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Fiziol. rast. genet. 2016, vol. 48, no. 3, 196-214, doi: https://doi.org/10.15407/frg2016.03.196

The modern biotechnologies of producing wheat plants resistant to stresses

Morgun V.V.1, Dubrovna O.V.1, Morgun B.V.1,2

  1. Institute of Plant Physiology and Genetics, National Academy of Sciences of Ukraine 31/17 Vasylkivska St., Kyiv, 03022, Ukraine
  2. Institute of Cell Biology and Genetic Engineering, National Academy of Sciences of Ukraine 148 Akademika Zabolotnoho St., Kyiv, 03143, Ukraine

The current state of development of plant cellular and molecular biotechnologies, in particular for wheat has been analyzed. Achievements of Ukrainian and foreign scientists in the field of cell selection and genetic engineering to obtain wheat plants resistant to biotic and abiotic stress factors are illustrated. Attention paid to the main directions, methods of selection and assessment opportunities, prospects and challenges of modern biotechnology research for this strategic crop in Ukraine.

Keywords: Triticum L., cell selection, genetic engineering, molecular markers, biotic and abiotic stresses

Fiziol. rast. genet.
2016, vol. 48, no. 3, 196-214

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References

1. Anapiyaev, B.B., Rsaliev, S.T. & Sarbaev, A.T. (2002). Accelerated selection for resistance to biotic environmental factors of Triticum aestivum L. using the haploid biotechnology method. Dokl. Rossel'khozakademii, No 4, pp 15-17 [in Russian].

2. Bavol, A.V., Dubrovna, O.V.& Lyalko, I.I. (2008). Selection and cytological analysis of resistant to the culture filtrate Gaeumannomyces graminis var. tritici cell lines of wheat and regenerates from them. Visnyk ukrainskoho tovarystva henetykiv i selektsioneriv, 6 (2), pp. 191-200 [in Ukrainian].

3. Bavol, A.V., Dubrovna, O.V. & Lyalko, I.I. (2009). In vitro selection of bread wheat for resistance to Gaeumannomyces graminis var. tritici. Fiziol. biokhim. kult. rastenij, 41, No. 4, pp. 314-320 [in Ukrainian].

4. Bavol, A.V. & Dubrovna, O.V. (2009). Molecular genetic polymorphism of cell lines of wheat, resistant to culture filtrate Gaeumannomyces graminis var. tritici and regenerants from them. Cytology and Genetics, 43, No. 5, pp. 28-34 [in Ukrainian]. https://doi.org/10.3103/S0095452709050041

5. Bavol, A.V., Dubrovna, O.V. & Morgun, B.V. (2014). Identification of Dreb1 genes in bread wheat plant-regenerants, obtained from callus lines resistant to modeled water deficit. Fiziol. rast. genet., 46, No 2, pp. 136-142 [in Ukrainian].

6. Bavol, A.V. (2010). Cell selection of bread wheat for resistance to Gaeumannomyces graminis var. tritici. (Extended abstract of Doctor thesis). Institute of Plant Physiology and genetic of NAS of Ukraine, Kyiv, Ukraine [in Ukrainian].

7. Voloschuk, S.I., Voloshchuk, G.D. & Girko, V.S. (2001). Use of cellular technologies in vitro in winter wheat selection for resistance to fungal pathogens. Henetyka i selektsiya v Ukrayini na mezhi tysyacholit. Kyiv: Logos [in Ukrainian].

8. Voloschuk, S.I., Voloshchuk, G.D. & Girko, V.S.(1998). Creation of initial material of winter wheat, resistant to fungal pathogens, methods of cell selection. Zakhyst roslyn, No. 8, pp 4-5 [in Ukrainian].

9. Voloshchuk, S.I. Cell selection of wheat for resistance to Fusarium graminearum Schwabe. (Extended abstract of Doctor thesis). Institute of Agriculture of the National Academy of Agrarian Sciences of Ukraine, Chabany, Ukraine [in Ukrainian].

