doi: 10.15389/agrobiology.2022.3.518eng

UDC: 635.64:579.254.2:581.143.6

Supported financially by assignments No. 0431-2022-0003 of the Ministry of Science and Higher Education of the Russian Federation



I.M. Mikhel1, M.R. Khaliluev1, 2 ✉

1All-Russian Research Institute of Agricultural Biotechnology, 42, ul. Timiryazevskaya, Moscow, 127550 Russia, e-mail, (✉ corresponding author);
2Timiryazev Russian State Agrarian University—Moscow Agrarian Academy, 49, ul. Timiryazevskaya, Moscow, 127550 Russia

Mikhel I.M.
Khaliluev M.R.

Received April 18, 2022

Tomato (Solanum lycopersicum L.) is the most important food crop which is also widely used as a model plant in molecular genetic investigations of vegetative development and reproductive biology, plant resistance to abiotic and biotic stresses, plant-microbe association and symbiosis, etc., that have both basic and applied value. The production of transgenic tomato plants expressing foreign heterologous genes, as well as with induced silencing or knockout of their own genes, is an important part of modern plant physiology. There are two radically different approaches to introducing foreign DNA into the tomato genome. The first method is based on the natural mechanism of infection with plant-associated bacterial pathogen Agrobacterium sp. (A. tumefaciens. or A. rhizogenes), followed by T-DNA transfer and insertion into the plant genome (Agrobacterim-mediated transformation). The second approach is based on the direct introducing of foreign DNA into the plant cells through the plasma membrane by chemical (Ca2+, polyethylene glycol, PEG) or physical exposure (electrical impulse or excessive pressure) (direct methods of tomato genetic transformation). Transgenic tomato plants can be produced both by the classical tissue culture-based transformation procedure and in planta transformation. This review article discusses classical direct methods for introducing foreign DNA into the tomato genome (chemical-mediated transfection, protoplast electroporation, microinjection, biolistic transformation), and in planta transformation methods (pollen-tube pathway, electroporation of mature seed embryo). The review considers features of producing tomato plants both with transient transgene expression and stably inherited insertion into the nuclear or plastid genomes are considered. In addition, the factors affecting the efficiency of transformation are analyzed in detail. A separate section is devoted to the direct tomato genetic transformation methods for delivering various genome editing tools (ZFNs, TALEN, CRISPR/Cas, base editing, prime editing) that have become widespread in the past five years.

Keywords: Solanum lycopersicum L., electroporation, PEG-mediated transformation, microinjection, biolistic transformation, transformation in planta, genome editing.



  1. FAO. FAOSTAT, 2021. Available: No date.
  2. Ron’zhina E.S., Podlesnova V.S. Izvestiya Gorskogo gosudarstvennogo agrarnogo universiteta, 2021, 58-3: 30-35 (in Russ.).
  3. Avdeev Yu.I. Kartofel’ i ovoshchi, 2014, 5: 7-9 (in Russ.).
  4. Sorokin A., Bryzzhev A., Strokov A., Mirzabaev A., Johnson T., Kiselev S.V. The economics of land degradation in Russia. In: Economics of land degradation and improvement – a global assessment for sustainable development. E. Nkonya, A. Mirzabaev, J. von Braun (eds). Springer, Cham., 2016: 541-576 CrossRef
  5. Salina Yu.B., Tyutyuma N.V., Tyutyuma A.V. Dostizheniya nauki i tekhniki APK, 2018, 32(12): 5-8 CrossRef (in Russ.).
  6. Lazarev A.M. Bakterial’nye bolezni tomata i mery bor’by s nimi [Bacterial diseases of tomato and their control]. St. Petersburg, 2015 (in Russ.).
  7. Blancard D. Tomato diseases. Academic Press, San Diego, CA, USA, 2012.
  8. Kigashpaeva O.P., Avdeev A.Yu. Problemy razvitiya APK regiona, 2020, 2: 93-97 CrossRef (in Russ.).
  9. Khaliluev M.R., Shpakovskii G.V. Genetic engineering strategies for enhancing tomato resistance to fungal and bacterial pathogens. Russian Journal of Plant Physiology, 2013, 60(6): 721-732 CrossRef
  10. Gerszberg A., Hnatuszko-Konka K., Kowalczyk T., Kononowicz A.K. Tomato (Solanum lycopersicum L.) in the service of biotechnology. Plant Cell Tissue and Organ Culture, 2015, 120: 881-902 CrossRef
  11. Anwar R., Fatima T., Mattoo A. Tomatoes: A model crop of Solanaceous plants. In: Oxford research encyclopedia of environmental science. Oxford University Press, Oxford, UK, 2019 CrossRef
  12. Chaban I., Khaliluev M., Baranova E., Kononenko N., Dolgov S., Smirnova E. Abnormal development of floral meristem triggers defective morphogenesis of generative system in transgenic tomatoes. Protoplasma, 2018, 255(6): 1597-1611 CrossRef
  13. Vershinina Z.R., Blagova D.K., Nigmatullina L.R. Lavina A.M., Baymiev A.Kh., Chemeris A.V. Biotekhnologiya, 2015, 31(3): 42-53 (in Russ.).
