridization propensity between genetically modified oilseed rape and nontransgenic relativesОценка возможности гибридизации генетически модифицированного рапса с родственными нетрансгенными растениямиMikhaylovaElena VladimirovnaМихайловаЕлена Владимировна

Postgraduate, assistant, faculty of biology, ecology department

аспирант, ассистент, кафедра экологии биологического факультета

mikhele@list.ruKuluevBulat RazyapovichКулуевБулат Разяпович

Senior Researcher, laboratory of molecular biology and nanobiotechnology

старший научный сотрудник, лаборатория молекулярной биологии и нанобиотехнологии

Kuluev@bk.ruKhaziakhmetovRashit MukhametovichХазиахметовРашит Мухаметович

Doctor of biological sciences, professor, faculty of biology, ecology department

д. б. н., профессор, кафедра экологии биологического факультета

eco3110@rambler.ruBashkir State UniversityБашкирский Государственный УниверситетInstitute of Biochemistry and genetics, Ufa Sci. Center of RASИнститут биохимии и генетики Уфимского научного центра РАН15062015132VOL 13, NO2 (2015)ТОМ 13, №2 (2015)10011730032016Copyright ©; 2015, Mikhaylova E.V., Kuluev B.R., Khaziakhmetov R.M.Copyright ©; 2015, Михайлова Е.В., Кулуев Б.Р., Хазиахметов Р.М.2015Mikhaylova E.V., Kuluev B.R., Khaziakhmetov R.M.Михайлова Е.В., Кулуев Б.Р., Хазиахметов Р.М.http://creativecommons.org/licenses/by/4.0https://journals.eco-vector.com/ecolgenet/article/view/2482

The lack of knowledge about the impact on ecosystems restricts the expansion of genetically modified plants. We review the potential gene flow into the environment due to the cultivation of transgenic oilseed rape. The problem is immediate for this crop on the ground of the widespread of its allogamous weedy relatives. The main difficulty in risk assessment is caused by fluctuation in hybridization frequencies depending on the transgenes used, crop’s line and population features and also the imperfection of current methods of molecular diagnostics. For minimization of such risks, preliminary investigation of cross-pollination, inheritance, expression and phenotypical effects of transgenes in hybrids with both wild and domestic relatives is recommended in all regions where GM-crops are going to be grown. On the basis of this data, specific measures and recommendations to prevent gene flow can be developed. Domestic GM-crop lines, properly tested in local ecosystems, can be grown without any environmental threat.

Недостаточная изученность влияния на экосистемы генетически модифицированных растений препятствует их широкому распространению. В статье рассмотрены вероятности распространения трансгенов в окружающей среде при возделывании трансгенного рапса. Проблема особенно актуальна для этой культуры, так как сорные дикие родственники рапса, размножающиеся перекрестным опылением, встречаются повсеместно. Особую сложность при оценке возможности распространения трансгенов в природе вызывают колебания в частоте скрещивания с родственными растениями в зависимости от привнесенных генов, линии трансгенного растения и особенностей дикой популяции, а также несовершенство современных методов молекулярной диагностики. В регионах, где планируется выращивание ГМ-культур, рекомендуется заблаговременно проводить исследования переопыления, а также процессов наследования, экспрессии и фенотипических проявлений трансгенов в гибридах как с дикорастущими, так и с культурными растениями, а затем на основе полученных данных разрабатывать конкретные меры и рекомендации по предотвращению попадания трансгенов в окружающую среду. Отечественные сорта, протестированные в местных экосистемах, могли бы стать экологически безопасными.