10. Voronova, S.S., Goncharuk, O.M., Bavol, A.V. & Dubrovna, O.V. (2015). Genetic transformation of bread wheat using vector constructs containing the genes of proline metabolism. Visnyk ukrainskoho tovarystva henetykiv i selektsioneriv, 13 (1), pp. 28-33 [in Ukrainian].

11. Jos, L. & Kalashnikova, E. (2000). Cell Selection of Wheats for Resistance to Septoria. S.-h. Biotechnology: Selected Works. Moskow, Eurasia+[in Russian].

12. Dolgikh, Yu.I. (2005). Somaclonal variability of plants and the possibility of its practical use (for example, maize) (Extended abstract of Doctor thesis). Institute of Plant Physiology of RAS. Moscow, Russia [in Russian].

13. Dridze, I.L. (1990). The use of an analogue of proline for the selection of stress-resistant variants in the culture tissues of soybean and tobacco (Extended abstract of Doctor thesis). Institute of Plant Physiology of RAS. Moscow, Russia [in Russian].

14. Dubrovna, O.V., Morgun, B.V. & Bavol, A.V. (2014). Biotechnology of wheat: Cell Selection and Genetic Engineering. Kyiv: Logos.

15. Dubrovna, O.V. & Morgun, B.V. (2009). Cell selection of wheat for resistance to stress factors of the environment. Fiziol. biokhim. kult. rastenij, 41, No. 6, pp. 463-476 [in Ukrainian].

16. Dubrovna, O.V., Chugunkova, T.V., Bavol, A.V. & Lyalko, I.I. (2012). Biotechnological bases for the creation of plants resistant to stress. Kyiv: Logos [in Ukrainian].

17. Erofeeva, E.A. (2010). The emergence of cross-adaptation to osmotic stress in wheat seedlings under the action of heavy metal salts. Retrieved from http://msu - research.ru /index.php/ biology/8-gidrobiology/259-cross-adtation.

18. Zinchenko, M.O., Dubrovna, O.V. & Bavol, O.V. (2012). In vitro selection of bread wheat on complex resistance to metabolites of the take-all and water deficit. Visn. Ukr. t-va henetykiv i selektsioneriv, 10, No 1, pp. 20 - 27 [in Ukrainian].

19. Kalashnikova, E.A. (2003). Biological bases of plant cell selection. Dokl. Timiryazevskoy sel'skokhozyaystvennoy akademii, No. 275, pp.110-112 [in Russian].

20. Lavrova, N.V. (2002). Biotechnological methods in wheat cell selection for resistance to septoria, caused by a pathogen of Septoria nodorum. Actual problems of science in the AIC. Kostroma: Kostroma publishing house [in Russian].

21. Lavrova, N.V. (2006). Development and application of biotechnologies for the production of fusarium-resistant plants of winter wheat (haploid) and cucumber (meristem, callus and microsporogenic). (Extended abstract of Doctor thesis). Institute of Plant Physiology of RAS. Moscow, Russia [in Russian].

22. Lavrova, N.V. (2002). Wheat breeding in vitro for resistance to fusarium. Actual problems of science in the AIC. Kostroma: Kostroma publishing house [in Russian].

23. Lapshin, P.V., Butenko, R.G. & Shevelukha, V.S. (2001). Cell selection of spring bread wheat for resistance to UV-B radiation. Izv. Timiryazevskoy sel'skokhozyaystvennoy akademii, No. 2, pp. 136-114 [in Russian].

24. Lobov, V.P., Tomilin, M.V. & Veselov, A.P. (2010). Genetically modified plants: achievements, prospects and limitations. Vestn. Nizhegorod. un-ta im. N.I. Lobachevskogo, No 2, pp. 423-429 [in Russian].

25. Mikhalskaya, S.I., Sergeeva, L.E., Matveeva, A.Yu., Kobernik, N.I., Kochetov, A.V., Tishchenko, E.N. & Morgun, B.V. (2014). Increase of Free Proline Content in Osmotolerant Maize Plants with Double-Stranded RNA-Suppressor of Proline Dehydrogenase Gene. Fiziol. rast. genet., 46, No 6, pp. 482-489 [in Russian].