  14. Arie T., Takahashi H., Kodama M., Teraoka T. Tomato as a model plant for plant-pathogen interactions. Plant Biotechnology, 2007, 24(1): 135-147 CrossRef
  15. Vershinina Z.R., Chubukova O.V., Maslennikova D.R. Fiziologiya rasteniy, 2021, 68(5): 524-532 CrossRef (in Russ.).
  16. Komakhin R.A., Komakhina V.V., Milyukova N.A., Goldenkova-Pavlova I.V., Fadina O.A., Zhuchenko A.A. Genetika, 2010, 46(12): 1635-1644 (in Russ.).
  17. Rothan C., Diouf I., Causse M. Trait discovery and editing in tomato. The Plant Journal, 2019, 97(1): 73-90 CrossRef
  18. Salim M.M.R., Rashid M.H., Hossain M.M., Zakaria, M. Morphological characterization of tomato (Solanum lycopersicum L.) genotypes. Journal of the Saudi Society of Agricultural Sciences, 2020, 19: 233-240 CrossRef
  19. Renna M., D’Imperio M., Gonnella M., Durante M., Parente A., Mita G., Santamaria P., Serio F. Morphological and chemical profile of three tomato (Solanum lycopersicum L.) landraces of a semi-arid Mediterranean environment. Plants, 2019, 8(8): 273 CrossRef
  20. Causse M., Giovannoni J., Bouzayen M., Zouine M. The Tomato Genome. Compendium of Plant Genomes. Springer, Berlin, Heidelberg, 2016 CrossRef
  21. The Tomato Genome Consortium. The tomato genome sequence provides insights into fleshy fruit evolution. Nature, 2012, 485: 635-641 CrossRef
  22. Bhatia P., Ashwath N., Senaratna T., Midmore D. Tissue culture studies of tomato (Lycopersicon esculentum). Plant Cell Tissue and Organ Culture, 2004, 78: 1-21 CrossRef
  23. Gavrish S.F. Izvestiya Timiryazevskoy sel’skokhozyaystvennoy akademii, 1992, 5: 147-161 (in Russ.).
  24. Bukharova A.R., Bukharov A.F. Otdalennaya gibridizatsiya ovoshchnykh paslenovykh kul’tur [Distant hybridization of nightshade vegetable crops]. Michurinsk, 2008 (in Russ.).
  25. Rommens C.M., Kishore G.M. Exploiting the full potential of disease-resistance genes for agricultural use. Current Opinion in Biotechnology, 2000, 11(2): 120-125 CrossRef
  26. Bock R. Engineering plastid genomes: methods, tools, and applications in basic research and biotechnology. Annual Review of Plant Biology, 2015, 66: 211-241 CrossRef
  27. Adem M., Beyene D., Feyissa T. Recent achievements obtained by chloroplast transformation. Plant Methods, 2017, 13(1): 30 CrossRef
  28. Ruf S., Hermann M., Berger I.J., Carrer H., Bock R. Stable genetic transformation of tomato plastids and expression of a foreign protein in fruit. Nature Biotechnology, 2001, 19(9): 870-875 CrossRef
  29. Staub J.M., Maliga P. Long regions of homologous DNA are incorporated into the tobacco plastid genome by transformation. The Plant Cell, 1992, 4(1): 39-45 CrossRef
  30. Kaplanoglu E., Kolotilin I., Menassa R., Donly C. Plastid transformation of Micro-Tom tomato with a hemipteran double-stranded RNA results in RNA interference in multiple insect species. International Journal of Molecular Sciences, 2022, 23(7): 3918 CrossRef
  31. Rogalski M., do Nascimento Vieira L., Fraga H.P., Guerra M.P. Plastid genomics in horticultural species: importance and applications for plant population genetics, evolution, and biotechnology. Frontiers in Plant Science, 2015, 6: 586 CrossRef
  32. Saveleva N.V., Burlakovskiy M.S., Yemelyanov V.V., Lutova L.A. Transgenic plants as bioreactors to produce substances for medical and veterinary uses. Russian Journal of Genetics: Applied Research, 2016, 6(6): 712-724 CrossRef
  33. Rozov S.M., Sidorchuk Y.V., Deineko E.V. Transplastomic plants: problems of production and their solution. Russian Journal of Plant Physiology, 2022, 69(2): 1-10 CrossRef
  34. Zagorskaya A.A., Deineko E.V. Plant-expression systems: a new stage in production of biopharmaceutical preparations. Russian Journal of Plant Physiology, 2021, 68(1): 17-30 CrossRef
  35. Gelvin S.B. Plant DNA repair and Agrobacterium T-DNA integration. International Journal of Molecular Sciences, 2021, 22(16): 8458 CrossRef
  36. Hwang H.H., Yu M., Lai E.M. Agrobacterium-mediated plant transformation: biology and applications. The Arabidopsis Book,2017, 15: e0186 CrossRef
  37. Anand A., Jones T.J. 2018 Advancing Agrobacterium-based crop transformation and genome modification technology for agricultural biotechnology. In: Agrobacterium Biology. Current Topics in Microbiology and Immunology. V. 418 /S.B. Gelvin (ed.). Springer, Cham., 2018: 489-507 CrossRef
  38. Chyi Y.S., Jorgensen R.A., Goldstein D., Tanksley S.D., Loaiza-Figueroa F. Locations and stability of Agrobacterium-mediated T-DNA insertions in the Lycopersicon genome. Molecular and General Genetics, 1986, 204(1): 64-69 CrossRef
