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Sel’skokhozyaistvennaya Biologiya [Agricultural Biology], 2019, Vol. 54, № 3, p. 426-445.
(how to cite this article)

doi: 10.15389/agrobiology.2019.3.426eng

UDC: 633.15:573.6.086.83:577.21]:58

Acknowledgements:
The authors are grateful to O.V. Gutorova for reading the manuscript and the comments made, and are grateful to L.M. Fedorova for valuable comments and discussion of the article. We are also grateful to the reviewer for the constructive questions and suggestions.

Supported financially in parts by the Russian Foundation for Basic Research (Project No. 18-29-14048mk) and the Program of Basic Research of State Academies, 2018-2020 (No. AAAA-A17-117102740101-5) for genetically modified corn development and field testing (allocated to M.I. Chumakov and Yu.S. Gusev). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

 

RISKS OF POLLEN-MEDIATED GENE FLOW FROM GENETICALLY MODIFIED MAIZE DURING CO-CULTIVATION WITH USUAL MAIZE VARIETIES (review)

M.I. Chumakov1, Yu.S. Gusev1, N.V. Bogatyreva2, A.Yu. Sockolov2

1Institute of Biochemistry and Physiology of Plants and Microorganisms RAS, 13, Prospekt Entuziastov, Saratov, 410049 Russia, e-mail chumakovmi@gmail.com (✉ corresponding author), gusev_yu@ibppm.ru;
2Saratov State Law Academy, 1, ul. Volskaya, Saratov, 410056 Russia, e-mail bog.junior@gmail.com, AYSockolov@mail.ru

ORCID:
Chumakov M.I. orcid.org/0000-0002-6396-2851
Bogatyreva N.V. orcid.org/0000-0001-5778-5249
Gusev Yu.S. orcid.org/0000-0001-7379-484X
Sockolov A.Yu. orcid.org/0000-0003-3350-7775

Received January 21, 2019

 

Since 1985, active development of agricultural biotechnology has been associated with genetically modified (GM) plants. After the production of GM maize in the second half of the 1990s, the area of its crops has increased over 100-fold. Therefore, the GM maize spreeding and cross-pollination have become more practically relevant. Almost one third of the total area of all GM plants is occupied by GM maize. The Russian Federal Law No. 358 of 03.07.2016 prohibits the commercial use of GM plants in agriculture but allows their cultivation and testing for research purposes. This necessitates assessing and developing criteria, currently absent in Russia, for the safe co-cultivation of non-GM and GM varieties. This review analyzes the factors influencing pollen dispersion: wind (speed and direction), humidity (rain), physiology (viability), the pollen amount, the character of the landscape, the size, shape and orientation of the recipient fields, and the synchrony of flowering of the pollen donor and recipient. Early studies of gene flow in cross-pollination were reviewed Y. Devos et al., (2005) and O. Sanvido et al. (2008). In particular, the distance between GM and traditional maize recommended in the EU countries, with the same threshold for GM content in food, varies considerably (from 25 to 600 m) (Y. Devos et al., 2009; L. Riesgo et al., 2010). In addition to the distance between crops and the synchronicity of flowering, the frequency of cross-pollination depends on the field size and orientation (M. Langhof et al., 2010). Estimates of the cross-pollination frequency and the pollen counts at different distances from the GM donor allowed the researchers to recommend isolation distances of 10 to 200 m. If the isolation distance cannot be ensured, the recipient and/or donor field should be bordered by a barrier to pollen. In the recipient field, the outer rows of maize plants can be the barrier. After a 10-20 m maize barrier, almost none of the analyzed samples contains more than 0.9 % of GM material. For recipient fields of less than 1 ha in area and/or low-depth fields, an isolation distance of at least 50 m should be recommended, especially in the wind rose direction. Data on spreading GM maize with pollen in Europe, South America, Africa, and Asia provide recommendations for safe co-cultivation of non-GM and GM maize varieties and lines. The cytoplasmic male sterility (CMS) approach for GM- and non-GM maize co-cultivation was developed. The genetic control of CMS (N-, S-, C-types and CRISPR-mediated approach) and the CMS application history are discussed. For CMS hybrids, the isolation distances between GM and traditional maize crops may be significantly reduced (up to 10 m) without violation of the European requirements of a 0.9 % marking threshold. However, GM-maize with CMS is not used for practical cultivation. Russia has yet to develop its own measures and recommendations for the joint cultivation of GM and traditional maize.