26. Morgun, V.V., Gavrilyuk, M.M., Oksem, V.P., Morgun, B.V. & Pochynok, V.M. (2014). Introduction of New, Stress Resistant, High-yielding Winter Wheat Varieties Based on Chromosome Engineering and Marker-Assisted Selection. Nauka ta innovatsiyi. 10, No 5, pp. 40-48 [in Ukrainian]. https://doi.org/10.15407/scin10.05.040

27. Morgun, B.V., Stepanenko, O.V., Stepanenko, A.I. & Rybalka, O.I. (2015). Molecular genetic identification of polymorphism of Wx genes in bread wheat hybrids with multiplex polymerase chain reactions. Fiziol. rast. genet., 47, No 1, pp. 25-35 [in Ukrainian].

28. Morgun, V.V., Tarasyuk, O.I., Pochinok, V.M. & Rybalka, A.I. (2015). Unique grain quality breeding lines of wheat with rare alleles of Gli / Glu loci. Fiziol. rast. genet., 47, No. 4, pp. 302-309 [in Russian].

29. Morgun, B.V, Chugunkova, T.V, Rybalka, O.I., Pochinok, V.M, Tarasyuk, O.I. & Stepanenko, A.I. (2013). Molecular identification of Glu-B1al allele in varieties and lines of wheat 2013. Fiziol. rast. genet, 45, No. 4, pp. 290-295 [in Ukrainian].

30. Tishchenko, E.N. (2013). Genetic engineering with the use of L-proline metabolism genes to increase the plant osmotolerance. Fiziol. rast. genet, 45, No. 6. pp. 488-500 [in Russian].

31. Shevelukha, V.S., Roginskaya, V.A. & Khizhnyak, S.V. (1992). Perspectives of the use of toxins pathogen of common root rot of cereals in cell selection. S.-kh. biologiya, 3, pp. 45-51[in Russian].

32. Abdel-Ghany, H., Nawar, A. & Ibrahim, M. (2004, September). Using tissue culture to select for drought tolerance in bread wheat. Proceedings of the 4-th Intern. Crop Science Congr.New directions for a diverse planet (p. 345). Brisbane, Australia.

33. Abdelsamad, A., Sayed, O. & Hayam, F. (2007). Development of drought tolerant double haploid wheat using biochemical genetic markers on in vitro culture. J. Appl. Sci. Res., 3, pp 1589-1599.

34. Abebe, T., Guenzi, A., Martin, B. & Cushman, J. (2003). Tolerance of mannitol-accumulating transgenic wheat to water stress and salinity. Plant Physiol., 131, No. 4, pp. 1748-1755. https://doi.org/10.1104/pp.102.003616

35. Ahmed, A. (1999). Response of immature embryos in vitro regeneration of some wheat (T. aestivum) genotypes under different osmotic stress of mannitol. J. Agr. Sci., 30, No. 3, pp. 25-34.

36. Altpeter, F., Vasil, V., Srivastava, V. & Vasil, I. (1996). Integration and expression of the high-molecular-weight glutenin subunit 1Ax1 gene into wheat. Nature Biotech., 14, pp.1155-1159. https://doi.org/10.1038/nbt0996-1155

37. Aly, M., Sabry, S., Abdelfatah, O. & Elgharbawy, H. (2007). In vitro screening for the effect of sea water salinity stress on growth and biochemical characteristics of wheat Triticum aestivum L. Int. J. Appl. Agricult. Res., 2, No. 1, pp. 1-11.

