vir-nwТруды по прикладной ботанике, генетике и селекцииProceedings on applied botany, genetics and breeding2227-88342619-0982N.I. Vavilov All-Russian Institute of Plant Genetic Resources10.30901/2227-8834-2024-3-256-264vir-nw-2045Research ArticleОБЗОРЫSURVEYSМежвидовая гибридизация и клеточная инженерия салата (Lactuca L.)Interspecific hybridization and cell engineering of lettuce (Lactuca L.)https://orcid.org/0009-0000-7079-3278ЗагнухинаН. А.ZagnukhinaN. A.

Наталья Андреевна Загнухина, и. о. младшего научного сотрудника 

190000, Санкт-Петербург, ул. Б. Морская, 42, 44

Natalia A. Zagnukhina, Acting Associate Researcher 

42, 44 Bolshaya Morskaya Street, St. Petersburg 190000

nzagnuhina97@gmail.comhttps://orcid.org/0000-0002-3197-4751КуринаА. Б.KurinaA. B.

Анастасия Борисовна Курина, кандидат биологических наук, старший научный сотрудник, и. о. заведующего лабораторией 

190000, Санкт-Петербург, ул. Б. Морская, 42, 44

Anastasia B. Kurina, Cand. Sci. (Biol.), Senior Researcher, Acting Head of a Laboratory 

42, 44 Bolshaya Morskaya Street, St. Petersburg 190000

a.kurina@vir.nw.ruФедеральный исследовательский центр Всероссийский институт генетических ресурсов растений имени Н.И. ВавиловаРоссияN.I. Vavilov All-Russian Institute of Plant Genetic ResourcesRussian Federation2024221020241853256264Copyright © Загнухина Н.А., Курина А.Б., 20242024Загнухина Н.А., Курина А.Б.Zagnukhina N.A., Kurina A.B.This work is licensed under a Creative Commons Attribution 4.0 License.https://elpub.vir.nw.ru/jour/article/view/2045

Lactuca sativa L. (салат) – овощная зеленная культура семейства Asteraceae, широко возделываемая во всем мире. Основными направлениями в селекции салата являются повышение урожайности, улучшение вкусовых качеств растения, скороспелость, устойчивость к абиотическим и биотическим стрессорам. Некоторые дикорастущие виды Lactuca L. широко используют в селекции салата в качестве доноров устойчивости к различным болезням. При создании новых сортов в настоящее время используют как традиционные, так и биотехнологические методы селекции. В данной статье представлен обзор основных достижений по получению межвидовых гибридов салата, включая методы культуры клеток и тканей и генной инженерии. Исследования искусственной гибридизации и изучение естественных популяций позволяют выяснить эволюционные связи между различными видами салата. Соматическая гибридизация – незаслуженно забытая, но перспективная технология в селекции салата – позволяет получать более широкий спектр изменений и не подвергается строгому контролю со стороны законов о ГМО. Этот метод имеет проблемы, связанные со сложностью регенерации протопластов и потерей способности к размножению у гибридов. Методы редактирования генома более эффективны и легче поддаются контролю, однако общество все еще настороженно относится к любым вмешательствам в геном растений и законодательно регулирует продажу ГМ-продуктов в качестве продуктов питания. Перед исследователями стоит задача усовершенствования данных методик.

Lactuca sativa L. is a leafy vegetable crop of the Asteraceae family, widely cultivated throughout the world. The main breeding trends for lettuce include higher yields, better taste quality, earliness, and resistance to abiotic and biotic stressors. Some wild Lactuca spp. have actively been employed by lettuce breeders as donors of resistance to various diseases. Conventional and biotechnological breeding methods are both currently used to develop new lettuce cultivars. This is an overview of the main advances in the production of interspecific Lactuca hybrids, including the use of cell and tissue culture techniques, and genetic engineering. Studying artificial hybridization and natural populations makes it possible to identify evolutionary relationships among various Lactuca spp. Somatic hybridization is an overlooked but promising technology in Lactuca breeding: it allows a breeder to obtain a wider range of variations, and is beyond the strict control by GMO laws. This technique faces problems associated with complicated protoplast regeneration and the loss of reproductive ability in hybrids. Genome-editing methods are more effective and better controllable, but society is still wary of any interference with the plant genome and legally regulates the sale of GM products as food. Thus, researchers are challenged with the task to improve these techniques.

