<?xml version="1.0" encoding="UTF-8"?>
<!DOCTYPE article PUBLIC "-//NLM//DTD JATS (Z39.96) Journal Publishing DTD v1.3 20210610//EN" "JATS-journalpublishing1-3.dtd">
<article article-type="review-article" dtd-version="1.3" xmlns:mml="http://www.w3.org/1998/Math/MathML" xmlns:xlink="http://www.w3.org/1999/xlink" xmlns:xsi="http://www.w3.org/2001/XMLSchema-instance" xml:lang="ru"><front><journal-meta><journal-id journal-id-type="publisher-id">vavilov</journal-id><journal-title-group><journal-title xml:lang="ru">Вавиловский журнал генетики и селекции</journal-title><trans-title-group xml:lang="en"><trans-title>Vavilov Journal of Genetics and Breeding</trans-title></trans-title-group></journal-title-group><issn pub-type="epub">2500-3259</issn><publisher><publisher-name>Institute of Cytology and Genetics of Siberian Branch of the RAS</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="doi">10.18699/vjgb-25-54</article-id><article-id custom-type="elpub" pub-id-type="custom">vavilov-4676</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="section-heading" xml:lang="ru"><subject>ГЕНЕТИКА РАСТЕНИЙ</subject></subj-group><subj-group subj-group-type="section-heading" xml:lang="en"><subject>PLANT GENETICS</subject></subj-group></article-categories><title-group><article-title>Особенности генетического картирования локусов, влияющих на образование эмбриогенного каллуса и регенерацию растений in vitro у зерновых и бобовых культур</article-title><trans-title-group xml:lang="en"><trans-title>Genetic mapping of loci affecting embryogenic callus formation and in vitro regeneration in cereals and leguminous crops</trans-title></trans-title-group></title-group><contrib-group><contrib contrib-type="author" corresp="yes"><name-alternatives><name name-style="eastern" xml:lang="ru"><surname>Потокина</surname><given-names>Е. К.</given-names></name><name name-style="western" xml:lang="en"><surname>Potokina</surname><given-names>E. K.</given-names></name></name-alternatives><bio xml:lang="ru"><p>Mосква</p></bio><bio xml:lang="en"><p>Moscow</p></bio><email xlink:type="simple">e.potokina@skoltech.ru</email><xref ref-type="aff" rid="aff-1"/></contrib><contrib contrib-type="author" corresp="yes"><name-alternatives><name name-style="eastern" xml:lang="ru"><surname>Сущенко</surname><given-names>А. С.</given-names></name><name name-style="western" xml:lang="en"><surname>Sushchenko</surname><given-names>A. S.</given-names></name></name-alternatives><bio xml:lang="ru"><p>Mосква</p></bio><bio xml:lang="en"><p>Moscow</p></bio><xref ref-type="aff" rid="aff-1"/></contrib></contrib-group><aff-alternatives id="aff-1"><aff xml:lang="ru">Сколковский институт науки и технологий (Сколтех)<country>Россия</country></aff><aff xml:lang="en">Skolkovo Institute of Science and Technology (Skoltech)<country>Russian Federation</country></aff></aff-alternatives><pub-date pub-type="collection"><year>2025</year></pub-date><pub-date pub-type="epub"><day>20</day><month>07</month><year>2025</year></pub-date><volume>29</volume><issue>4</issue><fpage>508</fpage><lpage>516</lpage><permissions><copyright-statement>Copyright &amp;#x00A9; Потокина Е.К., Сущенко А.С., 2025</copyright-statement><copyright-year>2025</copyright-year><copyright-holder xml:lang="ru">Потокина Е.К., Сущенко А.С.</copyright-holder><copyright-holder xml:lang="en">Potokina E.K., Sushchenko A.S.</copyright-holder><license license-type="creative-commons-attribution" xlink:href="https://creativecommons.org/licenses/by/4.0/" xlink:type="simple"><license-p>This work is licensed under a Creative Commons Attribution 4.0 License.