38. Arzani, A. & Mirodjagh, S. (1999). Response of durum wheat cultivars to immature embryo culture, callus induction and in vitro salt stress. Plant Cell, Tissue Organ Cult., No. 58, pp. 67-72. https://doi.org/10.1023/A:1006309718575

39. Baga, M., Nair, R., Repellin, A., Scoles, G. & Chibbar, R. (2000). Isolation of a cDNA encoding a granule-bound 152-kilodalton starch-branching enzyme in wheat. Plant Physiol., 124, pp. 253-264. https://doi.org/10.1104/pp.124.1.253

40. Bajji, M., Lutts, S. & Kinet, J. (2001). Physiological changes after exposure to and recovery from polyethyleneglycol induced water deficit in callus cultures issued from durum wheat (Triticum durum) cultivars differing in drought resistance. J. Plant Physiol., 156, pp 75-83. https://doi.org/10.1016/S0176-1617(00)80275-8

41. Bakos, F., Gaspar, L., Darko, E., Ascough, G., Ambrus, H. & Barnabas, B. (2008). A cytological study on aluminium-treated wheat anther cultures resulting in plants with increased Al tolerance. Plant Breed., 127, No. 1, pp. 236-240. https://doi.org/10.1111/j.1439-0523.2007.01473.x

42. Barakat, M. & Abdel-Latif, T. (1996). In vitro selection of wheat callus tolerant to high levels of salt and plant regeneration. Euphytica, 91, No. 2, pp. 127-140.

43. Barro, F, Rooke, L, Bekes, F, Gras, P, Tatham, A., Fido, R., Lazzeri, P., Shewry, P. & Barcelo P. (1997). Transformation of wheat with high molecular weight subunit genes results in improved functional properties. Nature Biotech., 15, pp. 1295-1299. https://doi.org/10.1038/nbt1197-1295

44. Ben-Saad, R., Ben-Ramdhan, W. & Zouari, N. (2012). Marker-free transgenic durum wheat cv. Karim expressing the AlSAP gene exhibits a high level of tolerance to salinity and dehydration stresses. Mol. Breed., 30, No. 1, pp. 521-533. https://doi.org/10.1007/s11032-011-9641-3

45. Bieri, S., Potrykus, I. & Futterer, J. (2000). Expression of active barley seed ribosome-inactivating protein in transgenic wheat. Theor. Appl. Genet., 100, pp. 755-763. https://doi.org/10.1007/s001220051349

46. Bi, R., Jia, H., Feng, D. & Wang, H. (2006). Production and analysis of transgenic wheat (Triticum aestivum L.) with improved insect resistance by the introduction of cowpea trypsin inhibitor gene. Euphytica, 151, pp. 351-360. https://doi.org/10.1007/s10681-006-9157-9

47. Bliffeld, M., Mundy, J., Potrykus, I. & Futterer, J. (1999). Genetic engineering of wheat for increased resistance to powdery mildew disease. Theor. Appl. Genet., 98, pp. 1079-1086. https://doi.org/10.1007/s001220051170

48. Brinch-Pederson, H., Oleson, A., Rasmussen, S. & Holm, P. Generation of transgenic wheat (Triticum aestivum L.) for constitutive accumulation of an Aspergillus phytase. Mol. Breed., 6, pp. 195-206.

49. Bruins, M.B.M. (1998). Fusarium Head Blight Resistance in Wheat. Wageningen.

50. Chen, Q., Xie, M., Ma, X., Dong, L., Chen, J. & Wang, X. (2010). MISSA is a highly efficient in vivo DNA assembly method for plant multiple-gene transformation. Plant Physiol., 153, pp. 41-50. https://doi.org/10.1104/pp.109.152249

51. Clausen, M., Krauter, R., Schachermayr, G., Potrykus, I. & Sautter, C. (2000). Antifungal activity of a virally encoded gene in transgenic wheat. Nature Biotech., 18, pp. 446-449. https://doi.org/10.1038/74521

52. Cong, L., Wang, C., Chen, L., Liu, H., Yang, G. & He, G. (2009). Expression of phytoene synthase1 and carotene desaturase crtI genes result in an increase in the total carotenoids content in transgenic elite wheat (Triticum aestivum L.). J. Agr. Food Chem., 57, 8652-8660. https://doi.org/10.1021/jf9012218

53. Crino, P. (1997). Culture filtrate as selective agent of resistance to phytopathogenic fungi. In Toxins in Plant Disease Development and Evolving Biotechnology (pp.183-208). New Hampshire (USA): Science Publishers.

