Gene Flow, Invasiveness, and Ecological Impact of Genetically Modified Crops
Abstract
The main environmental concerns about genetically modified (GM) crops are the potential weediness or invasiveness in the crop itself or in its wild or weedy relatives as a result of transgene movement. Here we briefly review evidence for pollen‐ and seed‐mediated gene flow from GM crops to non‐GM or other GM crops and to wild relatives. The report focuses on the effect of abiotic and biotic stress‐tolerance traits on plant fitness and their potential to increase weedy or invasive tendencies. An evaluation of weediness and invasive traits that contribute to the success of agricultural weeds and invasive plants was of limited value in predicting the effect of biotic and abiotic stress‐tolerance GM traits, suggesting context‐specific evaluation rather than generalizations. Fitness data on herbicide, insect, and disease resistance, as well as cold‐, drought‐, and salinity‐tolerance traits, are reviewed. We describe useful ecological models predicting the effects of gene flow and altered fitness in GM crops and wild/weedy relatives, as well as suitable mitigation measures. A better understanding of factors controlling population size, dynamics, and range limits in weedy volunteer GM crop and related host or target weed populations is necessary before the effect of biotic and abiotic stress‐tolerance GM traits can be fully assessed.
Number of times cited according to CrossRef: 75
- Sara L. Martin, Beatriz E. Lujan‐Toro, Connie A. Sauder, Tracey James, Sara Ohadi and Linda M. Hall, Hybridization rate and hybrid fitness for Camelina microcarpa Andrz. ex DC (♀) and Camelina sativa (L.) Crantz(Brassicaceae) (♂), Evolutionary Applications, 12, 3, (443-455), (2018).
- Patrick J. Bigelow, Wayne Loescher, James F. Hancock and Rebecca Grumet, Influence of intergenotypic competition on multigenerational persistence of abiotic stress resistance transgenes in populations of Arabidopsis thaliana, Evolutionary Applications, 11, 6, (950-962), (2018).
- Amit Jhala, Debalin Sarangi, Parminder Chahal, Ashish Saxena, Muthukumar Bagavathiannan, Bhagirath Chauhan and Prashant Jha, Inter-specific Gene Flow from Herbicide-Tolerant Crops to their Wild Relatives, Biology, Physiology and Molecular Biology of Weeds, 10.1201/9781315121031-7, (87-122), (2017).
- B. R. Kuluev, E. V. Mikhaylova, R. M. Taipova and A. V. Chemeris, Changes in phenotype of transgenic amaranth Amaranthus retroflexus L., overexpressing ARGOS-LIKE gene, Russian Journal of Genetics, 53, 1, (67), (2017).
- Vernie G. Sagun and Carol Auer, Pollen morphology of selected Camelineae (Brassicaceae), Palynology, 41, 2, (255), (2017).
- Aristidis M. Tsatsakis, Muhammad Amjad Nawaz, Demetrios Kouretas, Georgios Balias, Kai Savolainen, Victor A. Tutelyan, Kirill S. Golokhvast, Jeong Dong Lee, Seung Hwan Yang and Gyuhwa Chung, Environmental impacts of genetically modified plants: A review, Environmental Research, 10.1016/j.envres.2017.03.011, 156, (818-833), (2017).
- Khaled Moustafa, Joanna Cross and Seif Gasim, Food and starvation: is Earth able to feed its growing population?, International Journal of Food Sciences and Nutrition, (1), (2017).
- JA Thompson, AJ Stow and DA Raftos, Lack of genetic introgression between wild and selectively bred Sydney rock oysters Saccostrea glomerata, Marine Ecology Progress Series, 10.3354/meps12109, 570, (127-139), (2017).
- Ana Picanço, Artur Gil, François Rigal and Paulo A.V. Borges, Pollination services mapping and economic valuation from insect communities: a case study in the Azores (Terceira Island), Nature Conservation, 18, (1), (2017).
- Reginald J. Millwood, Hong S. Moon, Charleson R. Poovaiah, Balasubramaniam Muthukumar, John Hollis Rice, Jason M. Abercrombie, Laura L. Abercrombie, William Derek Green and Charles Neal Stewart, Engineered selective plant male sterility through pollen‐specific expression of the EcoRI restriction endonuclease, Plant Biotechnology Journal, 14, 5, (1281-1290), (2015).
- Miguel A. Sánchez, Pablo Cid, Humberto Navarrete, Carlos Aguirre, Gustavo Chacón, Erika Salazar and Humberto Prieto, Outcrossing potential between 11 important genetically modified crops and the Chilean vascular flora, Plant Biotechnology Journal, 14, 2, (625-637), (2015).