Lactuca L.селекцияметодымежвидовые гибридыклеточная и генная инженерияLactuca L.breedingmethodsinterspecific hybridscell and genetic engineeringстатья подготовлена в рамках государственного задания ВИР согласно тематическому плану ВИР по проекту FGEM-2022-0012 «Клеточные технологии для расширения селекционного потенциала культур овощного направления использования».the article was prepared within the framework of the state task according to the theme plan of VIR, Project No. FGEM-2022-0012 “Cell technologies to expand the breeding potential of crops for vegetable use”.ReferencesBerry S.F., Lu D.Y., Pental D., Cocking E.C. Regeneration of plants from protoplasts of Lactuca sativa L. Zeitschrift für Pflanzenphysiologie. 1982;108(1):31-38. DOI: 10.1016/s0044-328x(82)80088-3Berry S.F., Lu D.Y., Pental D., Cocking E.C. Regeneration of plants from protoplasts of Lactuca sativa L. Zeitschrift für Pflanzenphysiologie. 1982;108(1):31-38. DOI: 10.1016/s0044-328x(82)80088-3Bertier L.D., Ron M., Huo H., Bradford K.J., Britt A.B., Michelmore R.W. High-resolution analysis of the efficiency, heritability, and editing outcomes of CRISPR/Cas9-induced modifications of NCED4 in lettuce (Lactuca sativa). G3 (Bethesda). 2018;8(5):1513-1521. DOI: 10.1534/g3.117.300396Bertier L.D., Ron M., Huo H., Bradford K.J., Britt A.B., Michelmore R.W. High-resolution analysis of the efficiency, heritability, and editing outcomes of CRISPR/Cas9-induced modifications of NCED4 in lettuce (Lactuca sativa). G3 (Bethesda). 2018;8(5):1513-1521. DOI: 10.1534/g3.117.300396Brown C., Lucas J.A., Power J.B. Plant regeneration from protoplasts of a wild lettuce species (Lactuca saligna L.). Plant Cell Reports. 1987;6(3):180-182. DOI: 10.1007/BF00268472Brown C., Lucas J.A., Power J.B. Plant regeneration from protoplasts of a wild lettuce species (Lactuca saligna L.). Plant Cell Reports. 1987;6(3):180-182. DOI: 10.1007/BF00268472Chaipakdee W. Isolation and culture of protoplast from leaves of Lactuca sativa. Songklanakarin Journal of Science and Technology. 2007;29(4):929-935.Chaipakdee W. Isolation and culture of protoplast from leaves of Lactuca sativa. Songklanakarin Journal of Science and Technology. 2007;29(4):929-935.Chen Z., Han Y., Ning K., Ding Y., Zhao W., Yan S. et al. Inflorescence development and the role of LsFT in regulating bolting in lettuce (Lactuca sativa L.). Frontiers in Plant Science. 2018;8:2248. DOI: 10.3389/fpls.2017.02248Chen Z., Han Y., Ning K., Ding Y., Zhao W., Yan S. et al. Inflorescence development and the role of LsFT in regulating bolting in lettuce (Lactuca sativa L.). Frontiers in Plant Science. 2018;8:2248. DOI: 10.3389/fpls.2017.02248Choi S.H., Ahn W.S., Jie E.Y., Cho H.S., Kim S.W. Development of late-bolting plants by CRISPR/Cas9-mediated genome editing from mesophyll protoplasts of lettuce. Plant Cell Reports. 2022;41(7):1627-1630. DOI: 10.1007/s00299-022-02875-wChoi S.H., Ahn W.S., Jie E.Y., Cho H.S., Kim S.W. Development of late-bolting plants by CRISPR/Cas9-mediated genome editing from mesophyll protoplasts of lettuce. Plant Cell Reports. 2022;41(7):1627-1630. DOI: 10.1007/s00299-022-02875-wChu R., Xu X., Lu Z., Ma Y., Cheng H., Zhu S. et al. Plastome-based phylogeny and biogeography of Lactuca L. (Asteraceae) support revised lettuce gene pool categories. Frontiers in Plant Science. 2022;13:978417. DOI: 10.3389/fpls.2022.978417Chu R., Xu X., Lu Z., Ma Y., Cheng H., Zhu S. et al. Plastome-based phylogeny and biogeography of Lactuca L. (Asteraceae) support revised lettuce gene pool categories. Frontiers in Plant Science. 2022;13:978417. DOI: 10.3389/fpls.2022.978417Crute I.R. The role of resistance breeding in the integrated control of downy mildew (Bremia lactucae) in protected lettuce. Euphytica. 1992;63:95-102. DOI: 10.1007/BF00023915Crute I.R. The role of resistance breeding in the integrated control of downy mildew (Bremia lactucae) in protected lettuce. Euphytica. 1992;63:95-102. DOI: 10.1007/BF00023915Curtis I.S., Power J.B., Blackhall N.W., de Laat A.M.M., Davey M.R. Genotype-independent transformation of lettuce using Agrobacterium tumefaciens. Journal of Experimental Botany. 