54. Cushman, J.C. & Bohnert, H.J. (2000). Genomic approaches to plant stress tolerance. Curr. Opin. Plant Biol., 3, pp. 117-124. https://doi.org/10.1016/S1369-5266(99)00052-7

55. De Block, M., Debrouwer, D. & Moens, T. (1997). The development of a nuclear male sterility system in wheat. Expression of the barnase gene under the control of tapetum specific promoters. Theor. Appl. Genet., 95, pp. 125-131. https://doi.org/10.1007/s001220050540

56. Dorffling, K., Dorffling, H., Lesselich, G., Luck, E., Zimmermann, C., Melz, G. & Jurgens, H. (1997). Heritable improvement of frost tolerance in winter wheat by in vitro-selection of hydroxyproline-resistant proline overproducing mutants. Euphytica, 93, No. 1, pp. 1-10. https://doi.org/10.1023/A:1002946622376

57. Fadel, F. & Wenzel, G. (1994). In vitro selection for tolerance to fusarium in F1 microspore populations of wheat. Plant Pathol., 43, pp. 644-650.

58. Galovic, V., Kotaranin, Z. & Dencic, S. (2005). In vitro assessment of wheat tolerance to drought. Genetika, 37, No. 2, pp. 165-171. https://doi.org/10.2298/GENSR0502165G

59. He, C., Zhang, W. & Gao, Q. (2011). Enhancement of drought resistance and biomass by increasing the amount of glycine betaine in wheat seedling. Euphytica, 177, No. 2, pp. 151-167. https://doi.org/10.1007/s10681-010-0263-3

60. He, G., Rooke, L. Steele, S., Bekes, F., Gras, P., Tatham, A., Fido, R., Barcelo, P., Shewry, P. & Lazzeri, P. (1999). Transformation of pasta wheat (Triticum turgidum L. var. durum) with high-molecular weight glutenin subunit genes and modification of dough functionality. Mol. Breed., 5, pp.377-386. https://doi.org/10.1023/A:1009681321708

61. Hsissou, D. & Bouharmont, J. (1994). In vitro selection and characterization of drought-tolerant plants of durum wheat (Triticum durum Desf.). Agronomie, No. 2, pp. 65-70. https://doi.org/10.1051/agro:19940201

62. Javed, F. (2002). In vitro salt tolerance in wheat I: Growth and ion accumulation. Int. J. Agr. Biol., 4, No. 4, pp. 458-461.

63. Koop, H., Herz, S., Golds, T. & Nickelson, J. (2007). The genetic transformation of plastids. In Cell and molecular biology of plastids (pp. 457-510). Berlin, Heidelberg: Springer-Verlag. https://doi.org/10.1007/4735_2007_0225

64. Leckband, G. & Lorz, H. (1998). Transformation and expression of a stilbene synthase gene of Vitis vinifera L. in barley and wheat for increased fungal resistance. Theor. Appl. Genet., 96, pp. 1004-1012. https://doi.org/10.1007/s001220050832

65. Li, Z., Mouille, G., Kosar-Hashemi, B., Rahman, S., Clarke, B., Gale, K., Appels, R. & Morell, M. (2000). The structure and expression of the wheat starch synthase III gene. Motifs in the expressed gene define the lineage of the starch synthase III gene family. Plant Physiol., 123, pp. 613-624. https://doi.org/10.1104/pp.123.2.613

66. Lu, W., Zhou, M. & Zhang, X. (2000, May). Studies and improvement of wheat breeding for scab resistance using biotechnology. Proceedings of the Intern. Symp. Wheat improvement for Scab resistance (pp.151-155). Sunghou and Nanjing, China.