</license-p></license></permissions><self-uri xlink:href="https://vavilov.elpub.ru/jour/article/view/4676">https://vavilov.elpub.ru/jour/article/view/4676</self-uri><abstract><p>Рекальцитрантность определяется как неспосо6ность видов или отдельных генотипов растений к эффективной регенерации и/или трансформации в культуре in vitro и представляет со6ой самое существенное ограничение для геномного редактирования сельскохозяйственных культур. Для разра6отки протоколов генотип-независимой трансформации и регенерации культурных растений нео6ходимы знания о генетических факторах, детерминирующих рекальцитрантность у различных видов растений в условиях in vitro. Поиск их путем классического картирования QTL для признаков эффективности каллусоо6разования, регенерации, трансформации в расщепляющихся популяциях считается сложным и трудоемким процессом из-за специфичной природы анализируемых фенотипов и сильной взаимосвязи «генотип – среда». B статье приводится о6зор методологии, перспектив и наи6олее ярких достижений «прямой» генетики в идентификации генетических детерминант рекальцитрантности у самых востре6ованных и одновременно наи6олее трудных для ра6оты in vitro зерновых и 6о6овых культур. Приведены примеры генетического картирования и успешного клонирования генов, отвечающих за разные аспекты рекальцитрантности у злаков. Tак, установлено, что формирование 6ыстро пролиферирующего эм6риогенного каллуса II типа у кукурузы определяется повышенной экспрессией гена Wox2a. Популярный в „понии сорт риса Koshihikari плохо регенерирует в культуре in vitro из-за нарушенного мета6олизма нитратов, так как отличается низким уровнем экспрессии нитритредуктазы (NiR), прео6разующей нитрит в аммиак. По6урение каллуса, встречающееся среди многих видов растений и приводящее к снижению регенерационной спосо6ности, у сортов риса (Oryza sativa ssp. indica) зависит от уровня экспрессии гена Browning of Callus1 (BOC1), который кодирует 6елок SRO (Similar to RCD One), регулирующий реакцию растения на окислительный стресс. Аналогичные ра6оты по картированию локусов для признаков соматического эм6риогенеза у сои позволили о6наружить мажорные (major) QTL, о6ъясняющие 45 и 26 % изменчивости признака. Исследования по генетическому картированию локусов, влияющих на эффективность регенерации и эм6риогенеза у рекальцитрантных видов растений, имеют очевидные перспективы в связи с появлением аннотированных референсных геномов, высокопроизводительного генотипирования и генетических карт с высоким разрешением.</p></abstract><trans-abstract xml:lang="en"><p>Recalcitrance is defined as the inability of plant species or individual genotypes to effectively regenerate and/or to be transformed in in vitro culture, and is the most significant limitation for genome editing of agricultural crops. To develop protocols for genotype-independent transformation and regeneration of cultivated plants, knowledge of the genetic factors that determine recalcitrance in various plant species under in vitro conditions is required. Their search by classical QTL mapping in populations segregating for callus formation efficiency, regeneration, and transformation is considered a complex and labor-intensive process due to a specific nature of the analyzed phenotypes and a strong genotype-environment relationship. The article provides an overview of the methodology, prospects, and most outstanding achievements of “forward” genetics in identifying genetic determinants of recalcitrance in the most popular and at the same time most difficult to work with in vitro cereal and legume crops. Examples of genetic mapping and successful cloning of genes responsible for various aspects of recalcitrance in cereals are discussed. Thus, it was found that the formation of rapidly proliferating type II embryogenic callus in maize is determined by increased expression of the Wox2a gene. The Koshihikari rice variety, popular in Japan, poorly regenerates in vitro due to impaired nitrate metabolism, since it has a low expression level of nitrite reductase (NiR), which converts nitrite into ammonia. Callus browning, which occurs among many plant species and leads to a decrease in regenerative capacity and even to plant death, in rice varieties (Oryza sativa ssp. indica) depends on the expression level of the Browning of Callus1 (BOC1) gene, which encodes the SRO protein (Similar to RCD One), regulating the plant response to oxidative stress. Similar studies on mapping loci for somatic embryogenesis traits in soybean have revealed major QTLs explaining 45 and 26 % of phenotypic variation. Studies on genetic mapping of loci affecting the efficiency of regeneration and embryogenesis in recalcitrant plant species have obvious prospects due to the emergence of annotated reference genomes, high-throughput genotyping and high-resolution genetic maps.