1994;45(10):1441-1449. DOI: 10.1093/jxb/45.10.1441Curtis I.S., Power J.B., Blackhall N.W., de Laat A.M.M., Davey M.R. Genotype-independent transformation of lettuce using Agrobacterium tumefaciens. Journal of Experimental Botany. 1994;45(10):1441-1449. DOI: 10.1093/jxb/45.10.1441D’Andrea L., Felber F., Guadagnuolo R. Hybridization rates between lettuce (Lactuca sativa) and its wild relative (L. serriola) under field conditions. Environmental Biosafety Research. 2008;7(2):61-71. DOI: 10.1051/ebr:2008006D’Andrea L., Felber F., Guadagnuolo R. Hybridization rates between lettuce (Lactuca sativa) and its wild relative (L. serriola) under field conditions. Environmental Biosafety Research. 2008;7(2):61-71. DOI: 10.1051/ebr:2008006Davey M.R., Anthony P., Power J.B. Lowe K.C. Leafy vegetables. In: C. Kole, T.C. Hall (eds). Compendium of Transgenic Crop Plants. Vol. 6. Transgenic Vegetable Crops. Chichester: Wiley-Blackwell; 2009. p.217-248. DOI: 10.1002/9781405181099.k0610Davey M.R., Anthony P., Power J.B. Lowe K.C. Leafy vegetables. In: C. Kole, T.C. Hall (eds). Compendium of Transgenic Crop Plants. Vol. 6. Transgenic Vegetable Crops. Chichester: Wiley-Blackwell; 2009. p.217-248. DOI: 10.1002/9781405181099.k0610De Vries I.M. Crossing experiments of lettuce cultivars and species (Lactuca sect. Lactuca, Compositae). Plant Systematics and Evolution. 1990;171(3):233-248. DOI: 10.1007/BF00940608De Vries I.M. Crossing experiments of lettuce cultivars and species (Lactuca sect. Lactuca, Compositae). Plant Systematics and Evolution. 1990;171(3):233-248. DOI: 10.1007/BF00940608De Vries I.M. Origin and domestication of Lactuca sativa L. Genetic Resources and Crop Evolution. 1997;44(2):165-174. DOI: 10.1023/A:1008611200727De Vries I.M. Origin and domestication of Lactuca sativa L. Genetic Resources and Crop Evolution. 1997;44(2):165-174. DOI: 10.1023/A:1008611200727Dinant S., Maisonneuve B., Albouy J., Chupeau Y., Chupeau M.C., Bellec Y. et al. Coat protein gene-mediated protection in Lactuca sativa against lettuce mosaic potyvirus strains. Molecular Breeding. 1997;3:75-86. DOI: 10.1023/a:1009671925550Dinant S., Maisonneuve B., Albouy J., Chupeau Y., Chupeau M.C., Bellec Y. et al. Coat protein gene-mediated protection in Lactuca sativa against lettuce mosaic potyvirus strains. Molecular Breeding. 1997;3:75-86. DOI: 10.1023/a:1009671925550Енгалычева И.А., Пышная О.Н., Джос Е.А., Тимина Л.Т., Золотарева О.И. Использование межвидовой гибридизации в селекции перца и салата на устойчивость к вирусной инфекции. Russian Agricultural Science Review. 2015;6(6-2):2-4.Engalicheva I.A., Pishnaya O.N., Dzhos E.A., Timina L.T., Zolotareva O.I. Use of interspecific hybridization in Capsicum and Lactuca breeding for virus resistance. Russian Agricultural Science Review. 2015;6(6-2):2-4. [in Russian]Engler D.E., Grogan R.G. Isolation, culture and regeneration of lettuce leaf mesophyll protoplasts. Plant Science Letters. 1982;28(2):223-229. DOI: 10.1016/s0304-4211(83)80013-3Engler D.E., Grogan R.G. Isolation, culture and regeneration of lettuce leaf mesophyll protoplasts. Plant Science Letters. 1982;28(2):223-229. DOI: 10.1016/s0304-4211(83)80013-3FAOSTAT. Food and Agriculture Organization of the United Nations. Food and agriculture data. Rome: FAO; 2022. Available from: http://www.fao.org/ [accessed Feb. 06, 2024].FAOSTAT. Food and Agriculture Organization of the United Nations. Food and agriculture data. Rome: FAO; 2022. Available from: http://www.fao.org/ [accessed Feb. 06, 2024].Harlan J.R., de Wet J.M.J. Toward a rational classification of cultivated plants. Taxon. 1971;20(4):509-517. DOI: 10.2307/1218252Harlan J.R., de Wet J.M.J. Toward a rational classification of cultivated plants. Taxon. 1971;20(4):509-517. DOI: 10.2307/1218252Hartman Y., Uwimana B., Hooftman D.A.P., Schranz M.E., van de Wiel C., Smulders M.J.M. et al. Genomic and environmental selection patterns in two distinct lettuce crop–wild hybrid crosses. Evolutionary Applications. 2013;6(4):569-584. DOI: 10.1111/eva.12043Hartman Y., Uwimana B., Hooftman D.A.P., Schranz M.E., van de Wiel C., Smulders M.J.M. et al. Genomic and environmental selection patterns in two distinct lettuce crop–wild hybrid crosses. Evolutionary Applications. 