67. Naqvi, S., Farre, G., Sanahuja, G., Capell, T., Zhu, C.& Christou, P. (2010). When more is better: multigene engineering in plants. Trends Plant Sci.,15, pp. 48-56. https://doi.org/10.1016/j.tplants.2009.09.010

68. Patnaik, D. & Khurana, P. (2001). Wheat biotechnology: A minireview plant biotechnology. Electronic J. Biotechnol., 4, pp. 74-102. https://doi.org/10.2225/vol4-issue2-fulltext-4

69. Pauly, M., Shane, W. & Gengenbach, B. (1987). Selection for bacterial blight phytotoxin resistance in wheat tissue culture. Crop. Sci., 27, No. 2, pp. 340-344. https://doi.org/10.2135/cropsci1987.0011183X002700020044x

70. Peremarti, A., Twyman, R., Gomez-Galera, S., Naqvi, S., Farre, G., Sabalza, M., Miralpeix, B., Dashevskaya, S., Yuan, D., Ramessar, K., Christou, P., Zhu, C., Bassie, L. & Capell, T. (2010). Promoter diversity in multigene transformation. Plant Mol. Biol., 73, pp. 363-378. https://doi.org/10.1007/s11103-010-9628-1

71. Ral, J., Bowerman, A. & Li, Z. (2012). Down-regulation of glucan, water-dikinase activity in wheat endosperm increases vegetative biomass and yield. Plant Biotechnol. J., 10, No. 7, pp. 871-882. https://doi.org/10.1111/j.1467-7652.2012.00711.x

72. Ramana, R., Parameswari, C., Sripriya, R. & Veluthambi, K. (2011). Transgene stacking and marker elimination in transgenic rice by sequential Agrobacterium-mediated co-transformation with the same selectable marker gene. Plant Cell Rep., 30, pp. 1241-1252. https://doi.org/10.1007/s00299-011-1033-y

73. Rooke, L., Bekes, F., Fido, R., Barro, F., Gras, P., Tatham, A., Barcelo, P., Lazzeri, P. & Shewry, P. (1990). Overexpression of a gluten protein in transgenic wheat results in greatly increased dough strength. J. Cereal Sci., 30, pp. 115-120. https://doi.org/10.1006/jcrs.1999.0265

74. Roudsari, M., Salmanian, A., Mousavi, A. Sohi, H. & Jafari, M. (2009). Regeneration of glyphosate-tolerant Nicotiana tabacum after plastid transformation with a mutated variant of bacterial aroA gene. Iran. J. Biotechnol., 7, pp. 247-253.

75. Shah D.M. (1997). Genetic engineering for fungal and bacterial diseases. Curr. Opin. Biotechnol., 8, pp. 208-214. https://doi.org/10.1016/S0958-1669(97)80104-8

76. Sharma, H., Sharma, K., Seetharama, N. & Ortiz, R. (2000). Prospects for using transgenic resistance to insects in crop improvement. Electronic J. Biotechnol. [online]. Available from: http: // www.ejb.org/content/vol3/issue2/full/3 ISSN 0717-3458. https://doi.org/10.2225/vol3-issue2-fulltext-3

77. Shawla, H. & Wenzel, G. (1987). In vitro selection of barley and wheat for resistance against Helminthosporium sativum. Theor. Appl. Genet., 74, pp. 841-845. https://doi.org/10.1007/BF00247566

78. Sigurbjoornsson, E. (1995). Application of in vitro mutation techniques for crop improvement. Euphytica, 85, pp. 303-315. https://doi.org/10.1007/BF00023960

79. Sivamani, E., Bahieldin, A., Wraith, J., Al-Niemi, T., Dyer, W., Ho, T. &, Qu, R. (2000). Improved biomass productivity and water use efficiency under water deficit conditions in transgenic wheat constitutively expressing the barley HVA1 gene. Plant Sci., 155, pp. 1-9. https://doi.org/10.1016/S0168-9452(99)00247-2

80. Stoger E., Vaquero, C., Torres, E., Sack, M., Nicholson, L., Drossard, J., Williams, S., Keen, D., Perrin, Y., Christou, P. & Fischer, R. (2004). Cereal crops as viable production and storage systems for pharmaceutical scFv antibodies. Plant Mol. Biol., 42, pp. 583-590. https://doi.org/10.1023/A:1006301519427