Keywords: genetically modified corn, gene flow, pollen, CMS, GM crop co-cultivation, GMO regulations.

 

REFERENCES

  1. Pellegrino E., Bedini S., Nuti M.,  Ercoli L. Impact of genetically engineered maize on agronomic, environmental and toxicological traits: a meta-analysis of 21 years of field data. Scientific Reports, 2018, 8(3113): 1-12 CrossRef
  2. ISAAA. Global Status of Commercialized Biotech/GM Crops: 2017. Biotech Crop Adoption Surges as Economic Benefits Accumulate in 22 years. ISAAA Brief No. 53. ISAAA, Ithaca, NY, 2017.
  3. ISAAA. Global Status of Commercialized Biotech/GM Crops: 2016. ISAAA Brief No. 52. ISAAA, Ithaca, NY, 2016.
  4. Golikov A.G., Stepanova N.G., Krasovskii O.A., Skryabin K.G. Biotekhnologiya, 1997, 1: 53-58 (in Russ.).
  5. Chesnokov Yu.V. Vavilovskii zhurnal genetiki i selektsii, 2011, 15(4): 818-827 (in Russ.).
  6. Romeis J., Naranjo S.E., Meissle M., Shelton A.M. Genetically engineered crops help support conservation biological control. Biological Control, 2019, 130: 136-154 CrossRef
  7. Bannert M., Stamp P. Cross-pollination of maize at long distance. European Journal of Agronomy, 2007, 27: 44-51 CrossRef
  8. Baltazar B., Castro Espinoza L., Espinoza Banda A., de la Fuente Martínez J.M., Garzón Tiznado J.A., González García J., Gutiérrez M.A., Guzmán Rodríguez J.L., Heredia Díaz O., Horak M.J., Madueño Martínez J.I., Schapaugh A.W., Stojšin D., Uribe Montes H.R., Zavala García F. Pollen-mediated gene flow in maize: implications for isolation requirements and coexistence in Mexico, the center of origin of maize. PloS ONE, 2015, 10: e0131549 CrossRef
  9. Marceau A., Gustafson D.I., Brants I.O., Leprince F., Foueillassar X., Riesgo L., Areale F.-J., Sowaf S., Kraicg J., Badeah E.M. Updated empirical model of genetically modified maize grain production practices to achieve European Union labeling thresholds. Crop Science, 2013, 53: 1712-1721 CrossRef
  10. Luna S., Figueroa J., Baltazar B., Gomez R., Townsend R., Schoper J.B. Maize pollen longevity and distance isolation requirements for effective pollen control. Crop Science, 2001, 41: 1551-1557 CrossRef
  11. Angevin F., Klein E., Choimet C., Meynard J., de Rouw A., Sohbi Y. Modélisation des effets des systèmes de culture et du climat sur les pollinisations croisées chez le maïs.  Isolement des collectes et maîtrise des disséminations au champ. In: Rapport du groupe 3 du programme de recherche: pertinence économique et faisabilité d’une filière sans utilisation d’OGM, INRAFNSEA. J.-M. Meynard, M. Le Bail (eds.). Thiverval-Grignon, France, 2001: 21-36.
  12. Aylor D. Survival of maize (Zea mays) pollen exposed in the atmosphere. Agricultural and Forest Meteorology, 2004, 123: 125-133 CrossRef
  13. Jarosz N., Loubet B., Durand B., Foueillassar X., Huber L. Variations in maize pollen emission and deposition in relation to microclimate. Environmental Science & Technology, 2005, 39: 4377-4384 CrossRef
  14. Devos Y., Reheul D., De Schrijver A. The co-existence between transgenic and non-transgenic maize in the European Union: a focus on pollen flow and cross-fertilization. Environmental Biosafety Research, 2005, 4(2): 71-87 CrossRef
  15. Ma B.L., Subedi K.D., Reid L.M. Extent of cross-fertilization in maize by pollen from neighboring transgenic hybrids. Crop Science, 2004, 44: 1273-1282 CrossRef