2013;6(4):569-584. DOI: 10.1111/eva.12043Hassan M.N., Mekkawy S.A., Mahdy M., Salem K.F.M., Tawfik E. Recent molecular and breeding strategies in lettuce (Lactuca spp.). Genetic Resources and Crop Evolution. 2021;68(8):3055-3079. DOI: 10.1007/s10722-021-01246-wHassan M.N., Mekkawy S.A., Mahdy M., Salem K.F.M., Tawfik E. Recent molecular and breeding strategies in lettuce (Lactuca spp.). Genetic Resources and Crop Evolution. 2021;68(8):3055-3079. DOI: 10.1007/s10722-021-01246-wHooftman D.A.P., de Jong M.J., Oostermeijer J.G.B., Den Nijs H.C.M. Modelling the long-term consequences of crop–wild relative hybridization: a case study using four generations of hybrids. Journal of Applied Ecology. 2007;44(5):1035-1045. DOI: 10.1111/j.1365-2664.2007.01341.xHooftman D.A.P., de Jong M.J., Oostermeijer J.G.B., Den Nijs H.C.M. Modelling the long-term consequences of crop–wild relative hybridization: a case study using four generations of hybrids. Journal of Applied Ecology. 2007;44(5):1035-1045. DOI: 10.1111/j.1365-2664.2007.01341.xHooftman D.A.P., Hartman Y., Oostermeijer J.G.B., Den Nijs H.C.M. Existence of vigorous lineages of crop–wild hybrids in Lettuce under field conditions. Environmental Biosafety Research. 2009;8(4):203-217. DOI: 10.1051/ebr/2010001Hooftman D.A.P., Hartman Y., Oostermeijer J.G.B., Den Nijs H.C.M. Existence of vigorous lineages of crop–wild hybrids in Lettuce under field conditions. Environmental Biosafety Research. 2009;8(4):203-217. DOI: 10.1051/ebr/2010001Hooftman D.A.P., Oostermeijer J.G.B., Jacobs M.M.J., Den Nijs H.C.M. Demographic vital rates determine the performance advantage of crop–wild hybrids in lettuce. Journal of Applied Ecology. 2005;42(6):1086-1095. DOI: 10.1111/j.1365-2664.2005.01086.xHooftman D.A.P., Oostermeijer J.G.B., Jacobs M.M.J., Den Nijs H.C.M. Demographic vital rates determine the performance advantage of crop–wild hybrids in lettuce. Journal of Applied Ecology. 2005;42(6):1086-1095. DOI: 10.1111/j.1365-2664.2005.01086.xHooftman D.A.P., Oostermeijer J.G.B., Marquard E., Den Nijs H.C.M. Modelling the consequences of crop-wild relative gene flow: a sensitivity analysis of the effects of outcrossing rates and hybrid vigour breakdown in Lactuca. Journal of Applied Ecology. 2008;45(4):1094-1103. DOI: 10.1111/j.1365-2664.2008.01508.xHooftman D.A.P., Oostermeijer J.G.B., Marquard E., Den Nijs H.C.M. Modelling the consequences of crop-wild relative gene flow: a sensitivity analysis of the effects of outcrossing rates and hybrid vigour breakdown in Lactuca. Journal of Applied Ecology. 2008;45(4):1094-1103. DOI: 10.1111/j.1365-2664.2008.01508.xJemelková M., Kitner M., Křístková E., Beharav A., Lebeda A., Biodiversity of Lactuca aculeata germplasm assessed by SSR and AFLP markers, and resistance variation to Bremia lactucae. Biochemical Systematics and Ecology. 2015;61:344-356. DOI: 10.1016/j.bse.2015.07.003Jemelková M., Kitner M., Křístková E., Beharav A., Lebeda A., Biodiversity of Lactuca aculeata germplasm assessed by SSR and AFLP markers, and resistance variation to Bremia lactucae. Biochemical Systematics and Ecology. 2015;61:344-356. DOI: 10.1016/j.bse.2015.07.003Jing J., Ji J., Wang G., Wang P., Zhang P.Y. Establishment of genetic transformation system of lettuce by Agrobacterium tumefaciens and introduction of HIV gap-gp120 gene. Tianjin Agricultural Sciences. 2007;13(1):14-17.Jing J., Ji J., Wang G., Wang P., Zhang P.Y. Establishment of genetic transformation system of lettuce by Agrobacterium tumefaciens and introduction of HIV gap-gp120 gene. Tianjin Agricultural Sciences. 2007;13(1):14-17.Kanamoto H., Yamashita A., Asao H., Okumura S., Takase H., Hattori M. et al. Efficient and stable transformation of Lactuca sativa L. cv. ‘Cisco’ (lettuce) plastids. Transgenic Research. 2006;15(2):205-217. DOI: 10.1007/s11248-005-3997-2Kanamoto H., Yamashita A., Asao H., Okumura S., Takase H., Hattori M. et al. Efficient and stable transformation of Lactuca sativa L. cv. ‘Cisco’ (lettuce) plastids. Transgenic Research. 