</p></trans-abstract><kwd-group xml:lang="ru"><kwd>растения</kwd><kwd>in vitro</kwd><kwd>генотип-зависимая регенерация</kwd><kwd>рекальцитрантность</kwd><kwd>генетический контроль</kwd><kwd>QTL морфогенетических признаков</kwd></kwd-group><kwd-group xml:lang="en"><kwd>plants</kwd><kwd>in vitro</kwd><kwd>genotype-dependent regeneration</kwd><kwd>recalcitrance</kwd><kwd>genetic control</kwd><kwd>QTLs of morphogenetic traits</kwd></kwd-group><funding-group xml:lang="en"><funding-statement>The work was supported by the Russian Science Foundation, grant No. 24-26-00073</funding-statement></funding-group></article-meta></front><back><ref-list><title>References</title><ref id="cit1"><label>1</label><citation-alternatives><mixed-citation xml:lang="ru">Altpeter F., Springer N.M., Bartley L.E., Blechl A.E., Brutnell T.P., Citovsky V., Conrad L.J., Gelvin S.B., Jackson D.P., Kausch A.P., Lemaux P.G., Medford J.I., Orozco-Cárdenas M.L., Tricoli D.M., Van Eck J., Voytas D.F., Walbot V., Wang K., Zhang Z.J., Stewart C.N. Advancing crop transformation in the era of genome editing. Plant Cell. 2016;28(7):1510-1520. doi 10.1105/tpc.16.00196</mixed-citation><mixed-citation xml:lang="en">Altpeter F., Springer N.M., Bartley L.E., Blechl A.E., Brutnell T.P., Citovsky V., Conrad L.J., Gelvin S.B., Jackson D.P., Kausch A.P., Lemaux P.G., Medford J.I., Orozco-Cárdenas M.L., Tricoli D.M., Van Eck J., Voytas D.F., Walbot V., Wang K., Zhang Z.J., Stewart C.N. Advancing crop transformation in the era of genome editing. Plant Cell. 2016;28(7):1510-1520. doi 10.1105/tpc.16.00196</mixed-citation></citation-alternatives></ref><ref id="cit2"><label>2</label><citation-alternatives><mixed-citation xml:lang="ru">Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J Mol Biol. 1990;215(3):403-410. doi 10.1016/S0022-2836(05)80360-2</mixed-citation><mixed-citation xml:lang="en">Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J Mol Biol. 1990;215(3):403-410. doi 10.1016/S0022-2836(05)80360-2</mixed-citation></citation-alternatives></ref><ref id="cit3"><label>3</label><citation-alternatives><mixed-citation xml:lang="ru">Armstrong C.L., Romero-Severson J., Hodges T.K. Improved tissue culture response of an elite maize inbred through backcross breeding, and identification of chromosomal regions important for regeneration by RFLP analysis. Theor Appl Genet. 1992;84(5-6):755-762. doi 10.1007/BF00224181</mixed-citation><mixed-citation xml:lang="en">Armstrong C.L., Romero-Severson J., Hodges T.K. Improved tissue culture response of an elite maize inbred through backcross breeding, and identification of chromosomal regions important for regeneration by RFLP analysis. Theor Appl Genet. 1992;84(5-6):755-762. doi 10.1007/BF00224181</mixed-citation></citation-alternatives></ref><ref id="cit4"><label>4</label><citation-alternatives><mixed-citation xml:lang="ru">Baker A., Carrier D.J., Schaedler T., Waterham H.R., van Roermund C.W., Theodoulou F.L. Peroxisomal ABC transporters: functions and mechanism. Biochem Soc Trans. 2015;43(5):959-965. doi 10.1042/BST20150127</mixed-citation><mixed-citation xml:lang="en">Baker A., Carrier D.J., Schaedler T., Waterham H.R., van Roermund C.W., Theodoulou F.L. Peroxisomal ABC transporters: functions and mechanism. Biochem Soc Trans. 2015;43(5):959-965. doi 10.1042/BST20150127</mixed-citation></citation-alternatives></ref><ref id="cit5"><label>5</label><citation-alternatives><mixed-citation xml:lang="ru">Bekalu Z.E., Panting M., Bæksted Holme I., Brinch-Pedersen H. Opportunities and challenges of in vitro tissue culture systems in the era of crop genome editing. Int J Mol Sci. 2023;24(15):11920. doi 10.3390/ijms241511920</mixed-citation><mixed-citation xml:lang="en">Bekalu Z.E., Panting M., Bæksted Holme I., Brinch-Pedersen H. Opportunities and challenges of in vitro tissue culture systems in the era of crop genome editing. Int J Mol Sci. 2023;24(15):11920. doi 10.3390/ijms241511920</mixed-citation></citation-alternatives></ref><ref id="cit6"><label>6</label><citation-alternatives><mixed-citation xml:lang="ru">Benson E.E. Special symposium: In vitro plant recalcitrance: an introduction. In Vitro Cell Dev Biol Plant. 