  16. Galeano P., Debat C.M., Ruibal F., Fraguas L.F., Galván G.A. Cross-fertilization between genetically modified and non-genetically modified maize crops in Uruguay. Environmental Biosafety Research, 2010, 9(3): 147-154 CrossRef
  17. Aylor D., Schultes N., Shields E. An aerobiological framework for assessing cross-pollination in ma-ize. Agricultural and Forest Meteorology, 2003, 119: 111-129 CrossRef
  18. Emberlin J., Adams-Groom B., Tidmarsh J. A report on the dispersal of maize pollen. In: Report commissioned by and available from the Soil Association National Pollen Research Unit. Bristol House, Bristol, UK, 1999: 40-56.
  19. Mele E. Spanish study shows that coexistence is possible. Agricultural Biotechnology International Conference, 2004, 3: 2.
  20. Ortega Molina J. Results of the studies into the coexistence of genetically modified and conventional maize. COPA-COGECA colloquy on the co-existence and thresholds of adventitious presence on GMOs in conventional seeds, 2004. Available http://www.copa-cogeca.be/pdf/9.pdf. No date.
  21. Weber W.E., Bringezu T., Broer I., Eder J., Holz F. Coexistence between GM and non-GM maize crops — tested in 2004 at the field scale level (Erprobungsanbau 2004). Journal of Agronomy and Crop Science, 2007, 193: 79-92 CrossRef
  22. Palaudelmas M., Mele E., Monfort A., Serra J., Salvia J., Messeguer J. Assessment of the influence of field size on maize gene flow using SSR analysis. Transgenic Research, 2012, 21(3): 471-483 CrossRef
  23. Ingram J. The separation distances required to ensure cross-pollination is below specified limits in non-seed crops of sugar beet, maize and oilseed rape. Plant Varieties and Seeds, 2000, 13(3): 181-199.
  24. Novotny E., Perdang J. Report on a model for pollen transport by wind. In: Report for the Chardon LL hearing. London, 2002.
  25. Westgate M., Lizaso J., Batchelor W. Quantitative relationship between pollen-shed density and grain yield in maize. Crop Science, 2003, 43: 934-942 CrossRef
  26. Bock A.-K., Lheureux K., Libeau-Dulos M., Nilsagard H., Rodriguez-Cerezo E. Scenarios for co-existence of genetically modified, conventional and organic crops in European agriculture.  IPTS-JRC, Seville, Spain, 2002.
  27. Brookes G., Barfoot P., Melé E., Messeguer J., Bénétrix F., Bloc D., Foueillassar X., Fabié A., Poeydomenge C. Genetically modified maize: pollen movement and crop coexistence. PG Economics Ltd., Dorchester, UK, 2004.
  28. Du M., Kawashima S., Matsuo K., Yonemura S., Inoue S. Simulation of the effect of a cornfield on wind and pollen deposition. In: International Congress on Modelling and Simulation. F. Ghas-semi, P. Whetton, R. Little, M. Littleboy (eds.). Australian National University, 2001: 899-903.
  29. Liu Y., Chen F., Guan X., Li J. High crop barrier reduces gene flow from transgenic to conventional maize in large fields. European Journal of Agronomy, 2015, 71: 135-140 CrossRef
  30. Le Bail M., Lecroart B., Gauffreteau A., Angevin F., Messean A. Effect of the structural variables of landscapes on the risks of spatial dissemination between GM and non-GM maize. European Journal of Agronomy, 2010, 33: 12-23 CrossRef
  31. Henry C., Morgan D., Weekes R., Daniels R., Boffey C. Farm scale evaluations of GM crops: monitoring gene flow from GM crops to non-GM equivalent crops in the vicinity: Part I: Forage maize. DEFRA report EPG, 2003.
  32. Weekes R., Allnutt T., Boffey C., Morgan S., Bilton M., Daniels R., Henry C. A study of crop-to-crop gene flow using farm scale sites of fodder maize (Zea mays L.) in the UK. Transgenic Research, 2007, 16(2): 203-211 CrossRef