2006;15(2):205-217. DOI: 10.1007/s11248-005-3997-2Kim T.G., Kim M.Y., Kim B.G., Kang T.J., Kim Y.S., Jang Y.S. et al. Synthesis and assembly of Escherichia coli heat-labile enterotoxin B subunit in transgenic lettuce (Lactuca sativa). Protein Expression and Purification. 2007;51(1):22-27. DOI: 10.1016/j.pep.2006.05.024Kim T.G., Kim M.Y., Kim B.G., Kang T.J., Kim Y.S., Jang Y.S. et al. Synthesis and assembly of Escherichia coli heat-labile enterotoxin B subunit in transgenic lettuce (Lactuca sativa). Protein Expression and Purification. 2007;51(1):22-27. DOI: 10.1016/j.pep.2006.05.024Křístková E., Lebeda A., Kitner M., Vafková B., Matoušková Z., Doležalová I. et al. Phenotypes of the natural interspecific hybrids in the genus Lactuca. Úroda. 2012;60(9):28-31.Křístková E., Lebeda A., Kitner M., Vafková B., Matoušková Z., Doležalová I. et al. Phenotypes of the natural interspecific hybrids in the genus Lactuca. Úroda. 2012;60(9):28-31.Кузьмина Ю.В. Методы редактирования генома для увеличения лёжкости плодов томата. Биотехнология и селекция растений. 2020;3(1):31-39. DOI: 10.30901/2658-6266-2020-1-o6Kuzmina Y.V. Methods of genome editing for increasing the shelf life of tomato fruits. Plant Biotechnology and Breeding. 2020;3(1):31-39. [in Russian] DOI: 10.30901/2658-6266-2020-1-o6Lebeda A., Křístková E., Kitner M., Mieslerova B., Jemelková M., Pink D. Wild Lactuca species, their genetic diversity, resistance to diseases and pests, and exploitation in lettuce breeding. European Journal of Plant Pathology. 2014;138(3):597-640. DOI: 10.1007/s10658-013-0254-zLebeda A., Křístková E., Kitner M., Mieslerova B., Jemelková M., Pink D. Wild Lactuca species, their genetic diversity, resistance to diseases and pests, and exploitation in lettuce breeding. European Journal of Plant Pathology. 2014;138(3):597-640. DOI: 10.1007/s10658-013-0254-zLebeda A., Ryder E.J., Grube R., Doležalová I., Křístková E. Lettuce (Asteraceae; Lactuca spp.). In: R.J. Singh (ed.). Genetic Resources, Chromosome Engineering, and Crop Improvement. Vol. 3. Vegetable Crops. Boca Raton, FL: CRC Press; 2007. p.377-472. DOI: 10.1201/9781420009569.ch9Lebeda A., Ryder E.J., Grube R., Doležalová I., Křístková E. Lettuce (Asteraceae; Lactuca spp.). In: R.J. Singh (ed.). Genetic Resources, Chromosome Engineering, and Crop Improvement. Vol. 3. Vegetable Crops. Boca Raton, FL: CRC Press; 2007. p.377-472. DOI: 10.1201/9781420009569.ch9Liu C.W., Chen J.J.W., Kang C.C., Wu C.H., Yiu J.C. Transgenic lettuce (Lactuca sativa L.) expressing H1N1 influenza surface antigen (neuraminidase). Scientia Horticulturae. 2012;139:8-13. DOI: 10.1016/j.scienta.2012.02.037Liu C.W., Chen J.J.W., Kang C.C., Wu C.H., Yiu J.C. Transgenic lettuce (Lactuca sativa L.) expressing H1N1 influenza surface antigen (neuraminidase). Scientia Horticulturae. 2012;139:8-13. DOI: 10.1016/j.scienta.2012.02.037Maisonneuve B. Lactuca virosa, a source of disease resistance genes in lettuce breeding: results and difficulties for gene introgression. In: Th.J.L. van Hintum, A. Lebeda, D. Pink, J.W. Schur (eds.). EUCARPIA Leafy Vegetables 2003: Proceedings of the EUCARPIA Meeting on Leafy Vegetables Genetics and Breeding; Noordwijkerhout, the Netherlands, 19–21 March 2003. Wageningen: CGN; 2003. p.61-67.Maisonneuve B. Lactuca virosa, a source of disease resistance genes in lettuce breeding: results and difficulties for gene introgression. In: Th.J.L. van Hintum, A. Lebeda, D. Pink, J.W. Schur (eds.). EUCARPIA Leafy Vegetables 2003: Proceedings of the EUCARPIA Meeting on Leafy Vegetables Genetics and Breeding; Noordwijkerhout, the Netherlands, 19–21 March 2003. Wageningen: CGN; 2003. p.61-67.Maisonneuve B., Bellec Y. Utilisation de la culture in vitro d’embryons immatures pour les croisements interspécifiques entre Lactuca sativa L. et L. saligha L. ou L. virosa L.; étude des hybrides obtenu. Agronomie. 1987;7(5):313-319. [in French] DOI: 10.1051/agro:19870503Maisonneuve B., Bellec Y. Utilisation de la culture in vitro d’embryons immatures pour les croisements interspécifiques entre Lactuca sativa L. et L. saligha L. ou L. virosa L.; étude des hybrides obtenu. Agronomie. 