Brassica napusBrassica napuscanolaoilseed rapegenetically modified plantsGM cropscross-pollinationрапсгенетически модифицированные растенияГМ-сортапереопылениеЗыбалов В. С. (2002) Рапс как адаптивная кормовая культура на Южном Урале. Кормопроизводство. № 3: C.19-21.Зыбалов В. С., Миркин Б. М. (2002) Управление функцией агроценозов. Роль промежуточных посевов и поликультур. Сельскохозяйственная биология. № 1 С. 3-10.Куликов А. М. (2005) Генетически-модифицированные организмы и риски их использования. Физиология растений. Т. 52. № 1: С. 115-128.Allainguillaume J., Alexander M., Bullock J. M. et al. (2006) Fitness of hybrids between rapeseed (Brassica napus) and wild Brassica rapa in natural habitats. Molecular Ecology. V. 15 (4): P. 1175-1184.Aono M., Wakiyama S., Nagatsu M. et al. (2011) Seeds of a possible natural hybrid between herbicide-resistant Brassica napus and Brassica rapa detected on a riverbank in Japan. GM crops. V. 2 (3): P. 201-210.Beckie H. J., Warwick S. I., Nair H., Seguin-Swartz G. (2003) Gene flow in commercial fields of herbicide-resistant canola (Brassica napus). Ecological applications. V. 13 (5): P. 1276-1294.Bing D. J., Downey R. K., Rakow G. F. W. (1996) Hybridizations 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 Breeding. V. 115 (6): P. 470-473.Chevre A. M. Eber F., Baranger A. et al. (1994) Interspecific gene flow as a component of risk assessment for transgenic Brassicas. ISHS Brassica Symposium-IX Crucifer Genetics Workshop 407: P. 169-180.Chevre A. M., Eber F., Darmency H. et al. (2000) Assessment of interspecific hybridization between transgenic oilseed rape and wild radish under normal agronomic conditions. Theoretical and Applied Genetics. V. 100 (8): P. 1233-1239.Chevre A. M., Adamczyk K., Eber F. et al. (2007) Modelling gene flow between oilseed rape and wild radish. I. Evolution of chromosome structure. Theoretical and Applied Genetics. V. 114 (2): P. 209-221.Chiang M. S., Chiang B. Y., Grant W. F. (1977) Transfer of resistance to race 2 of Plasmodiophora Brassicae from Brassica napus to cabbage (B. oleracea var. Capitata). Interspecific hybridization between B. napus and B. oleracea var. Capitata. Euphytica. V. 26 (2): P. 319-336.Culpepper A. S., Whitaker J. R., MacRae A. W., York A. C. (2008) Distribution of glyphosate-resistant Palmer amaranth (Amaranthus palmeri) in Georgia and North Carolina during 2005 and 2006. J. Cotton Sci. V. 12: P. 306-310.Crawley M. J., Hails R. S., Rees M. et al. (1993) Ecology of transgenic oilseed rape in natural habitats. Nature. V. 363 (6430): P. 620-623.Crawley M. J., Brown S. L., Hails R. et al. (2001) Transgenic crops in natural habitats. Nature. V. 409 (6821): P.682-683.Daniels R., Boffey C., Mogg R. et al. (2005) The potential for dispersal of herbicide tolerance genes from genetically-modified, herbicide tolerant oilseed rape crops to wild relatives. Final report to DEFRA, contract reference EPG. V. 20 (5): P. 245-252.Darmency H., Lefol E., Fleury A. (1998) Spontaneous hybridizations between oilseed rape and wild radish. Molecular Ecology. V. 7 (11): P. 1467-1473.Darmency H., Fleury A. (2000) Mating system in Hirschfeldia incana and hybridization to oilseed rape. Weed Research (Oxford). V. 40 (2): P. 231-238.Devos Y., Reheul D., Schrijver A. D. et al. (2004) Management of herbicide-tolerant oilseed rape in Europe: a case study on minimizing vertical gene flow. Environmental biosafety research. V. 3 (03): P. 135-148.Devos Y., De Schrijver A., Reheul D. (2009) Quantifying the introgressive