  33. Devos Y., Demont M., Sanvido O. Coexistence in the EU — return of the moratorium on GM crops? Nature Biotechnology, 2008, 26(11): 1223-1225 CrossRef
  34. Gustafson D.I., Brants I.O., Horak M.J., Remund K.M., Rosenbaum E.W., Soteres J.K. Empirical modeling of genetically-modified maize grain production practices to achieve European Union labeling thresholds. Crop Science, 2006, 46: 2133-2140 CrossRef
  35. Chamecki M., Gleicher S.C., Dufault N.S., Isard S.A. Diurnal variation in settling velocity of pollen released from maize and consequences for atmospheric dispersion and cross-pollination. Agricultural and Forest Meteorology, 2011, 151: 1055-1065 CrossRef
  36. Makowski D., Bancal R., Bensadoun A., Monod H., Messéan A. Sampling strategies for evaluating the rate of adventitious transgene presence in non-genetically modified crop fields. Risk Analysis, 2017, 37(9): 1693-1705 CrossRef
  37. Bohn T., Primicerio R., Traavik T. The German ban on GM maize MON810: scientifically justified or unjustified? Environmental Sciences Europe, 2012, 24(22): 1-7 CrossRef
  38. Della Porta G., Ederle D., Bucchini L., Prandi M., Verderio A., Pozzi C. Maize pollen mediated gene flow in the Po valley (Italy): Source—recipient distance and effect of flowering time. European Journal of Agronomy, 2008, 28: 255-265 CrossRef           
  39. Popescu S., Leprince F., Ioja-Boldura O., Marutescu A., Sabau I., Marcela Badea E. Quantification of pollen mediated gene flow in maize. Romanian Biotechnological Letters, 2010, 15: 5351-5360.
  40. Van de Wiel C.C.M., Groeneveld R.M.W., Dolstra O., Kok E.J., Scholtens I.M.J., Thissen J., Smulders M.J.M., Lotz L.A.P. Pollen-mediated gene flow in maize tested for coexistence of GM and non-GM crops in the Netherlands: Effect of isolation distances between fields. Njas-Wageningen Journal of Life Sciences, 2009, 56: 405-423 CrossRef
  41. Jaffe G. Regulating transgenic crops: a comparative analysis of different regulatory processes. Transgenic Research, 2004, 13: 5-19 CrossRef
  42. Nicolia A., Manzo A., Veronesi F., Rosellini D. An overview of the last 10 years of genetically engineered crop safety research. Critical Review Biotechnology, 2014, 34(1): 77-88 (doi:10.3109/07388551.2013.823595">CrossRef
  43. Sirsi E. Coexistence: a new perspective, a new field. Agriculture and Agricultural Science Procedia, 2016, 8: 449-454 CrossRef
  44. Ujj O. European and American views on genetically modified foods. The New Atlantis, 2016, 49: 77-92.
  45. EC (European Commission). 2015b. Fact sheet: Questions and answers on EU’s policies on GMOs. Available http://europa.eu/rapid/press-release_MEMO-15-4778_en.htm. Accessed 30.11.2015.
  46. Restrictions on Genetically Modified Organisms. Washington: Law Library of Congress, Global Legal Research Center, 2014. Available https://www.loc.gov/law/help/restrictions-on-gmos/index.php. No date.
  47. Deppermann A., Balkovic J., Bundle S.-C., Di Fulvio F., Havlík P., Leclère D., Lesiv M., Prishchepov A., Schepaschenko D. Increasing crop production in Russia and Ukraine— regional and global impacts from intensification and recultivation. Environmental Research Letters, 2018, 13: 025008 CrossRef
  48. Clive J. Global status of commercialized biotech/gm crops: 2014. ISAAA Brief No. 49. ISAAA, Ithaca, NY, 2014.