1987;7(5):313-319. [in French] DOI: 10.1051/agro:19870503Marcondes J., Hansen E. Transgenic lettuce seedlings carrying hepatitis B virus antigen HBsAg. The Brazilian Journal of Infectious Diseases. 2008;12(6):469-471. DOI: 10.1590/s1413-86702008000600004Marcondes J., Hansen E. Transgenic lettuce seedlings carrying hepatitis B virus antigen HBsAg. The Brazilian Journal of Infectious Diseases. 2008;12(6):469-471. DOI: 10.1590/s1413-86702008000600004Matsumoto E. Interspecific somatic hybridization between lettuce (Lactuca sativa) and wild species L. virosa. Plant Cell Reports. 1991;9(10):531-534. DOI: 10.1007/BF00232325Matsumoto E. Interspecific somatic hybridization between lettuce (Lactuca sativa) and wild species L. virosa. Plant Cell Reports. 1991;9(10):531-534. DOI: 10.1007/BF00232325Matsumoto E. Production of somatic hybrids between Lactuca sativa and L. serriola by cell fusion. Japanese Journal of Breeding. 1987;37 Suppl l:134-135.Matsumoto E. Production of somatic hybrids between Lactuca sativa and L. serriola by cell fusion. Japanese Journal of Breeding. 1987;37 Suppl l:134-135.Matvieieva N.A., Kudryavets Y.I., Lichova A.A. Shachovsky A.M., Bezdenezhnykh N.A., Kvasko E.Yu. Antiviral activity of extracts of transgenic chicory and lettuce plants with the human interferon alpha2b gene. Cytology and Genetics. 2012;46(5):285-290. DOI: 10.3103/S0095452712050076Matvieieva N.A., Kudryavets Y.I., Lichova A.A. Shachovsky A.M., Bezdenezhnykh N.A., Kvasko E.Yu. Antiviral activity of extracts of transgenic chicory and lettuce plants with the human interferon alpha2b gene. Cytology and Genetics. 2012;46(5):285-290. DOI: 10.3103/S0095452712050076Matvieieva N.A., Vasylenko M.Yu., Shakhovsky A.M., Kuchuk N.V. Agrobacterium-mediated transformation of lettuce (Lactuca sativa L.) with genes coding bacterial antigens from Mycobacterium tuberculosis. Cytology and Genetics. 2009;43(2):94-98. DOI: 10.3103/S0095452709020042Matvieieva N.A., Vasylenko M.Yu., Shakhovsky A.M., Kuchuk N.V. Agrobacterium-mediated transformation of lettuce (Lactuca sativa L.) with genes coding bacterial antigens from Mycobacterium tuberculosis. Cytology and Genetics. 2009;43(2):94-98. DOI: 10.3103/S0095452709020042Michelmore R., Marsh E., Seely S., Landry B. Transformation of lettuce (Lactuca sativa) mediated by Agrobacterium tumefaciens. Plant Cell Reports. 1987;6(6):439-442. DOI: 10.1007/BF00272777Michelmore R., Marsh E., Seely S., Landry B. Transformation of lettuce (Lactuca sativa) mediated by Agrobacterium tumefaciens. Plant Cell Reports. 1987;6(6):439-442. DOI: 10.1007/BF00272777Mizutani T., Liu X.J., Tashiro Y., Miyazaki S., Shimazaki K. Plant regeneration and cell fusion of protoplasts from lettuce cultivars and related wild species in Japan. Bulletin of the Faculty of Agriculture, Saga University. 1989;67:109-118.Mizutani T., Liu X.J., Tashiro Y., Miyazaki S., Shimazaki K. Plant regeneration and cell fusion of protoplasts from lettuce cultivars and related wild species in Japan. Bulletin of the Faculty of Agriculture, Saga University. 1989;67:109-118.Nishio T., Sato T., Mori K., Takayanagi K. Simple and efficient protoplast culture procedure of lettuce, Lactuca sativa L. Japanese Journal of Breeding. 1988;38(2):165-171.Nishio T., Sato T., Mori K., Takayanagi K. Simple and efficient protoplast culture procedure of lettuce, Lactuca sativa L. Japanese Journal of Breeding. 1988;38(2):165-171.Park J., Choi S., Park S., Yoon J., Park A.Y., Choe S. DNA-free genome editing via ribonucleoprotein (RNP) delivery of CRISPR/Cas in lettuce. Methods in Molecular Biology. 2019;1917:337-354. DOI: 10.1007/978-1-4939-8991-1_25Park J., Choi S., Park S., Yoon J., Park A.Y., Choe S. DNA-free genome editing via ribonucleoprotein (RNP) delivery of CRISPR/Cas in lettuce. Methods in Molecular Biology. 2019;1917:337-354. DOI: 10.1007/978-1-4939-8991-1_25Pileggi M., Mielniczki Pereira A.A., dos Santos Silva J.,Pileggi S.A.V., Verma D.P.S., Delauney A.J. et al. An improved method for transformation of lettuce by Agrobacterium tumefaciens with a gene that confers freezing resistance. Brazilian Archives of Biology and Technology. 