hybridisation propensity between transgenic oilseed rape and its wild/weedy relatives. Environmental monitoring and assessment. V. 149 (1-4): P. 303-322.Di K., Stewart C. N., Wei W. et al. (2009) Fitness and maternal effects in hybrids formed between transgenic oilseed rape (Brassica napus L.) and wild brown mustard (B. juncea (L.) Czern et Coss.) in the field. Pest management science. V. 65 (7): P. 753-760.Eastham K., Sweet J. (2002) Genetically modified organisms (GMOs): The significance of gene flow through pollen transfer. Copenhagen, Denmark: European Environment Agency. P.1-74.Ellstrand N. C. (2001) When transgenes wander, should we worry? Plant Physiology. V. 125 (4): P. 1543-1545.FitzJohn R. G., Armstrong T. T., Newstrom-Lloyd L. E. et al. (2007) Hybridisation within Brassica and allied genera: evaluation of potential for transgene escape. Euphytica. V. 158 (1-2): P. 209-230.Ford C. S., Allainguillaume J., Grilli-Chantler P. et al. (2006) Spontaneous gene flow from rapeseed (Brassica napus) to wild Brassica oleracea. Proceedings of the Royal Society B: Biological Sciences. V. 273 (1605): P. 3111-3115.Friesen L. F., Nelson A. G., Van Acker R. C. (2003) Evidence of contamination of pedigreed canola seedlots in Western Canada with genetically engineered herbicide resistance traits. Agronomy Journal. V. 95 (5): P. 1342-1347.Gassmann A. J., Petzold-Maxwell J. L., Clifton E. H. et al. (2014) Field-evolved resistance by western corn rootworm to multiple Bacillus thuringiensis toxins in transgenic maize. Proceedings of the National Academy of Sciences. V. 111 (14): P. 5141-5146.Gepts P., Papa R. (2010) Possible effects of (trans) gene flow from crops on the genetic diversity from landraces and wild relatives. Environmental biosafety research. V. 2 (2): P. 89.Gruber S., Hüsken A., Dietz-Pfeilstetter A. et al. (2012) Biological Confinement Strategies for Seed-and Pollen-Mediated Gene Flow of GM Canola (Brassica napus L.). AgBioForum. V. 15 (1): P. 44-53.Gueritaine G., Sester M., Eber F. et al. (2002) Fitness of backcross six of hybrids between transgenic oilseed rape (Brassica napus) and wild radish (Raphanus raphanistrum). Molecular Ecology. V. 11: P. 1419-1426.Halfhill M., Raymer P., Stewart C. Jr. (2002) Bt-transgenic oilseed rape hybridization with its weedy relative, Brassica rapa. Environmental Biosafety Research. V. 1 (1): P. 19-28.Halfhill M. D., Zhu B., Warwick S. I. et al. (2004) Hybridization and backcrossing between transgenic oilseed rape and two related weed species under field conditions. Environmental Biosafety Research. V. 3 (02): P. 73-81.Hall L., Topinka K., Huffman J. et al. (2000) Pollen flow between herbicide-resistant Brassica napus is the cause of multiple-resistant B. napus volunteers. Weed Science. V. 48 (6): P. 688-694.Heenan P. B., Dawson M. I., Fitzjohn R. G., Stewart A. V. (2007) Experimental hybridisation of Brassica species in New Zealand. New Zealand Journal of Botany. V. 45 (1): P. 53-66.Hoyle M., Hayter K., Cresswell J. E. (2007) Effect of pollinator abundance on self-fertilization and gene flow: application to GM canola. Ecological Applications. V. 17 (7): P. 2123-2135.Huiming P. U., Cunkou Q. I., Jiefu Z. H. A. N. G. et al. (2007) Studies on gene flow from GM herbicide-tolerant rapeseed (B. napus) to other species of crucifers. Proceedings of the 12th International Rapeseed Congress. P. 79-81.Husken A., Dietz-Pfeilstetter A. (2007) Pollen-mediated intraspecific gene flow from herbicide resistant oilseed rape (Brassica napus