  49. Brookes G., Barfoot P. Farm income and production impacts of using GM crop technology 1996-2016. GM Crops & Food, 2018, 9: 59-89 CrossRef
  50. Zhuchenko A.A. Role of genetic engeneering in adaptive system of plant breeding (myths and reality). Sel’skokhozyaistvennaya Biologiya [Agricultural Biology], 2003, 1: 3-33.
  51. Zhivotovskii L.A. V sbornike: GMO — skrytaya ugroza Rossii /Pod redaktsiei I.V. Starikova [In: GMO — the hidden threat to Russia. I.V. Starikov (ed.)]. Moscow, 2004: 94-104 (in Russ.).
  52. Muir W.M., Howard R.D. Possible ecological risks of transgenic organism release when transgenes affect mating success: Sexual selection and the Trojan gene hypothesis. Proc. Natl. Acad. Sci. USA, 1999, 96 (24): 13853–13856 CrossRef
  53. Piperno D.R., Flannery K.V. The earliest archaeological maize (Zea mays L.) from highland Mexico: new accelerator mass spectrometry dates and their implications. Proc. Natl. Acad. Sci. USA, 2001, 98: 2101-2103 CrossRef
  54. Cárdenas F. Latin American maize germplasm regeneration and conservation. In: Proc. Workshop CIMMYT, Mexico, June 4-6, 1996. S. Taba (ed.). CIMMYT, Mexico, 1997: 74.
  55. Serratos-Hernandez J.-A., Islas-Gutierrez F., Buendia-Rjdrigueez E., Berthaud J. Gene flow scenarios with transgenic maize in Mexico. Environmental Biosafety Research, 2004. 3: 149-157 CrossRef
  56. Quist D., Chapela I.H. Transgenic DNA introgressed into traditional maize landraces in Oaxaca, Mexico. Nature, 2001, 41: 541-543 CrossRef 
  57. Ortiz-Garcıa S., Ezcurra E., Schoel B., Acevedo F., Soberon J., Snow A.A. Absence of detectable transgenes in local landraces  of maize in Oaxaca, Mexico (2003-2004). Proc. Natl. Acad. Sci. USA, 2005, 102(35): 12338-12343 CrossRef 
  58. Bellon M.R., Berthaud J. Transgenic maize and the evolution of landrace diversity in Mexico. The importance of farmers’ behavior. Plant Physiology, 2004, 134: 883-888 CrossRef
  59. McHughen A. A critical assessment of regulatory triggers for products of biotechnology: Product vs. process. GM Crops & Food, 2016, 7: 125-158 CrossRef
  60. Ramessar K., Capell T., Twyman R.M., Quemada H., Christou P. Trace and traceability — a call for regulatory harmony. Natural Biotechnology, 2008, 26: 975-978 CrossRef
  61. Tetsuya I., Motoko A. A future scenario of the global regulatory landscape regarding genome-edited crops. GM Crops & Food, 2017, 8(1): 44-56 CrossRef
  62. Baram M. Governance of GM crop and food safety in the United States. In: Governing risk in GM agriculture. M. Baram, M. Bourrier (eds.). Cambridge University Press. 2011: 15-55.
  63. Nabradi A., Popp J. Economics of GM crop cultivation. Applied Studies in Agribusiness and Commerce, 2011, 05: 7-19 CrossRef
  64. Xu Z., Hennessy D.A., Sardana K., Moschini G.C. The realized yield eject of genetically engineered crops: U.S. maize and soybean. Crop Science, 2013, 53: 735-745 CrossRef
  65. Eastham K., Sweet J. Genetically modified organisms (GMOs): the significance of gene flow through pollen transfer. In: European Environment Agency. Environmental issue report. D. Gee (ed.). Copenhagen, 2002, 28: 38-42.
  66. Lee M.S., Anderson E.K., Stojšin D., McPherson M.A., Baltazar B., Horak M.J., de la Fuente J.M., Wu K., Crowley J.H., Rayburn A.L., Lee D.K. Assessment of the potential for gene flow from transgenic maize (Zea mays L.) to eastern gamagrass (Tripsacum dactyloides L.). Transgenic Research, 2017, 26(4): 501-514 CrossRef