2001;44(2):191-196. DOI: 10.1590/S1516-89132001000200013Pileggi M., Mielniczki Pereira A.A., dos Santos Silva J.,Pileggi S.A.V., Verma D.P.S., Delauney A.J. et al. An improved method for transformation of lettuce by Agrobacterium tumefaciens with a gene that confers freezing resistance. Brazilian Archives of Biology and Technology. 2001;44(2):191-196. DOI: 10.1590/S1516-89132001000200013Porcel R., Aroca R., Azcón R., Ruiz-Lozano J.M. PIP aquaporin gene expression in arbuscular mycorrhizal Glycine max and Lactuca sativa plants in relation to drought stress tolerance. Plant Molecular Biology. 2006;60(3):389-404. DOI: 10.1007/s11103-005-4210-yPorcel R., Aroca R., Azcón R., Ruiz-Lozano J.M. PIP aquaporin gene expression in arbuscular mycorrhizal Glycine max and Lactuca sativa plants in relation to drought stress tolerance. Plant Molecular Biology. 2006;60(3):389-404. DOI: 10.1007/s11103-005-4210-yСамко О.В., Снигирева А.В. Использование технологии соматической гибридизации в селекции растений. Амурский научный вестник. 2009;(1):233-239.Samko O.V., Snigireva A.V. The use of somatic hybridization technology in plant breeding (Ispolzovaniye tekhnologii somaticheskoy gibridizatsii v selektsii rasteniy). Amurskiy nauchny vestnik = Amur Scientific Bulletin. 2009;(1):233-239. [in Russian]Sharma S., Gautam N., Thakur A.K., Srivastava D.K. Transgenic lettuce (Lactuca sativa L.) harboring chitinase gene expressed resistance against a devastating fungus, Sclerotinia sclerotiorum. International Journal of Plant Research. 2022;36(2):1265–1274. DOI: 10.1007/s42535-022-00519-8Sharma S., Gautam N., Thakur A.K., Srivastava D.K. Transgenic lettuce (Lactuca sativa L.) harboring chitinase gene expressed resistance against a devastating fungus, Sclerotinia sclerotiorum. International Journal of Plant Research. 2022;36(2):1265–1274. DOI: 10.1007/s42535-022-00519-8Шмыкова Н.А., Супрунова Т.П., Пивоваров В.Ф. Биотехнологические и молекулярно-генетические методы в селекции овощных культур (к 95-летию ВНИИССОК). Сельскохозяйственная биология. 2015;50(5):561-570. DOI: 10.15389/agrobiology.2015.5.561rusShmykova N.A., Suprunova T.P., Pivovarov V.F. Biotechnologies and molecular methods in vegetable crop breeding (to 95th anniversary of VNIISSOK). Agricultural Biology. 2015;50(5):561-570. [in Russian] DOI: 10.15389/agrobiology.2015.5.561rusSiddiqui M.R. Somatic hybridization via protoplasts fusion in Lactuca sativa (Lettuce) and it’s fused product response to culture media. Journal of Agricultural Research. 2014;52(1):1-9.Siddiqui M.R. Somatic hybridization via protoplasts fusion in Lactuca sativa (Lettuce) and it’s fused product response to culture media. Journal of Agricultural Research. 2014;52(1):1-9.Singh R.J. (ed.). Genetic resources, chromosome engineering, and crop improvement. Vol. 3. Vegetable Crops. Boca Raton, FL: CRC Press; 2006. DOI: 10.1201/9781420009569Singh R.J. (ed.). Genetic resources, chromosome engineering, and crop improvement. Vol. 3. Vegetable Crops. Boca Raton, FL: CRC Press; 2006. DOI: 10.1201/9781420009569Son B.H., Park C.G., Khakurel D., Hwang J., Kim W.Y., Jeon B.G. et al. Fertile plant regeneration from protoplasts of the Korean lettuce cultivar “Cheongchima” (Lactuca sativa L.). Journal of Agriculture and Life Science. 2022;56(5):45-50. DOI: 10.14397/jals.2022.56.5.45Son B.H., Park C.G., Khakurel D., Hwang J., Kim W.Y., Jeon B.G. et al. Fertile plant regeneration from protoplasts of the Korean lettuce cultivar “Cheongchima” (Lactuca sativa L.). Journal of Agriculture and Life Science. 2022;56(5):45-50. DOI: 10.14397/jals.2022.56.5.45Song D., Han Q., Dong Z., He Z. Genetic transformation of lettuce (Lactuca sativa): A review. African Journal of Biotechnology. 2014;13(16):1686-1693. DOI: 10.5897/AJB2014.13651Song D., Han Q., Dong Z., He Z. Genetic transformation of lettuce (Lactuca sativa): A review. African Journal of Biotechnology. 2014;13(16):1686-1693. DOI: 10.5897/AJB2014.13651Государственный реестр селекционных достижений, допущенных к использованию: [сайт]. URL: https://gossortrf.ru [дата обращения: 06.02.2024].State Register for Selection Achievements Admitted for Usage: [website]. [in Russian] URL: https://gossortrf.ru [дата обращения: 06.02.2024].Torres A.C., Cantliffe D.J., Laughner B., Bieniek M., Nagata R., Ashraf M. et al. Stable transformation of lettuce cultivar South Bay from cotyledon explants. Plant Cell, Tissue and Organ Culture. 