  39. Saifi S.K., Passricha N., Tuteja R., Kharb P., Tuteja N. In planta transformation: A smart way of crop improvement. In: Advancement in crop improvement techniques. N. Tuteja, R. Tuteja, N. Passricha (eds.). Woodhead Publishing, Sawston, Cambridge, 2020: 351-362 CrossRef
  40. Keshavareddy G., Kumar A.R.V., Ramu V.S. Methods of plant transformation-a review. International Journal of Current Microbiology and Applied Sciences, 2018, 7(7): 2656-2668 CrossRef
  41. Marenkova T.V., Loginova D.B., Deineko E.V. Mosaic patterns of transgene expression in plants. Russian Journal of Genetics, 2012, 48(3): 249-260 CrossRef
  42. Xia X., Cheng X., Li R., Yao J., Li Z., Cheng Y. Advances in application of genome editing in tomato and recent development of genome editing technology. Theoretical and Applied Genetics, 2021, 134(9): 2727-2747 CrossRef
  43. Gaj T., Gersbach C.A., Barbas C.F. ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends in Biotechnology, 2013, 31: 397-405 CrossRef
  44. Khan Z., Khan S.H., Mubarik, Sadia B., Ahmad A. Use of TALEs and TALEN Technology for Genetic Improvement of Plants. Plant Molecular Biology Reporter, 2017, 35: 1-19 CrossRef
  45. Petolino J.F. Genome editing in plants via designed zinc finger nucleases. In Vitro Cellular & Developmental Biology - Plant, 2015, 51(1): 1-8 CrossRef
  46. Sardesai N., Subramanyam S. Agrobacterium: a genome-editing tool-delivery system. In: Agrobacterium biology. Current Topics in microbiology and immunology. V. 418. S.B. Gelvin (ed.). Springer, Cham., 2018: 463-488 CrossRef
  47. Ruf S., Bock R. Plastid Transformation in Tomato. In: Chloroplast biotechnology. Methods in molecular biology (methods and protocols). V. 1132. P. Maliga (ed.). Humana Press, Totowa, NJ., 2014: 265-276 CrossRef
  48. Gleba Yu.Yu., Khasanov M.M., Slyusarenko A.G., Butenko R.G., Vinetskiy Yu.P. Doklady AN SSSR, 1974, 219(4-6): 1478-1481 (in Russ.).
  49. Ohyama K., Gamborg O.L., Miller R.A. Uptake of exogenous DNA by plant protoplasts. Canadian Journal of Botany, 1972, 50(10): 2071-2080 CrossRef
  50. Graham F.L., Van der Eb A.J. A new technique for the assay of infectivity of human adenovirus 5 DNA. Virology, 1973, 52: 456-467 CrossRef
  51. Jongsma M., Koornneef M., Zabel P., Hille J. Tomato protoplast DNA transformation: physical linkage and recombination of exogenous DNA sequences. Plant Molecular Biology, 1987, 8(5): 383-394 CrossRef
  52. Negrutm I., Shillito R., Potrykus I., Biasini G., Sala F. Hybrid genes m the analysis of transformation conditions. I. Setting up a simple method for direct gene transfer m plant protoplasts. Plant Molecular Biology, 1987, 8: 363-373 CrossRef
  53. Nugent G.D., ten Have M., van der Gulik A., Dix P.J., Uijtewaal B.A., Mordhorst A.P. Plastid transformants of tomato selected using mutations affecting ribosome structure. Plant Cell Reports, 2005, 24: 341-349 CrossRef
  54. Ray S., Lahiri S., Halder M., Mondal M., Choudhuri T.R., Kundu S. An efficient method of isolation and transformation of protoplasts from tomato leaf mesophyll tissue using the binary vector pCambia 1302. International Advanced Research Journal in Science, Engineering and Technology, 2015, 2: 146-150 CrossRef
  55. Diacumakos E.G. Methods of micromanipulation of human somatic cells in culture. In: Methods in cell biology. V. 7 /D.M. Prescott (ed.). Academic Press, New York, 1974: 287-312 CrossRef
  56. Capecchi M.R. High efficiency transformation by direct microinjection of DNA into cultured mammalian cells. Cell, 1980, 22(2): 479-488 CrossRef
  57. Griesbach R.J. Protoplast microinjection. Plant Molecular Biology Reporter, 1983, 1(4): 32-37 CrossRef
  58. Steinbiss H.H., Stabel P. Protoplast derived tobacco cells can survive capillary microinjection of the fluorescent dye Lucifer Yellow. Protoplasma, 1983, 116(2): 223-227 CrossRef
  59. Morikawa H., Yamada Y. Capillary microinjection into protoplasts and intranuclear localization of injected materials. Plant and Sell Physiology, 1985, 26(2): 229-236 CrossRef
  60. Griesbach R.J., Sink K.C. Evacuolation of mesophyll protoplasts. Plant Science Letters, 1983, 30(3): 297-301 CrossRef
  61. Spangenberg G., Koop H.U., Lichter R., Schweiger H.G. Microculture of single protoplasts of Brassica napus. Physiologia Plantarum, 1986, 66(1): 1-8 CrossRef