  67. Instituto Colombiano Agropecuario. Por medio de la cual se implementa el plan de manejo, bioseguridad y seguimiento para siembras controladas de maíz genéticamente modificado. Resolución No. 2894. Bogota, 2010.
  68. Chaparro-Giraldo A., Blanco M.J.T., López-Pazos S.A. Evidence of gene flow between transgenic and non-transgenic maize in Colombia. Agronomía Colombiana, 2015, 33(3): 297-304 CrossRef
  69. Vicién C., Trigo E. The Argentinian GMO biosafety system: an evolving perspective. In: Genetically modified organisms in developing countries risk analysis and governance. A. Adendle, E. Jane Morris, J. Denis (eds.). Cambridge University Press, Cambridge, UK, 2017: 247-257 CrossRef
  70. Burachik M. Experience from use of GMOs in Argentinian agriculture, economy and environment. New Biotechnology, 2010, 27(5): 588-592 CrossRef
  71. Coelho M.V.S. Coexistence in Brazil. In: The coexistence of genetically modified, organic and conventional foods. N. Kalaitzandonakes, P. Phillips, J. Wesseler, S. Smyth (eds.). Natural Resource Management and Policy, Springer, NY, USA, 2016, 49: 87-94 CrossRef
  72. Viljoen C., Chetty L. A case study of GM maize gene flow in South Africa. Environmental Sciences Europe, 2011, 23: 1-8 CrossRef
  73. Wang C.Y., Kuo B.J., Hsu Y.H., Yiu T.J., Lin W.S. Using the two-step model based on the field border consideration to evaluate pollen-mediated gene flow (PMGF) model and the isolation distance of GM maize in Potzu city of Chiayi county. Crop, Environment & Bioinformatics, 2013, 10: 172-189 CrossRef
  74. Smyth S.J. Genetically modified crops, regulatory delays, and international trade. Food Energy Security, 2017, 6: 78-86 CrossRef
  75. Bückmann H., Capellades G., Hamouzová K., Holec J., Soukup J., Messeguer J., Melé E., Nadal A., Guillen X.P., Pla M., Serra J., Thiele K., Schiemann J. Cytoplasmic male sterility as a biological confinement tool for maize coexistence: Optimization of pollinator spatial arrangement. Plant, Soil and Environment, 2017, 63: 145-151 CrossRef
  76. Bruns H.A. Southern corn leaf blight: a story worth retelling. Agronomy Journal. 2017, 109: 1218-1224 CrossRef
  77. Schnable P.S., Wise R.P. The molecular basis of cytoplasmic male sterility and fertility restoration. Trends in Plant Science, 1998, 3: 175-180 CrossRef
  78. Su A., Song W., Xing J., Zhao Y., Zhang R., Li C., Duan M., Luo M., Shi Z., Zhao J. identification of genes potentially associated with the fertility instability of S-type cytoplasmic male sterility in maize via bulked segregant RNA-seq. PLoS ONE, 2016, 11(9): e0163489 CrossRef
  79. Liu Y., Wei G., Xia Y., Liu X., Tang J., Lu Y., Lan H., Zhang S., Li C., Cao M. Comparative transcriptome analysis reveals that tricarboxylic acid cycle-related genes are associated with maize CMS-C fertility restoration. BMC Plant Biology, 2018, 18(1): 190 CrossRef
  80. Herman R.A., Zhuang M., Storer N.P., Cnudde F., Delaney B. Risk-only assessment of genetically engineered crops is risky. Trends in Plant Science, 2019, 24(1): 58-68 CrossRef
  81. Bückmann H., Hüsken A., Schiemann J. Applicability of cytoplasmic male sterility (CMS) as a reliable biological confinement method for the cultivation of genetically modified maize in Germany. Journal of Agricultural Science and Technology, 2013, A3: 385-403.
  82. Bückmann H., Thiele K., Schiemann J., Husken A. Influence of air temperature on the stability of cytoplasmic male sterility (CMS) in maize (Zea mays L.). AgBioForum, 2014, 2: 205-212.