1993;34:279-285. DOI: 10.1007/bf00029717Torres A.C., Cantliffe D.J., Laughner B., Bieniek M., Nagata R., Ashraf M. et al. Stable transformation of lettuce cultivar South Bay from cotyledon explants. Plant Cell, Tissue and Organ Culture. 1993;34:279-285. DOI: 10.1007/bf00029717Uwimana B., D’Andrea L., Felber F., Hooftman D.A.P., Den Nijs H.C.M., Smulders M.J.M. et al. A Bayesian analysis of gene flow from crops to their wild relatives: cultivated (Lactuca sativa L.) and prickly lettuce (L. serriola L.) and the recent expansion of L. serriola in Europe. Molecular Ecology. 2012a;21(11):2640-2654. DOI: 10.1111/j.1365-294X.2012.05489.xUwimana B., D’Andrea L., Felber F., Hooftman D.A.P., Den Nijs H.C.M., Smulders M.J.M. et al. A Bayesian analysis of gene flow from crops to their wild relatives: cultivated (Lactuca sativa L.) and prickly lettuce (L. serriola L.) and the recent expansion of L. serriola in Europe. Molecular Ecology. 2012a;21(11):2640-2654. DOI: 10.1111/j.1365-294X.2012.05489.xUwimana B., Smulders M.J.M., Hooftman D.A.P., Hartman Y., van Tienderen P.H., Jansen J. et al. Hybridization between crops and wild relatives: the contribution of cultivated lettuce to the vigour of crop–wild hybrids under drought, salinity and nutrient deficiency conditions. Theoretical and Applied Genetics. 2012b;125(6):1097-1111. DOI: 10.1007/s00122-012-1897-4Uwimana B., Smulders M.J.M., Hooftman D.A.P., Hartman Y., van Tienderen P.H., Jansen J. et al. Hybridization between crops and wild relatives: the contribution of cultivated lettuce to the vigour of crop–wild hybrids under drought, salinity and nutrient deficiency conditions. Theoretical and Applied Genetics. 2012b;125(6):1097-1111. DOI: 10.1007/s00122-012-1897-4Wei T., van Treuren R., Liu X., Zhang Z., Chen J., Liu Y. et al. Whole-genome resequencing of 445 Lactuca accessions reveals the domestication history of cultivated lettuce. Nature Genetics. 2021;53(5):752-760. DOI: 10.1038/s41588-021-00831-0Wei T., van Treuren R., Liu X., Zhang Z., Chen J., Liu Y. et al. Whole-genome resequencing of 445 Lactuca accessions reveals the domestication history of cultivated lettuce. Nature Genetics. 2021;53(5):752-760. DOI: 10.1038/s41588-021-00831-0Wei Z., Zhu S.X., Van Den Berg R.G., Bakker F.T., Schranz M.E. Phylogenetic relationships within Lactuca L. (Asteraceae), including African species, based on chloroplast DNA sequence comparisons. Genetic Resources and Crop Evolution. 2017;64(1):55-71. DOI: 10.1007/s10722-015-0332-5Wei Z., Zhu S.X., Van Den Berg R.G., Bakker F.T., Schranz M.E. Phylogenetic relationships within Lactuca L. (Asteraceae), including African species, based on chloroplast DNA sequence comparisons. Genetic Resources and Crop Evolution. 2017;64(1):55-71. DOI: 10.1007/s10722-015-0332-5Woo J.W., Kim J., Kwon S.I., Corvalán C., Cho S.W., Kim H. et al. DNA-free genome editing in plants with preassembled CRISPR-Cas9 ribonucleoproteins. Nature Biotechnology. 2015;33(11):1162-1164. DOI: 10.1038/nbt.3389Woo J.W., Kim J., Kwon S.I., Corvalán C., Cho S.W., Kim H. et al. DNA-free genome editing in plants with preassembled CRISPR-Cas9 ribonucleoproteins. Nature Biotechnology. 2015;33(11):1162-1164. DOI: 10.1038/nbt.3389Wroblewski T., Tomczak A., Michelmore R. Optimization of Agrobacterium-mediated transient assays of gene expression in lettuce, tomato and Arabidopsis. Plant Biotechnology Journal. 2005;3(2):259-273. DOI: 10.1111/j.1467-7652.2005.00123.xWroblewski T., Tomczak A., Michelmore R. Optimization of Agrobacterium-mediated transient assays of gene expression in lettuce, tomato and Arabidopsis. Plant Biotechnology Journal. 2005;3(2):259-273. DOI: 10.1111/j.1467-7652.2005.00123.xZohary D. The wild genetic resources of cultivated lettuce (Lactuca sativa L.). Euphytica. 1991;53(1):31-35. DOI: 10.1007/BF00032029Zohary D. The wild genetic resources of cultivated lettuce (Lactuca sativa L.). Euphytica. 1991;53(1):31-35. DOI: 10.1007/BF00032029

The authors declare that there are no conflicts of interest present.