  62. Griesbach R.J. Chromosome-mediated transformation via microinjection. Plant Science, 1987, 50(1): 69-77 CrossRef
  63. Schnorf M., Neuhaus-Url G., Galli A., Iida S., Potrykus I., Neuhaus G. An improved approach for transformation of plant cells by microinjection: molecular and genetic analysis. Transgenic Research, 1991, 1(1): 23-30 CrossRef
  64. Holm P.B., Olsen O., Schnorf M., Brinch-Pedersen H., Knudsen S. Transformation of barley by microinjection into isolated zygote protoplasts. Transgenic Research, 2000, 9(1): 21-32 CrossRef
  65. Toyoda H., Matsuda Y., Utsumi R., Ouchi S. Intranuclear microinjection for transformation of tomato callus cells. Plant Cell Reports, 1988, 7(5): 293-296 CrossRef
  66. Reich T.J., Iyer V.N., Miki B.L. Efficient transformation of alfalfa protoplasts by the intranuclear microinjection of Ti plasmids. Nature Biotechnology, 1986, 4(11): 1001-1004 CrossRef
  67. Okada K., Nagata T., Takebe I. Introduction of functional RNA into plant protoplasts by electroporation. Plant and Cell Physiology, 1986, 27(4): 619-626 CrossRef
  68. Chen C., Smye S.W., Robinson M.P., Evans J.A. Membrane electroporation theories: a review. Medical and Biological Engineering and Computing, 2006, 44(1-2): 5-14 CrossRef
  69. Kotnik T., Frey W., Sack M., Haberl Meglič S., Peterka M., Miklavčič D. Electroporation-based applications in biotechnology. Trends in Biotechnology, 2015, 33: 480-488 CrossRef
  70. Kotnik T., Rems L., Tarek M., Miklavčič D. Membrane electroporation and electropermeabilization: mechanisms and models. Annual Review of Biophysics, 2019, 48: 63-91 CrossRef
  71. Reberšek M., Faurie C., Kandušer M., Čorović S., Teissié J., Rols M.P., Miklavčič D. Electroporator with automatic change of electric fled direction improves gene electrotransfer in-vitro. BioMedical Engineering OnLine, 2007, 6(1): 1-11 CrossRef
  72. Hanze J., Fischer L., Koenen M., Worgall S., Rascher W. Electroporation of nucleic acids into prokaryotic and eukaryotic cells by square wave pulses. Biotechnology Techniques, 1998, 12(2): 159-163 CrossRef
  73. Kotnik T., Pucihar G., Miklavčič D. Induced transmembrane voltage and its correlation with electroporation-mediated molecular transport. Journal of Membrane Biology, 2010, 236: 3-13 CrossRef CrossRef
  74. Gurel F., Gozukirmizi N. Electroporation transformation of barley. In: Genetic transformation of plants. Molecular methods of plant analysis. V. 23. J.F. Jackson, H.F. Linskens (eds.). Springer, Berlin, 2003: 69-89 CrossRef
  75. Nakata K., Tanaka H., Yano K., Takagi M. An effective transformation system for Lycopersicon peruvianum by electroporation. Japanese Journal of Breeding, 1992, 42(3): 487-495 CrossRef
  76. Sherba J.J., Hogquist S., Lin H., Shan J.W., Shreiber D.I., Zahn J.D. The effects of electroporation buffer composition on cell viability and electro-transfection efficiency. Scientific Reports, 2020, 10(1): 3053 CrossRef
  77. Azencott H.R., Peter G.F., Prausnitz M.R. Influence of the cell wall on intracellular delivery to algal cells by electroporation and sonication. Ultrasound in Medicine & Biology, 2007, 33(11): 1805-1817 CrossRef
  78. Ortiz-Matamoros M.F., Villanueva M.A., Islas-Flores T. Genetic transformation of cell-walled plant and algae cells: delivering DNA through the cell wall. Briefings in Functional Genomics, 2018, 17(1): 26-33 CrossRef
  79. D’Halluin K., Bonne E., Bossut M., De Beuckeleer M., Leemans J. Transgenic maize plants by tissue electroporation. The Plant Cell, 1992, 4(12): 1495-1505 CrossRef
  80. Bellini C., Chupeau M.C., Guerche P., Vastra G., Chupeau Y. Transformation of Lycopersicon peruvianum and Lycopersicon esculentum mesophyll protoplasts by electroporation. Plant Science, 1989, 65(1): 63-75 CrossRef
  81. Tsukada M., Kusano T., Kitagawa Y. Introduction of foreign genes into tomato protoplasts by electroporation. Plant and Cell Physiology, 1989, 30(4): 599-603 CrossRef
  82. Sanford J.C., Klein T.M., Wolf E.D. Delivery of substances into cells and tissues using a particle bombardment process. Particulate Science and Technology, 1987, 5: 27-37 CrossRef
  83. Van Eck J.M., Blowers A.D., Earle E.D. Stable transformation of tomato cell cultures after bombardment with plasmid and YAC DNA. Plant Cell Reports, 1995, 14(5): 299-304 CrossRef
  84. Ruma D., Dhaliwal M.S., Kaur A., Gosal S.S. Transformation of tomato using biolistic gun for transient expression of the β-glucuronidase gene. Indian Journal of Biotechnology, 2009, 8(4): 363-369.