  83. Bückmann H., Thiele K., Schiemann J. CMS maize: a tool to reduce the distance between GM and non‐GM maize. EuroChoices, 2016, 15(1): 31-35 CrossRef
  84. Wan X., Wu S., Li Z., Dong Z., An X., Ma B., Tian Y., Li J. Maize genic male-sterility genes and their applications in hybrid breeding: progress and perspectives. Molecular Plant, 2019, 12(3): 321-342 CrossRef
  85. Wu Y., Fox T.W., Trimnell M.R., Wang L., Xu R.J., Cigan A.M., Huffman G.A., Garnaat C.W., Hershey H., Albertsen M.C. Development of a novel recessive genetic male sterility system for hybrid seed production in maize and other cross pollinating crops. Plant Biotechnology Journal, 2016, 14: 1046-1054 CrossRef
  86. Zhang D., Wu S., An X., Xie K., Dong Z., Zhou Y., Xu L., Fang W., Liu S., Liu S., Zhu T., Li J., Rao L., Zhao J., Wan X. Construction of a multicontrol sterility system for a maize male-sterile line and hybrid seed production based on the ZmMs7 gene encoding a PHD-finger transcription factor. Plant Biotechnology Journal, 2018, 16: 459-471 CrossRef
  87. Feng P.C., Qi Y., Chiu T., Stoecker M.A., Schuster C.L., Johnson S.C., Fonseca A.E., Huang J. Improving hybrid seed production in corn with glyphosate-mediated male sterility. Pest Management Science, 2014, 70: 212-218 CrossRef
  88. Xie K., Wu S., Li Z., Zhou Y., Zhang D., Dong Z., An X., Zhu T., Zhang S., Liu S., Li J., Wan X. Map-based cloning and characterization of Zea mays male sterility33 (ZmMs33) gene, encoding a glycerol-3-phosphate acyltransferase. Theoretical and Applied Genetics, 2018, 131: 1363 CrossRef
  89. Chen R., Xu Q., Liu Y., Zhang J., Ren D., Wang G., Liu Y. Generation of transgene-free maize male sterile lines using the CRISPR/Cas9 system. Frontiers in Plant Science, 2018, 9: 1180 CrossRef
  90. Svitashev S., Schwartz C., Lenderts B., Young J.K., Mark C.A. Genome editing in maize directed by CRISPR–Cas9 ribonucleoprotein complexes. Nature Communications, 2016, 7: 13274 CrossRef
  91. Sanvido O., Widmer F., Winzeler M., Streit B., Szerencsits E., Bigler F. Definition and feasibility of isolation distances for transgenic maize cultivation. Transgenic Research, 2008, 17: 317-335 CrossRef
  92. Devos Y., Demont M., Dillen K., Reheul D., Kaiser M., Sanvido O. Coexistence of genetically modified (GM) and non-GM crops in the European Union (review). Agronomy for Sustainable Development, 2009, 29: 11-30 CrossRef
  93. Riesgo L., Areal F.J., Sanvido O., Rodriguez-Cerezo E. Distances needed to limit cross-fertilization between GM and conventional maize in Europe. Nature Biotechnology, 2010, 28: 780-782 CrossRef
  94. Langhof M., Hommel B., Hüsken A., Njontie C., Schiemann J., Wehling P., Wilhelm R., Rühl G. Coexistence in maize: isolation distance in dependence on conventional maize field depth and separate edge harvest. Crop Science, 2010, 50: 1496-1508 CrossRef
  95. Marceau A., Saint-Jean S., Loubet B., Foueillassar X., Huber L. Biophysical characteristics of maize pollen: Variability during emission and consequences on cross-pollination risks. Field Crops Research, 2012, 127: 51-63 CrossRef
  96. Venus T.J., Dillen K., Punt M.J., Wesseler J.H. The costs of coexistence measures for genetically modified maize in Germany. Journal of Agricultural Economics, 2017, 68: 407-426 CrossRef

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