- Hui Xia, Hongbin Zhang, Wei Wang, Xiao Yang, Feng Wang, Jun Su, Hanbing Xia, Kai Xu, Xingxing Cai and Bao‐Rong Lu, Ambient insect pressure and recipient genotypes determine fecundity of transgenic crop‐weed rice hybrid progeny: Implications for environmental biosafety assessment, Evolutionary Applications, 9, 7, (847-856), (2016).
- Titus Magomere, Silas Obukosia, Mark Albertsen, Florence Wambugu, Daniel Kamanga, Michael Njuguna, Jim Gaffney, Zuo-Yu Zhao, Ping Che, Antony Aseta, Esther Kimani and Evans Mwasame, Evaluation of fitness in F 2 generations of Africa Biofortified Sorghum event 188 and weedy Sorghum bicolor ssp. drummondii, Electronic Journal of Biotechnology, 22, (52), (2016).
- Henri Darmency, Consequences of Gene Flow between Transgenic, Insect-Resistant Crops and Their Wild Relatives, Genetically Modified Organisms in Food, 10.1016/B978-0-12-802259-7.00037-3, (423-430), (2016).
- Chanjuan Liang, Genetically Modified Crops with Drought Tolerance: Achievements, Challenges, and Perspectives, Drought Stress Tolerance in Plants, Vol 2, 10.1007/978-3-319-32423-4_19, (531-547), (2016).
- Oz Barazani, Alexandra Keren-Keiserman, Erik Westberg, Nir Hanin, Arnon Dag, Giora Ben-Ari, Ori Fragman-Sapir, Yizhar Tugendhaft, Zohar Kerem and Joachim W. Kadereit, Genetic variation of naturally growing olive trees in Israel: from abandoned groves to feral and wild?, BMC Plant Biology, 16, 1, (2016).
- Thomas A. McKeon, Douglas G. Hayes, David F. Hildebrand and Randall J. Weselake, Introduction to Industrial Oil Crops, Industrial Oil Crops, 10.1016/B978-1-893997-98-1.00001-4, (1-13), (2016).
- Sara L. Martin, Connie A. Sauder, Tracey James, Kyle W. Cheung, Fakhria M. Razeq, Paul Kron and Linda Hall, Sexual hybridization between Capsella bursa‐pastoris (L.) Medik (♀) and Camelina sativa (L.) Crantz (♂) (Brassicaceae), Plant Breeding, 134, 2, (212-220), (2015).
- S. H. Luijten, N. S. Schidlo, P. G. Meirmans and T. J. Jong, Hybridisation and introgression between Brassica napus and B. rapa in the Netherlands, Plant Biology, 17, 1, (262-267), (2014).
- O. Magomere Titus, K. Ngugi Eliud, D. Obukosia Silas, Mutitu Eunice and I. Shibairo Solomon, The population structure of wild sorghum species in agro-ecological zones of Western Kenya, African Journal of Biotechnology, 14, 17, (1475), (2015).
- Kensuke Katsuta, Kazuhito Matsuo, Yasuyuki Yoshimura and Ryo Ohsawa, Long-term monitoring of feral genetically modified herbicide-tolerant Brassica napus populations around unloading Japanese ports, Breeding Science, 65, 3, (265), (2015).
- Kyle W. Cheung, Fakhria M. Razeq, Connie A. Sauder, Tracey James and Sara L. Martin, Bidirectional but asymmetrical sexual hybridization between Brassica carinata and Sinapis arvensis (Brassicaceae), Journal of Plant Research, 10.1007/s10265-015-0702-2, 128, 3, (469-480), (2015).
- Jochen Graw, Veränderungen im Genom: Mutationen, Genetik, 10.1007/978-3-662-44817-5_10, (399-458), (2015).
- Menachem Moshelion and Arie Altman, Current challenges and future perspectives of plant and agricultural biotechnology, Trends in Biotechnology, 10.1016/j.tibtech.2015.03.001, 33, 6, (337-342), (2015).
- , Scientific advice to the European Commission on the internal review submitted under Regulation (EC) No 1367/2006 on the application of the provisions of the Aarhus Convention against the Commission Implementing Decision 2015/687 to authorise genetically modified oilseed rape MON88302, EFSA Supporting Publications, 12, 8, (2015).
- Olena Kalinina, Simon L. Zeller and Bernhard Schmid, Persistence of seeds, seedlings and plants, performance of transgenic wheat in weed communities in the field and effects on fallow weed diversity, Perspectives in Plant Ecology, Evolution and Systematics, 10.1016/j.ppees.2015.09.005, 17, 6, (421-433), (2015).