  85. Guillet C., Aboul-Soud M.A., Le Menn A., Viron N., Pribat A., Germain V., Just D., Baldet P., Rousselle P., Lemaire-Chamley M., Rothan C. Regulation of the fruit-specific PEP carboxylase SlPPC2 promoter at early stages of tomato fruit development. PLoS ONE, 2012, 7(5): e36795 CrossRef
  86. Sun L., Liu S., Ren J., Cui M., Wang L., Leng P. Optimization of particle bombardment conditions by b-glucuronidase (GUS) reporter system in tomato fruit. African Journal of Biotechnology, 2011, 10(4): 675-683 CrossRef
  87. Stolbikov A.S., Salyaev R.K., Rekoslavskaya N.I., Tret’yakova A.V. Izvestiya Irkutskogo gosudarstvennogo universiteta. Seriya: Biologiya. Еkologiya, 2015, 13: 2-8 (in Russ.).
  88. Stolbikov A.S., Salyaev R.K., Rekoslavskaya N.I. MaterialyVserossiiskoynauchno-prakticheskoykonferentsii s mezhdunarodnym uchastiem i shkoly molodykh uchenykh «Mekhanizmy ustoychivosti rasteniy i mikroorganizmov k neblagopriyatnym usloviyam sredy» [Proc. Russian Conf. «Mechanisms of resistance of plants and microorganisms to adverse environmental conditions»]. Irkutsk, 2018: 1378-1380 (in Russ.).
  89. Baum K., Gröning B., Meier I. Improved ballistic transient transformation conditions for tomato fruit allow identification of organ‐specific contributions of I‐box and G‐box to the RBCS2 promoter activity. The Plant Journal, 1997, 12(2): 463-469 CrossRef
  90. Wurbs D., Ruf S., Bock R. Contained metabolic engineering in tomatoes by expression of carotenoid biosynthesis genes from the plastid genome. The Plant Journal, 2007, 49(2): 276-288 CrossRef
  91. Abu-El-Heba G.A., Hussein G.M., Abdalla N.A. A rapid and efficient tomato regeneration and transformation system. Landbauforschung Volkenrode, 2008, 58: 103-110.
  92. Abbas D.E., Abdallah N.A., Madkour M.M. Production of transgenic tomato plants with enhanced resistance against the fungal pathogen Fusarium oxysporum. Arabian Journal of Biotechnology, 2009, 12(1): 73-84.
  93. Abdallah N.A., Shah D., Abbas D., Madkour M. Stable integration and expression of a plant defensin in tomato confers resistance to fusarium wilt. GM Crops, 2010, 1(5): 344-350 CrossRef
  94. Jiménez V.A.O., Varela G.B., Domínguez M.R., Sañudo R.B., Rojas R.T., Hernández M.E.T. Development of a regeneration and genetic transformation protocol for tomato (Solanum lycopersicum L.) cv. Rutgers. Agrociencia, 2019, 53(5): 725-740.
  95. Kaplanoglu E., Kolotilin I., Menassa R., Donly C. Transplastomic tomato plants expressing insect-specific double-stranded RNAs: a protocol based on biolistic transformation. In: RNAi strategies for pest management. Humana, NY, 2022: 235-252 CrossRef
  96. Rajkumari N., Alex S., Soni K.B., Anith K.N., Viji M.M., Kiran A.G. Silver nanoparticles for biolistic transformation in Nicotiana tabacum L. 3 Biotech, 2021, 11(12): 497 CrossRef
  97. Sanford J.C., Wolf E.D. Apparatus for transporting substances into living cells and tissues. US Patent № 5 371 015, December 6 1994.