L.). Transgenic Research. V. 16 (5): P. 557-569.ISAAA's GM Approval Database. Updated 26.01.2015. URL: http://www.isaaa.org/gmapprovaldatabase/.James Clive. (2013) Global Status of Commercialized Biotech/GM Crops: 2013 // ISAAA Brief. ISAAA: Ithaca, NY. N 46.James Clive. (2014) Global Status of Commercialized Biotech/GM Crops: 2014 // ISAAA Brief. ISAAA: Ithaca, NY. N 49.Jorgensen R. B., Andersen B., Landbo L., Mikkelsen T. R. (1996) Spontaneous hybridization between oilseed rape (Brassica napus) and weedy relatives. Acta Horticulturae. V. 407: P. 193-200.Knispel A. L., McLachlan S. M., Van Acker R. C., Friesen L. F. (2008) Gene flow and multiple herbicide resistance in escaped canola populations. Weed Science. V. 56 (1): P. 72-80.Lefol E., Fleury A., Darmency H. (1996) Gene dispersal from transgenic crops. Sexual plant reproduction. V. 9 (4): P.189-196 (a).Lefol E., Danielou V., Darmency H. (1996) Predicting hybridization between transgenic oilseed rape and wild mustard. Field Crops Research. V. 45 (1): P. 153-161 (b).Lefol E., Seguin-Swartz G., Downey R. K. (1997) Sexual hybridisation in crosses of cultivated Brassica species with the crucifers Erucastrum gallicum and Raphanus raphanistrum: potential for gene introgression. Euphytica. V. 95 (2): P. 127-139.Liu Y. B., Wei W., Ma K. P., Darmency, H. (2010) Backcrosses to Brassica napus of hybrids between B. juncea and B. napus as a source of herbicide-resistant volunteer-like feral populations. Plant Science. V. 179 (5): P. 459-465.Londo J. P., Bollman M. A., Sagers C. L. et al. (2011) Glyphosate drift but not herbivory alters the rate of transgene flow from single and stacked trait transgenic canola (Brassica napus) to nontransgenic B. napus and B. rapa. New Phytologist. V. 191 (3): P. 840-849.Lu B. R., Snow A. A. (2005) Gene flow from genetically modified rice and its environmental consequences. BioScience. V. 55 (8): P. 669-678.Millwood, R. J. (2011) Consequences of gene flow and transgene introgression in hybrids between transgenic Brassica napus and its weedy wild relative Brassica rapa. Master's Thesis, University of Tennessee.Moyes C. L., Lilley J. M., Casais C. A. et al. (2002) Barriers to gene flow from oilseed rape (Brassica napus) into populations of Sinapis arvensis. Molecular Ecology. V. 11 (1): P. 103-112.Pallett D. W., Huang L., Cooper J. I., Wang H. (2006) Within population variation in hybridisation and transgene transfer between wild Brassica rapa and Brassica napus in the UK. Annals of applied biology. V. 148 (2): P. 147-155.Pu H. M., Qi C. K., Zhang J. F. et al. (2005) Studies on the gene flow from herbicide-tolerant GM rapeseed to its close relative crops. Acta Ecologica Sinica. V. 25: P. 581-588.Que Q., Chilton M. D. M., de Fontes C. M. et al. (2010) Trait stacking in transgenic crops: Challenges and opportunities. GM Crops. V. 1 (4): P. 220-229.Rieger M. A., Potter T. D., Preston C., Powles S. B. (2001) Hybridization between Brassica napus L and Raphanus raphanistrum L under agronomic field conditions. Theor Appl Genet. V. 103: P. 555-560.Rieger M. A., Lamond M., Preston C. et al. (2002) Pollen-mediated movement of herbicide resistance between commercial canola fields. Science (Washington). V. 296: P. 2386-2388.Rieseberg L. H., Kim S. C., Randell R. A. et al. (2007) Hybridization and the colonization of novel habitats by annual sunflowers. Genetica. 