- , Statement on a conceptual framework for the risk assessment of certain food additives re‐evaluated under Commission Regulation (EU) No 257/2010, EFSA Journal, 12, 6, (2014).
- , Scientific Opinion on application (EFSA‐GMO‐BE‐2011‐101) for the placing on the market of herbicide‐tolerant genetically modified oilseed rape MON 88302 for food and feed uses, import and processing under Regulation (EC) No 1829/2003 from Monsanto, EFSA Journal, 12, 6, (2014).
- Geoffrey Barrows, Steven Sexton and David Zilberman, Agricultural Biotechnology: The Promise and Prospects of Genetically Modified Crops, Journal of Economic Perspectives, 28, 1, (99), (2014).
- Gerhart U Ryffel, Transgene flow: Facts, speculations and possible countermeasures, GM Crops & Food, 10.4161/21645698.2014.945883, 5, 4, (249-258), (2014).
- Andrew Roberts, Yann Devos, Alan Raybould, Patrick Bigelow and Alan Gray, Environmental risk assessment of GE plants under low-exposure conditions, Transgenic Research, 23, 6, (971), (2014).
- Weng Hui Liew, Mimi H. Hassim and Denny K.S. Ng, Review of evolution, technology and sustainability assessments of biofuel production, Journal of Cleaner Production, 10.1016/j.jclepro.2014.01.006, 71, (11-29), (2014).
- Jing Ding, Hui Duan, Ziniu Deng, Degang Zhao, Ganjun Yi, Richard McAvoy and Yi Li, Molecular Strategies for Addressing Gene Flow Problems and Their Potential Applications in Abiotic Stress Tolerant Transgenic Plants, Critical Reviews in Plant Sciences, 33, 2-3, (190), (2014).
- , Scientific Opinion on a request from the European Commission related to the prolongation of prohibition of the placing on the market of genetically modified oilseed rape events Ms8, Rf3 and Ms8 × Rf3 for import, processing and feed uses in Austria, EFSA Journal, 11, 4, (n/a-n/a), (2013).
- , Scientific Opinion on a request from the European Commission related to the prolongation of prohibition of the placing on the market of genetically modified oilseed rape event GT73 for import, processing and feed uses in Austria, EFSA Journal, 11, 4, (n/a-n/a), (2013).
- , Scientific Opinion on application (EFSA‐GMO‐NL‐2010‐87) for the placing on the market of genetically modified herbicide tolerant oilseed rape GT73 for food containing or consisting of, and food produced from or containing ingredients produced from, oilseed rape GT73 (with the exception of refined oil and food additives) under Regulation (EC) No 1829/2003 from Monsanto, EFSA Journal, 11, 2, (2013).
- Erling Holden and Geoffrey Gilpin, Biofuels and Sustainable Transport: A Conceptual Discussion, Sustainability, 5, 12, (3129), (2013).
- Sven Ove Hansson and Karin Joelsson, Crop Biotechnology for the Environment?, Journal of Agricultural and Environmental Ethics, 26, 4, (759), (2013).
- Young Jin Chun, Dae In Kim, Kee Woong Park, Soon-Chun Jeong, Sangkyu Park, Kyoungwhan Back and Chang-Gi Kim, Fitness cost and competitive ability of transgenic herbicide-tolerant rice expressing a protoporphyrinogen oxidase gene, Journal of Ecology and Environment, 10.5141/ecoenv.2013.005, 36, 1, (39-47), (2013).
- Yosuke Kuroda, Akito Kaga, Norihiko Tomooka, Hiroshi Yano, Yoshitake Takada, Shin Kato and Duncan Vaughan, QTL affecting fitness of hybrids between wild and cultivated soybeans in experimental fields, Ecology and Evolution, 3, 7, (2150-2168), (2013).
- Yi Sang, Reginald J. Millwood and C. Neal Stewart Jr, Gene use restriction technologies for transgenic plant bioconfinement, Plant Biotechnology Journal, 11, 6, (649-658), (2013).
- Gerhart U. Ryffel, Orgenic plants: Gene‐manipulated plants compatible with organic farming, Biotechnology Journal, 7, 11, (1328-1331), (2012).
- BRIGITTE UWIMANA, LUIGI D’ANDREA, FRANÇOIS FELBER, DANNY A. P. HOOFTMAN, HANS C. M. Den NIJS, MARINUS J. M. SMULDERS, RICHARD G. F. VISSER and CLEMENS C. M. Van De WIEL, A Bayesian analysis of gene flow from crops to their wild relatives: cultivated (Lactuca sativa L.) and prickly lettuce (L. serriola L.) and the recent expansion of L. serriola in Europe, Molecular Ecology, 21, 11, (2640-2654), (2012).