  98. McCabe D., Christou P. Direct DNA transfer using electric discharge particle acceleration (ACCELL™ technology). Plant Cell, Tissue and Organ Culture, 1993, 33(3): 227-236 CrossRef
  99. Finer J.J., Vain P., Jones M.W., McMullen M.D. Development of the particle inflow gun for DNA delivery to plant cells. Plant Cell Reports, 1992, 11(7): 323-328 CrossRef
  100. Sautter C., Waldner H., Neuhaus-Url G., Galli A., Neuhaus G., Potrykus I. Micro-targeting: high efficiency gene transfer using a novel approach for the acceleration of micro-projectiles. Nature Biotechnology, 1991, 9(11): 1080-1085 CrossRef
  101. Finer J.J., Finer K.R., Ponappa T. Particle bombardment mediated transformation. In: Plant biotechnology. Current topics in microbiology and immunology. V. 240. J. Hammond, P. McGarvey, V. Yusibov (eds.). Springer, Berlin, Heidelberg, 2000: 59-80 CrossRef
  102. Chaithra N., Gowda R.P.H., Guleria N. Transformation of tomato with Cry2ax1 by biolistic gun method for fruit borer resistance. International Journal of Agriculture, Environment and Biotechnology, 2015, 8(4): 795-803 CrossRef
  103. Zhimulev I.F. Obshchaya i molekulyarnaya genetika [General and molecular genetics]. Novosibirsk, 2003 (in Russ.).
  104. Russell J.A., Roy M.K., Sanford J.C. Major improvements in biolistic transformation of suspension-cultured tobacco cells. In Vitro Cellular & Developmental Biology - Plant, 1992, 28(2): 97-105 CrossRef
  105. Trujillo-Moya C., Gisbert C., Vilanova S., Nuez F. Localization of QTLs for in vitro plant regeneration in tomato. BMC Plant Biology, 2011, 11: 140 CrossRef
  106. Pino L.E., Lombardi-Crestana S., Azevedo M.S., Scotton D.C., Borgo L., Quecini V., Figueira A., Peres L.E. The Rg1 allele as a valuable tool for genetic transformation of the tomato ‘Micro-Tom’ model system. Plant Methods, 2010, 6(1): 23 CrossRef
  107. Lech M., Miczyński K., Pindel A. Comparison of regeneration potentials in tissue cultures of primitive and cultivated tomato species (Lycopersicon sp.). Acta Societatis Botanicorum Poloniae, 1996, 65(1-2): 53-56 CrossRef
  108. Khaliluev M.R., Bogoutdinova L.R., Baranova G.B., Baranova E.N., Kharchenko P.N., Dolgov S.V. Influence of genotype, explant type, and component of culture medium on in vitro callus induction and shoot organogenesis of tomato (Solanum lycopersicum L.). Biology Bulletin, 2014, 41(6): 512-521 CrossRef
  109. Klein T.M., Gradziel M.E., Fromm M., Sanford J.C. Factors influencing gene delivery into Zea mays cells by high-velocity microprojectiles. Nature Biotechnology, 1988, 6: 559-563 CrossRef
  110. Krishna H., Alizadeh M., Singh D., Singh U., Chauhan N., Eftekhari M., Sadh R.K. Somaclonal variations and their applications in horticultural crops improvement. 3 Biotech, 2016, 6(1): 54 CrossRef
  111. Ranghoo-Sanmukhiya V.M. Somaclonal variation and methods used for its detection. In: Propagation and genetic manipulation of plants. I. Siddique (ed.). Springer, Singapore, 2021: 59-68 CrossRef
  112. Chesnokov Yu.V. Nasledstvennye izmeneniya, vyzvannye perenosom еkzogennoy DNK v vysshie rasteniya posredstvom prorastayushchey pyl’tsy. Doktorskaya dissertatsiya [Hereditary changes caused by the transfer of exogenous DNA into higher plants through germinating pollen. DSc Thesis]. Minsk, 2000 (in Russ.).
  113. Chesnokov Yu.V. Biopolimery i kletka, 1992, 8(2): 53-58 (in Russ.).
  114. Kaur R.P., Devi S. In planta transformation in plants: a review. Agricultural Reviews, 2019, 40(3): 159-174 CrossRef
  115. Hess D., Lorz H., Weissert E.-W. Die Aufnahme bakterieller DNA in quellende und keimende Pollen von Petunia hybrid und Nicotiana glauca [Uptake of bacterial DNA into swelling and germinating pollen grains of Petunia hybrid and Nicotiana glauca]. Zeitschrift fur Pflanzenphysiologie, 1974, 74(1): 52-63 CrossRef
  116. Hess D., Gresshoff P.M., Fielits U., Gleiss D. Uptake of protein and bacteriophage into swelling and germinating pollen of Petunia hybrida. Zeitschrift fur Pflanzenphysiologie, 1975, 74(4): 371-376 CrossRef
  117. Turbin N.V., Soyfer V.N., Kartel’ N.A., Chekalin N.M., Dorohov Y.L., Titov Y.B., Cieminis K.K. Genetical change of waxy barley mutant after treatment with normal DNA. Sel'skokhozyaistvennaya biologiya [Agricultural Biology], 1974, 9(6): 204-215 (in Russ.).
  118. Zhou G.Y., Weng J., Zeng Y., Huang J., Qian S., Liu G. Introduction of exogenous DNA into cotton embryos. In: Methods in enzymology. V. 101. Academic Press, 1983: 433-481 CrossRef
  119. Kartеl’ M.A., Zabyan’kova K.I. Genetychnyya zmeny і magchymy mekhanіzm іkh uznіknennya pad dzeyannem DNK u raslіn. Vestsіnatsyyanal’nayakadеmііnavukBelarusі. Seryyabіyalagіchnykhnavuk, 1984, 6: 42-46.