2007. V. 129 (2): P. 149-165.Saji H., Nakajima N., Aono M. (2005) Monitoring the escape of transgenic oilseed rape around Japanese ports and roadsides. Environment Biosafety Research. V. 4 (4): P. 217-222.Schafer M. G., Ross A. A., Londo J. P. et al. (2011) The Establishment of Genetically Engineered Canola Populations in the U. S. PLoS ONE. V. 6 (10): e25736. doi:10.1371/journal.pone.0025736.Scheffler J. A., Dale P. J. (1994) Opportunities for gene transfer from transgenic oilseed rape (Brassica napus) to related species. Transgenic research. V. 3 (5): P. 263-278.Scott S. E., Wilkinson M. J. (1998) Transgene risk is low. Nature. V. 393: P. 320.Scott S. E., Wilkinson M. J. (1999) Low probability of chloroplast movement from oilseed rape (Brassica napus) into wild Brassica rapa. Nature biotechnology. V. 17 (4): P. 390-392.Shen B. C., Stewart C. N., Zhang M. Q. et al. (2006) Correlated expression of gfp and Bt cry1Ac gene facilitates quantification of transgenic hybridization between Brassicas. Plant Biology. V. 8 (5): P.723-730.Simard M. J., Legere A., Warwick S. I. (2006) Transgenic Brassica napus fields and Brassica rapa weeds in Quebec: sympatry and weed-crop in situ hybridization. Botany. V. 84 (12): P. 1842-1851.Song X., Wang Z., Zuo J. et al. (2010) Potential gene flow of two herbicide-tolerant transgenes from oilseed rape to wild B. juncea var. gracilis. Theoretical and applied genetics. V. 120 (8): P. 1501-1510.Staniland B. K., McVetty P. B., Friesen L. F. et al. (2000) Effectiveness of border areas in confining the spread of transgenic Brassica napus pollen. Canadian journal of plant science. V. 80 (3): P. 521-526.Stewart C. N., Halfhill M. D., Warwick S. I. (2003) Transgene introgression from genetically modified crops to their wild relatives. Nature Reviews Genetics. V. 4 (10): P. 806-817.Tabashnik B. E. Carriere Y., Dennehy T. J. et al. (2003) Insect resistance to transgenic Bt crops: lessons from the laboratory and field. Journal of economic entomology. V. 96 (4): P. 1031-1038.Tsuda M., Okuzaki A., Kaneko Y., Tabei Y. (2012) Relationship between hybridization frequency of Brassica juncea × B. napus and distance from pollen source (B. napus) to recipient (B. juncea) under field conditions in Japan. Breeding science. V. 62 (3): P. 274.Warwick S I., Simard M. J., Legere A. et al. (2003) Hybridization between transgenic Brassica napus L and its wild relatives: B rapa L, Raphanus raphanistrum L, Sinapis arvensis L and Erucastrum gallicum (Willd) OE Schulz. Theor Appl Genet. V. 107: P. 528-539.Warwick S. I., Legere A., Simard M. J., James T. (2008) Do escaped transgenes persist in nature? The case of an herbicide resistance transgene in a weedy Brassica rapa population. Molecular Ecology. V. 7 (5): P. 1387-1395.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. V. 1168 (1): P. 72-99.Wilkinson M. J., Elliott L. J., Allainguillaume J. et al. (2003) Hybridization between Brassica napus and B. rapa on a national scale in the United Kingdom. Science. V. 302 (5644): P. 457-459.Wolf D. E., Takebayashi N., Rieseberg L. H. (2001) Predicting the risk of extinction through hybridization. Conservation Biology. V. 15 (4): P.1039-1053.Zhao X. X., Lu W. P., Qi C. K. et al. (2005) Assessment on alien herbicide-resistant gene flow among crucifers by sexual compatibility. Chinese Science Bulletin. V. 50 (15): P. 1605-1612.Zou J., Fu D., Gong H. et al. (2011) De novo genetic variation associated with retrotransposon activation, genomic rearrangements and trait variation in a recombinant inbred line population of Brassica napus derived from interspecific hybridization with Brassica rapa. The Plant Journal. V. 68 (2): P. 212-224.