- , Scientific Opinion on application (EFSA‐GMO‐BE‐2010‐81) for the placing on the market of genetically modified herbicide‐tolerant oilseed rape Ms8, Rf3 and Ms8 × Rf3 for food containing or consisting of, and food produced from or containing ingredients produced from, oilseed rape Ms8, Rf3 and Ms8 × Rf3 (with the exception of processed oil) under Regulation (EC) No 1829/2003 from Bayer, EFSA Journal, 10, 9, (n/a-n/a), (2012).
- Jonathan Gressel and Hani Al‐Ahmad, Transgenic Mitigation of Transgene Dispersal by Pollen and Seed, Plant Gene Containment, (125-146), (2012).
- , Scientific Opinion on a request from the European Commission related to the prolongation of prohibition of the placing on the market of genetically modified oilseed rape event GT73 for import, processing and feed uses in Austria, EFSA Journal, 10, 9, (n/a-n/a), (2012).
- , Scientific Opinion on a request from the European Commission related to the prolongation of prohibition of the placing on the market of genetically modified oilseed rape events Ms8, Rf3 and Ms8 × Rf3 for import, processing and feed uses in Austria, EFSA Journal, 10, 9, (n/a-n/a), (2012).
- Jonathan Gressel, Containing and mitigating transgene flow from crops to weeds, to wild species, and to crops, Plant Biotechnology and Agriculture, 10.1016/B978-0-12-381466-1.00032-8, (509-523), (2012).
- Brigitte Uwimana, Marinus J. M. Smulders, Danny A. P. Hooftman, Yorike Hartman, Peter H. van Tienderen, Johannes Jansen, Leah K. McHale, Richard W. Michelmore, Clemens C. M. van de Wiel and Richard G. F. Visser, Hybridization between crops and wild relatives: the contribution of cultivated lettuce to the vigour of crop–wild hybrids under drought, salinity and nutrient deficiency conditions, Theoretical and Applied Genetics, 125, 6, (1097), (2012).
- Arie Altman and Paul Michael Hasegawa, Introduction to plant biotechnology 2011: Basic aspects and agricultural implications, Plant Biotechnology and Agriculture, 10.1016/B978-0-12-381466-1.00050-X, (xxix-xxxviii), (2012).
- Marcus J. Collier and Ewen Mullins, Potential for longevity of novel genetically modified herbicide-tolerant traits in the Irish landscape, Irish Geography, 45, 2, (117), (2012).
- Andrea Foetzki, Carolina Diaz Quijano, Odile Moullet, Alessandro Fammartino, Yvan Kneubuehler, Fabio Mascher, Christof Sautter and Franz Bigler, Surveying of pollen-mediated crop-to-crop gene flow from a wheat field trial as a biosafety measure, GM Crops & Food, 3, 2, (115), (2012).
- Paul Howles and Joe Smith, Risk Assessment of Abiotic Stress Tolerant GM Crops, Improving Crop Productivity in Sustainable Agriculture, (163-181), (2012).
- R. A. de Maagd and K. Boutilier, Biological Containment Strategies for Transgenic Crops, Genetically Modified and Non‐Genetically Modified Food Supply Chains: Co‐Existence and Traceability, (61-77), (2012).
- Tom J. de Jong and Elze Hesse, Selection against hybrids in mixed populations of Brassica rapa and Brassica napus: model and synthesis, New Phytologist, 194, 4, (1134-1142), (2012).
- Kimberly D. Walsh, Debra M. Puttick, Melissa J. Hills, Rong-Cai Yang, Keith C. Topinka and Linda M. Hall, Short Communication: First report of outcrossing rates in camelina [Camelina sativa (L.) Crantz], a potential platform for bioindustrial oils, Canadian Journal of Plant Science, 92, 4, (681), (2012).
- Yann Devos, Rosemary S. Hails, Antoine Messéan, Joe N. Perry and Geoffrey R. Squire, Feral genetically modified herbicide tolerant oilseed rape from seed import spills: are concerns scientifically justified?, Transgenic Research, 21, 1, (1), (2012).
- Zhulong Chan, Patrick J. Bigelow, Wayne Loescher and Rebecca Grumet, Comparison of salt stress resistance genes in transgenic Arabidopsis thaliana indicates that extent of transcriptomic change may not predict secondary phenotypic or fitness effects, Plant Biotechnology Journal, 10, 3, (284-300), (2011).
