doi: 10.15389/agrobiology.2021.1.66eng

UDC: 633.15:581.15:631.543.8

The authors are grateful to Yu.V. Smolkina for seeds of the hybrid Purpurnii and the line Saratovskaya Purpurnaya, and to I.B. Ivanova and A.V. Ul’yanov for help in handling the 2019 crop.
Supported financially under the Program of Basic Scientific Research of State Academies of Sciences for 2020, the State registration No. AAAA-A17-117102740101-5 (for GM corn obtaining and risk assessment), and with the grant No. 18-29-14048mk from the Russian Foundation for Basic Research (for modeling GM corn behavior in field conditions)



Yu.S. Gusev1, O.V. Gutorova1, E.M. Moiseeva1, V.V. Fadeev1,
S.A. Zaytsev2, D.P. Volkov2, E.A. Zuk2, I.V. Volokhina1,
M.I. Chumakov1

1Institute of Biochemistry and Physiology of Plants and Microorganisms RAS, 13, prosp. Entuziastov, Saratov, 410049 Russia, e-mail,,,,, (corresponding author ✉);
2Russian Research, Design and Technology Institute for Sorghum and Maize, 4, 1-i Institutskii proezd, Saratov, 410050 Russia,e-mail,,

Gusev Yu.S.
Volkov D.P.
Gutorova O.V.
Zuk E.A.
Moiseeva E.M.
Volokhina I.V.
Fadeev V.V.
Chumakov M.I.
Zaytsev S.A.

Received July 3, 2020


The new Russian Federal law (No. 358 of 03.07.2016) prohibits the commercial use of GM plants in agriculture, but allows, since 2018, for the first time in Russia their cultivation and testing for research purposes. Consequently, there is a need to assess and develop criteria for safe co-cultivation of non-GM and GM varieties, which are currently absent in Russia. In this paper, it was established for the first time that the 10-15 m distance is sufficient to prevent cross-pollination between maize lines with an acceptable presence of 0.9 % of the donor’s genetic material, regardless of the recipient line, donor and recipient time flowering, and the wind direction in Saratov condition (South-West region of European part of Russia). The work aimed to assess the influence of the distance between pollen donor and recipient, wind direction, donor and recipient time flowering, and a buffer zone presence between them on the crossing frequency in mixed maize crops. The maize lines Korichnevyi marker (KM), GPL-1, Zarodyshevyi marker Saratovskii Purpurnyi (ZMS-P), Purpurnaya Saratovskaya (PS), as well as hybrids Purpurnyi (GP), Raduga and Tester 3 were grown (the experimental field of the Rossorgo, Saratov, South-West region of European Russia, 2018-2019). We planted the GP and ZMS-P lines as pollen donors in 2018 on a 3×80 m2 area with planting density of 7-10 plants per 1 m2. Between the pollen donor area, maize KM and GPL-1 lines were planted, and around them there were a 1290 m2 area of yellow-colored grain recipients (Raduga and Tester 3 hybrids). In September, 5-12 ears from each pollen recipient were harvested. The cross-pollination frequency was calculated as the ratio of purple grains (GP pollination result) or yellow grains with a purple spot (ZMS-P pollination result) to the total grain number in recipient lines. In 2018 it was established that the maximum percentage (from 0.1 to 13.2 %) derived from cross-pollination with two pollen donors depends on different factors. At closer distances (1-4 m), the cross-pollination increased 4-fold for the earlier flowering recipient. The percentage of crosses for recipient Raduga decreased 3 times with a 10 m increase in the distance and 11 times at a 40 m distance from the donor plants. Experiments in 2018 indicate that the 10 m distance from the pollen donor guarantees the percentage of crosses not exceeding the 0.9 % GM threshold in food products accepted in the European Union and Russia. In 2019, we used PS inbred line as a pollen donor. The PS was planted on a 3×5 m plot with Sudanese grass (Sorghum × drummondii) Allegory cultivar as a buffer zone 3 m wide to the East and West and 15 m long to the South-West and North-East. Yellow-grain hybrid Raduga was planted around the buffer zone. The frequency of crosses was calculated as the ratio of the number of purple grains to the total number of Raduga grains per ear. In 2018, the frequency of crosses was also estimated depending on the synchronism of flowering between pollen donors and recipients. The GPL-1 recipient with a 9-day difference from PG (pollen donor) in the beginning of flowering showed a 4 % lower pollination rate compared to a KM line with a flowering period closer to the PG pollen donor (1-day difference). Tall plants of PG donor of pollen prevented spreading pollen from a short ZMS-P donor to the Tester 3 and Raduga recipients in the direction of the wind rose. In 2019, no more than 0.9 % of purple grains were observed for the recipient Raduga when using a buffer zone of 15 m and more from the pollen donor in the wind rose direction. Based on the results of field experiments, the isolation distance from 15 m or more can be recommended to exclude cross-pollination of maize within the threshold of 0.9 % in the conditions of the South-East of the European part of Russia.

Keywords: GM plants, cross-pollination risks, maize, buffer zones.