  120. De la Pena A., Lorz H., Schell J. Transgenic rye plants obtained by injecting DNA into young floral tillers. Nature, 1987, 325(6101): 274-276 CrossRef
  121. Chesnokov Yu.V., Sedov G.I., Vikonskaya N.A. Izvestiya AN MSSR, 1989, 6: 61-62 (in Russ.).
  122. Chen D.P., Yu L.J. Establishment of tomato transformation technique via the pollen tube pathway method. Northern Horticulture, 2010, 14: 131-135.
  123. Xiaoxia J., Li W., Yu L. Transgenic technology of pollen-tube pathway in tomato (Solanum lycopersicum M.). Molecular Plant Breeding, 2013, 11(4): 605-610.
  124. Wang R., Li R., Xu T., Li T. Optimization of the pollen-tube pathway method of plant transformation using the Yellow Cameleon 3.6 calcium sensor in Solanum lycopersicum. Biologia, 2017, 72(10): 1147-1155 CrossRef
  125. Chesnokov Yu.V., Sedov G.I., Vikonskaya N.A. Genetika, 1995, 31(5): 648-691 (in Russ.).
  126. Wang Y., Shen J. Probing into cytological embryology mechanism of pollen-tube pathway transgenic technology. Acta Botanica Boreali-Occidentalia Sinica, 2005, 26: 628-634.
  127. Luo Z.-X., Wu R. A simple method for the transformation of rice via the pollen-tube pathway. Plant Molecular Biology Report, 1988, 6: 165-174 CrossRef
  128. Jian C., Li K., Ou W. Research progress in pollen-tube pathway method in transgenic plants. Chinese Journal of Tropical Crops, 2012, 33(5): 956-961.
  129. Bechtold N., Ellis J., Pelletier G. In planta Agrobacterium mediated gene transfer by infiltration of adult Arabidopsis thaliana plants. Comptes Rendus de L’Académie des Sciences Serie III-Sciences De La Vie-Life Sciences, 1993, 316: 1194-1199.
  130. Bent A.F., Clough S.J. Agrobacterium germ-line transformation: transformation of Arabidopsis without tissue culture. In: Plant molecular biology manual. S.B. Gelvin, R.A. Schilperoort (eds.). Springer, Dordrecht, 1998: 17-30 CrossRef
  131. Bent A. Arabidopsis thaliana floral dip transformation method. In: Agrobacterium protocols. Methods in molecular biology. V. 343. K. Wang (ed.). Humana Press, 2006: 87-104 CrossRef
  132. Yasmeen A., Mirza B., Inayatullah S., Safdar N., Jamil M., Ali S., Choudhry M.F. In planta transformation of tomato. Plant Molecular Biology Reporter, 2009, 27: 20-28 CrossRef
  133. Hilioti Z., Ganopoulos I., Ajith, S., Bossis I., Tsaftaris A. A novel arrangement of zinc finger nuclease system for in vivo targeted genome engineering: the tomato LEC1-LIKE4 gene case. Plant Cell Reports, 2016, 35(11): 2241-2255 CrossRef
  134. Kuz’mina Yu.V. Biotekhnologiya i selektsiya rasteniy, 2020, 3(1): 31-39 CrossRef (in Russ.).
  135. Kuluev B.R., Gumerova G.R., Mikhaylova E.V., Gerashchenkov G.A., Rozhnova N.A., Vershinina Z.R., Khyazev A.V., Matniyazov R.T., Baymiev A.K., Chemeris A.V. Delivery of CRISPR/Cas components into higher plant cells for genome editing. Russian Journal of Plant Physiology, 2019, 66(5): 694-706 CrossRef
  136. Nemudryi A.A., Valetdinova K.R., Medvedev S.P., Zakian S.M. TALEN and CRISPR/Cas genome editing systems: tools of discovery. Acta Naturae, 2014, 6(3): 19-40.