- Yasuyuki Yoshimura and Kazuhito Matsuo, The Current State of the Environmental Impact Assessment of Abiotic Stress-Tolerant Genetically Modified Plants in the U.S., Canada, Australia, EU and Japan, Japanese Journal of Crop Science, 81, 2, (137), (2012).
- A.M. Mannion and Stephen Morse, Biotechnology in agriculture, Progress in Physical Geography, 10.1177/0309133312457109, 36, 6, (747-763), (2012).
- Martina Talianova and Bohuslav Janousek, What can we learn from tobacco and other Solanaceae about horizontal DNA transfer?, American Journal of Botany, 98, 8, (1231-1242), (2011).
- I. Y. Rabbi, H. K. Parzies, D. Kiambi, B. I. G. Haussmann, R. Folkertsma and H. H. Geiger, Experimental studies on pollen‐mediated gene flow in Sorghum bicolor (L.) Moench using male‐sterile bait plants, Plant Breeding, 130, 2, (217-224), (2010).
- Chris A. Wozniak and Jeannette C. Martinez, U.S. EPA Regulation of Plant-Incorporated Protectants: Assessment of Impacts of Gene Flow from Pest-Resistant Plants, Journal of Agricultural and Food Chemistry, 59, 11, (5859), (2011).
- Josef Soukup, Josef Holec, Miroslav Jursík and Kateřina Hamouzová, Environmental and agronomic monitoring of adverse effects due to cultivation of genetically modified herbicide tolerant crops, Journal für Verbraucherschutz und Lebensmittelsicherheit, 6, S1, (125), (2011).
- Chao-he Huangfu, Sheng Qiang and Xiao-ling Song, Performance of hybrids between transgenic oilseed rape (Brassica napus) and wild Brassica juncea: An evaluation of potential for transgene escape, Crop Protection, 10.1016/j.cropro.2010.09.009, 30, 1, (57-62), (2011).
- Charles Kwit, Hong S. Moon, Suzanne I. Warwick and C. Neal Stewart, Transgene introgression in crop relatives: molecular evidence and mitigation strategies, Trends in Biotechnology, 10.1016/j.tibtech.2011.02.003, 29, 6, (284-293), (2011).
- Noriko Nakamura, Ursula Tems, Masako Fukuchi-Mizutani, Steve Chandler, Yoshiie Matsuda, Shunsuke Takeuchi, Shogo Matsumoto and Yoshikazu Tanaka, Molecular based evidence for a lack of gene-flow between Rosa×hybrida and wild Rosa species in Japan, Plant Biotechnology, 28, 2, (245), (2011).
- E. Jane Morris, A semi-quantitative approach to GMO risk-benefit analysis, Transgenic Research, 20, 5, (1055), (2011).
- Young Jin Chun, Dae In Kim, Kee Woong Park, Hyo-Jeong Kim, Soon-Chun Jeong, Ju Hee An, Kang Hyun Cho, Kyoungwhan Back, Hwan Mook Kim and Chang-Gi Kim, Gene flow from herbicide-tolerant GM rice and the heterosis of GM rice-weed F2 progeny, Planta, 233, 4, (807), (2011).
- Marcus Müller, Birgit Freitag and Franziska Köder, Plant biotechnology in German media: A linguistic analysis of the public image of genetically modified organisms, Biotechnology Journal, 5, 6, (541-544), (2010).
- Ismail Y. Rabbi, Hartwig H. Geiger, Bettina I. G. Haussmann, Dan Kiambi, Rolf Folkertsma and Heiko K. Parzies, Impact of farmers' practices and seed systems on the genetic structure of common sorghum varieties in Kenya and Sudan, Plant Genetic Resources, 8, 02, (116), (2010).
- Jody E. Dexter, Amit J. Jhala, Melissa J. Hills, Rong-Cai Yang, Keith C. Topinka, Randall J. Weselake and Linda M. Hall, Quantification and Mitigation of Adventitious Presence of Volunteer Flax (Linum usitatissimum) in Wheat, Weed Science, 58, 01, (80), (2010).
- , Guidance on the environmental risk assessment of genetically modified plants, EFSA Journal, 8, 11, (2010).
- Anne Légère, La malherbologie au coeur des enjeux du XXI siècle, Phytoprotection, 90, 1, (5), (2009).
- Collin W. Ahrens and Carol A. Auer, Annual Glyphosate Treatments Alter Growth of Unaffected Bentgrass (Agrostis) Weeds and Plant Community Composition, PLoS ONE, 10.1371/journal.pone.0050643, 7, 12, (e50643), (2012).