81. Taverniers, I., Papazova, N., Bertheau, Y., De Loose, M. & Holst-Jensen, A. (2008). Gene stacking in transgenic plants: towards compliance between definitions, terminology, and detection within the EU regulatory framework. Environ. Biosafety Res., 7, pp. 197-218. https://doi.org/10.1051/ebr:2008018

82. Tishchenko, O.M., Komisarenko, A.G., Mykhalska, S.I., Sergeeva, L.E., Adamenko, N.I., Morgun, B.V. & Kochetov, A.V. (2014). Agrobacterium-mediated transformation of sunflower (Helianthus annuus L.) in vitro and in planta using LBA4404 strain harboring binare vector pBi2E with dsRNA-supressor of proline dehydrogenase gene. Cytol. and Genet., 48, No. 4, pp. 19-30. https://doi.org/10.3103/S0095452714040094

83. Upadhyaya, C., Nookaraju, A., Gururani, M., Upadhaya, D., Kim, D., Chun, S. & Park, S (2010). An update on the progress towards the development of marker-free transgenic plants. Bot. Stud., 51, pp. 277-292.

84. Vain, P. (2007). Thirty years of plant transformation technology development. Plant Biotechnol. J., No. 5, pp. 221-229. https://doi.org/10.1111/j.1467-7652.2006.00225.x

85. Vasil, I. & Vasil, V. (2000). Transgenic cereals: Triticum aestivum (wheat). In Molecular Improvement of Cereal Crops (pp. 137-147). Dordrecht (Netherlands): Kluwer Academic Publishers https://doi.org/10.1007/978-94-011-4802-3_6

86. Vij, S. & Tyagi, A. (2007). Emerging trends in the functional genomics of the abiotic stress response in crop plants. Plant Biotechnol. J., 3, pp. 361-380. https://doi.org/10.1111/j.1467-7652.2007.00239.x

87. Wang, H., Yin, W. & Hu, Z. (2009). Advances in chloroplast engineering. J. Genet. Genomics, 36, pp. 387-398. https://doi.org/10.1016/S1673-8527(08)60128-9

88. Wang, W., Shang, X., Yucel, M. & Nguyen, H. (1993). Selection of cultured wheat cells for tolerance to high temperature stress. Crop. Sci., 33, pp. 315-320. https://doi.org/10.2135/cropsci1993.0011183X003300020020x

89. Weinthal, D., Tovkach, A., Zeevi, V. & Tzfira, T. (2010). Genome editing in plant cells by zinc finger nucleases. Trends Plant Sci., 15, pp. 308-321. https://doi.org/10.1016/j.tplants.2010.03.001

90. Wright, M., Dawson, J., Dunder, E., Suttiet, J., Reed, J., Kramer, C., Chang, Y., Novitzky, R., Wang, H. & Artim-Moore, L. (2001). Efficient biolistic transformation of maize (Zea mays L.) using the phosphomannose isomerase gene, pmi, as selectable marker. Plant Cell Rep., 20, pp. 429-436. https://doi.org/10.1007/s002990100318

91. Yang, Z., Yang, X. & Huang, D. (2006). Studies on somaclonal variants for resistance to scab in bread wheat (Triticum aestivum L.) through in vitro selection for tolerance to deoxynivalenol. Euphytica, 101, No. 2, pp. 213-219. https://doi.org/10.1023/A:1018354606939

92. Zair, I., Chlyah, A. & Sabounji, K. (2003). Salt tolerance improvement in some wheat cultivars after application of in vitro selection pressure. Plant Cell, Tissue Organ Cult., 73, No. 3, pp. 237-244. https://doi.org/10.1023/A:1023014328638

93. Zemetra, R., Schotzko, D., Smith, S. & Lauver, M. (1993). In vitro selection for Russian wheat aphid (Diuraphis noxia) resistance in wheat (Triticum aestivum). Plant Cell Rep., 12, No. 6., pp. 312-315. https://doi.org/10.1007/BF00237425