  137. Gerashchenkov G.A., Rozhnova N.A., Kuluev B.R., Kiryanova O.Yu., Gumerova G.R., Knyazev A.V., Vershinina Z.R., Mikhailova E.V., Chemeris D.A., Matniyazov R.T., Baimiev A.Kh., Gubaidullin I.M., Baimiev A.Kh., Chemeris A.V. Design of guide RNA for CRISPR/Cas plant genome editing. Molecular Biology, 2020, 54(1): 24-42 CrossRef
  138. Malzahn A., Lowder L., Qi Y. Plant genome editing with TALEN and CRISPR. Cell & Bioscience, 2017, 7(1): 21 CrossRef
  139. Zhan X., Lu Y., Zhu J.K., Botella J.R. Genome editing for plant research and crop improvement. Journal of Integrative Plant Biology, 2021, 63(1): 3-33 CrossRef
  140. Feder A., Jensen S., Wang A.Q., Courtney L., Middleton L., Van Eck J., Liu Y.S., Giovannoni J.J. Tomato fruit as a model for tissue-specific gene silencing in crop plants. Horticulture Research, 2020, 7: 142 CrossRef
  141. Liu L., Zhang J., Xu J., Li Y., Guo L., Wang Z., Zhang X., Zhao B., Guo Y.D., Zhang N. CRISPR/Cas9 targeted mutagenesis of SlLBD40, a lateral organ boundaries domain transcription factor, enhances drought tolerance in tomato. Plant Science, 2020, 301: 110683 CrossRef
  142. Danilo B., Perrot L., Mara K., Botton E., Nogué F., Mazier M. Efficient and transgene-free gene targeting using Agrobacterium-mediated delivery of the CRISPR/Cas9 system in tomato. Plant Cell Reports, 2019, 38(4): 459-462 CrossRef
  143. Nekrasov V., Wang C., Win J., Lanz C., Weigel D., Kamoun S. Rapid generation of a transgene-free powdery mildew resistant tomato by genome deletion. Scientific Reports, 2017, 7(1): 482 CrossRef
  144. Ortigosa A., Gimenez-Ibanez S., Leonhardt N., Solano R. Design of a bacterial speck resistant tomato by CRISPR/Cas9-mediated editing of SlJAZ2. Plant Biotechnology Journal, 2019, 17: 665-673 CrossRef
  145. Martínez M.I.S., Bracuto V., Koseoglou E., Appiano M., Jacobsen E., Visser R.G., Wolters A.A., Bai Y. CRISPR/Cas9-targeted mutagenesis of the tomato susceptibility gene PMR4 for resistance against powdery mildew. BMC Plant Biology, 2020, 20(1): 284 CrossRef
  146. Yoon Y.J., Venkatesh J., Lee J.H., Kim J., Lee H.E., Kim D.S., Kang B.C. Genome editing of eIF4E1 in tomato confers resistance to pepper mottle virus. Frontiers in Plant Science, 2020, 11: 1098 CrossRef
  147. Ito Y., Sekiyama Y., Nakayama H., Nishizawa-Yokoi A., Endo M., Shima Y., Nakamura N., Kotake-Nara E., Kawasaki S., Hirose S., Toki S. Allelic mutations in the Ripening-inhibitor locus generate extensive variation in tomato ripening. Plant Physiology, 2020, 183: 80-95 CrossRef
  148. Li S., Xu H.J.L., Ju Z., Cao D.Y., Zhu H.L., Fu D.Q., Grierson D., Qin G.Z., Luo Y.B., Zhu B.Z. The RIN-MC fusion of MADS-box transcription factors has transcriptional activity and modulates expression of many ripening genes. Plant Physiology, 2018, 176: 891-909 CrossRef
  149. Hunziker J., Nishida K., Kondo A., Kishimoto S., Ariizumi T., Ezura H. Multiple gene substitution by Target-AID base-editing technology in tomato. Scientific Reports, 2020, 10(1): 20471 CrossRef
  150. Nonaka S., Arai C., Takayama M., Matsukura C., Ezura H. Efficient increase of gamma-aminobutyric acid (GABA) content in tomato fruits by targeted mutagenesis. Scientific Reports, 2017, 7: 7057 CrossRef
  151. Deng L., Wang H., Sun C.L., Li Q., Jiang H.L., Du M.M., Li C.B., Li C.Y. Efficient generation of pink-fruited tomatoes using CRISPR/Cas9 system. Journal of Genetics and Genomics, 2018, 45: 51-54 CrossRef
  152. D’Ambrosio C., Stigliani A.L., Giorio G. CRISPR/Cas9 editing of carotenoid genes in tomato. Transgenic Research, 2018, 27(4): 367-378 CrossRef
  153. Zsögön A., Čermák T., Naves E.R., Notini M.M., Edel K.H., Weinl S., Freschi L., Voytas D.F., Kudla J., Peres L.E.P. De novo domestication of wild tomato using genome editing. Nature Biotechnology, 2018, 36(12): 1211-1216 CrossRef
  154. Li T., Yang X., Yu Y., Si X., Zhai X., Zhang H., Dong W., Gao C., Xu C. Domestication of wild tomato is accelerated by genome editing. Nature Biotechnology, 2018, 36: 1160-1163 CrossRef
  155. Čermák T., Baltes N.J., Čegan R., Zhang Y., Voytas D.F. High-frequency, precise modification of the tomato genome. Genome Biology, 2015, 16(1): 232 CrossRef
  156. Nicolia A., Andersson M., Hofvander P., Festa G., Cardi T. Tomato protoplasts as cell target for ribonucleoprotein (RNP)-mediated multiplexed genome editing. Plant Cell, Tissue and Organ Culture, 2021, 144(2): 463-467 CrossRef
  157. Lin Y. C. DNA-free CRISPR-Cas9 gene editing of wild tetraploid tomato Solanum peruvianum using protoplast regeneration. Plant Physiology, 2022, 188(4): 1917-1930 CrossRef
  158. Lu Y., Tian Y., Shen R., Yao Q., Zhong D., Zhang X., Zhu J. K. Precise genome modification in tomato using an improved prime editing system. Plant Biotechnology Journal, 2021, 19(3): 415-417 CrossRef







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