  1. United States Department of Agriculture. World Agricultural Production. Current Report. Circular Series WAP 9-20. October 2020. Available: Accessed: 01.07.2020.
  2. Zhao S., Liu B., Piao S., Wang X., Lobell D.B., Huang Y., Huang M., Yao Y., Bassu S., Ciais P., Durand J.L., Elliott J., Ewert F., Janssens I.A., Li T., Lin E., Liu Q., Martre P., Müller C., Peng S., Peñuelas J., Ruane A.C., Wallach D., Wang T., Wu D., Liu Z., Zhu Y., Zhu Z., Asseng S. Temperature increase reduces global yields of major crops in four independent estimates. Proceedings of the National Academy of Sciences, 2017, 114(35): 9326-9331 CrossRef
  3. 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(1): 3113 CrossRef
  4. ISAAA. Global Status of Commercialized Biotech/GM Crops: 2016. ISAAA Brief No. 52. ISAAA, Ithaca, NY, 2016.
  5. Golikov A.G., Stepanova N.G., Krasovskii O.A., Skryabin K.G. Biotekhnologiya, 1997, 1: 53-58 (in Russ.).
  6. Chesnokov Yu.V. Vavilovskii zhurnal genetiki i selektsii, 2011, 15(4): 818-827 (in Russ.).
  7. Ujj O. European and American views on genetically modified foods. The New Atlantis, 2016, 49: 77-92.
  8. McHughen A. A critical assessment of regulatory triggers for products of biotechnology: Product vs. process. GM Crops & Food, 2016, 7(3-4): 125-158 CrossRef
  9. Ramessar K., Capell T., Twyman R.M., Quemada H., Christou P. Trace and traceability — a call for regulatory harmony. Natural Biotechnology, 2008, 26(9): 975-978 CrossRef
  10. 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: 15-56 CrossRef
  11. Chumakov M.I., Gusev Yu.S., Bogatyreva N.V., Sokolov A.Yu. Risks of pollen-mediated gene flow from genetically modified maize during co-cultivation with usual maize varieties (review). Sel'skokhozyaistvennaya biologiya[Aricultural Biology], 2019, 54(3): 426-445 CrossRef
  12. 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(4): 1712-1721 CrossRef
  13. 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 CrossRef
  14. Sirsi E. Coexistence: a new perspective, a new field. Agriculture and Agricultural Science Procedia, 2016, 8: 449-454 CrossRef
  15. Meillet A., Angevin F., Bensadoun A., Huby G., Monod H., Messéan A. Design of a decision support tool for managing coexistence between genetically modified and conventional maize at farm and regional levels. Ecological Informatics, 2015, 30: 379-388 CrossRef
  16. 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
  17. 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(8): 780-782 CrossRef
  18. 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
  19. 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(7): e0131549 CrossRef
  20. 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
  21. 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(2): 407-426 CrossRef
  22. Ricci B., Messéana A., Lelièvrec A., Colénod F.C., Angevin F. Improving the management of coexistence between GM and non-GM maize with a spatially explicit model of cross-pollination. European Journal of Agronomy, 2016, 77: 90-100 CrossRef
  23. 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
  24. Duncan B., Leyva-Guerrero E., Werk T, Stojšin D., Baltazar B.M., García-Lara S., Zavala-López M., de la Fuente-Martínez J.M., Meng C. Assessment of potential impacts associated with gene flow from transgenic hybrids to Mexican maize landraces. Transgenic Research, 2019, 28(5-6): 509-523 CrossRef
  25. Bøhn T., Aheto D.W., Mwangala F.S., Fischer K., Bones I.L., Simoloka C., Mbeule I., Schmidt G., Breckling B. Pollen-mediated gene flow and seed exchange in small-scale Zambian maize farming, implications for biosafety assessment. Scientific Reports, 2016, 6: 34483 CrossRef
  26. Kil' V.I. Teoreticheskoe obosnovanie i prakticheskoe ispol'zovanie molekulyarno-geneticheskikh metodov v zashchite sel'skokhozyaistvennykh rastenii ot vreditelei i otsenke transgennykh rastenii na biobezopasnost'. Avtoreferat doktorskoi dissertatsii [Theoretical substantiation and practical use of molecular genetic methods in protecting agricultural plants from pests and assessing transgenic plants for biosafety. DSc Thesis]. Krasnodar, 2010 (in Russ.).
  27. 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(4): 1273-1282 CrossRef
  28. Bannert M., Stamp P. Cross-pollination of maize at long distance. European Journal of Agronomy, 2007, 27(1): 44-51 CrossRef
  29. Langhof M., Hommel B., Hüsken A., Schiemann J., Wehling P., Wilhelm R., Rühl G. Coexistence in maize: do nonmaize buffer zones reduce gene flow between maize fields? Crop Science, 2008, 48(1): 305-316 CrossRef
  30. Gutorova O.V., Apanasova N.V., Yudakova O.I. Izvestiya Samarskogo nauchnogo tsentra Rossiiskoi akademii nauk, 2016, 18(2): 341-344 (in Russ.).
  31. Coe E.H. Jr. A line of maize with high haploid frequency. The American Naturalist, 1959, 93(873): 381-382 CrossRef
  32. Smol'kina Yu.V., Serikov L.V., Kalashnikova E.V. Byulleten' botanicheskogo sada Saratovskogo gosudarstvennogo universiteta,2004, 3(1): 144-148 (in Russ.).
  33. 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(8): 1055-1065 CrossRef
  34. 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(5): 1551-1557 CrossRef
  35. 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.
  36. 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(12): 4377-4384 CrossRef
  37. Gutorova O.V. Byulleten' Botanicheskogo sada Saratovskogo gosudarstvennogo universiteta, 2016, 14(2): 62-70 (in Russ.).
  38. 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.
  39. 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
  40. Westgate M., Lizaso J., Batchelor W. Quantitative relationship between pollen-shed density and grain yield in maize. Crop Science, 2003, 43(3): 934-942 CrossRef
  41. 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(3): 255-265 CrossRef        






Full article PDF (Rus)