2000;36:141-148. doi 10.1007/s11627-000-0029-z</mixed-citation><mixed-citation xml:lang="en">Benson E.E. Special symposium: In vitro plant recalcitrance: an introduction. In Vitro Cell Dev Biol Plant. 2000;36:141-148. doi 10.1007/s11627-000-0029-z</mixed-citation></citation-alternatives></ref><ref id="cit7"><label>7</label><citation-alternatives><mixed-citation xml:lang="ru">Boutilier K., Offringa R., Sharma V.K., Kieft H., Ouellet T., Zhang L., Hattori J., Liu C.M., van Lammeren A.A., Miki B.L., Custers J.B., van Lookeren Campagne M.M. Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell. 2002;14:1737-1749. doi 10.1105/tpc.001941</mixed-citation><mixed-citation xml:lang="en">Boutilier K., Offringa R., Sharma V.K., Kieft H., Ouellet T., Zhang L., Hattori J., Liu C.M., van Lammeren A.A., Miki B.L., Custers J.B., van Lookeren Campagne M.M. Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell. 2002;14:1737-1749. doi 10.1105/tpc.001941</mixed-citation></citation-alternatives></ref><ref id="cit8"><label>8</label><citation-alternatives><mixed-citation xml:lang="ru">Chanvivattana Y., Bishopp A., Schubert D., Stock C., Moon Y.H., Sung Z.R., Goodrich J. Interaction of Polycomb-group proteins controlling flowering in Arabidopsis. Development. 2004;131(21): 5263-5276. doi 10.1242/dev.01400</mixed-citation><mixed-citation xml:lang="en">Chanvivattana Y., Bishopp A., Schubert D., Stock C., Moon Y.H., Sung Z.R., Goodrich J. Interaction of Polycomb-group proteins controlling flowering in Arabidopsis. Development. 2004;131(21): 5263-5276. doi 10.1242/dev.01400</mixed-citation></citation-alternatives></ref><ref id="cit9"><label>9</label><citation-alternatives><mixed-citation xml:lang="ru">Chen F., Yang Y., Luo X., Zhou W., Dai Y., Zheng C., Liu W., Yang W., Shu K. Genome-wide identification of GRF transcription factors in soybean and expression analysis of GmGRF family under shade stress. BMC Plant Biol. 2019;19(1):269. doi 10.1186/s12870-019-1861-4</mixed-citation><mixed-citation xml:lang="en">Chen F., Yang Y., Luo X., Zhou W., Dai Y., Zheng C., Liu W., Yang W., Shu K. Genome-wide identification of GRF transcription factors in soybean and expression analysis of GmGRF family under shade stress. BMC Plant Biol. 2019;19(1):269. doi 10.1186/s12870-019-1861-4</mixed-citation></citation-alternatives></ref><ref id="cit10"><label>10</label><citation-alternatives><mixed-citation xml:lang="ru">Chen Z., Debernardi J.M., Dubcovsky J., Gallavotti A. Recent advances in crop transformation technologies. Nat Plants. 2022;8(12): 1343-1351. doi 10.1038/s41477-022-01295-8</mixed-citation><mixed-citation xml:lang="en">Chen Z., Debernardi J.M., Dubcovsky J., Gallavotti A. Recent advances in crop transformation technologies. Nat Plants. 2022;8(12): 1343-1351. doi 10.1038/s41477-022-01295-8</mixed-citation></citation-alternatives></ref><ref id="cit11"><label>11</label><citation-alternatives><mixed-citation xml:lang="ru">Debernardi J.M., Tricoli D.M., Ercoli M.F., Hayta S., Ronald P., Palatnik J.F., Dubcovsky J. A GRF–GIF chimeric protein improves the regeneration efficiency of transgenic plants. Nature Biotechnol. 2020;38(11):1274-1279. doi 10.1038/s41587-020-0703-0</mixed-citation><mixed-citation xml:lang="en">Debernardi J.M., Tricoli D.M., Ercoli M.F., Hayta S., Ronald P., Palatnik J.F., Dubcovsky J. A GRF–GIF chimeric protein improves the regeneration efficiency of transgenic plants. Nature Biotechnol. 2020;38(11):1274-1279. doi 10.1038/s41587-020-0703-0</mixed-citation></citation-alternatives></ref><ref id="cit12"><label>12</label><citation-alternatives><mixed-citation xml:lang="ru">Duncan D.R., Williams M.E., Zehr B.E., Widholm J.M. The production of callus capable of plant regeneration from immature embryos of numerous Zea mays genotypes. Planta. 1985;165(3):322-332. doi 10.1007/BF00392228</mixed-citation><mixed-citation xml:lang="en">Duncan D.R., Williams M.E., Zehr B.E., Widholm J.M. The production of callus capable of plant regeneration from immature embryos of numerous Zea mays genotypes. Planta. 1985;165(3):322-332. doi 10.1007/BF00392228</mixed-citation></citation-alternatives></ref><ref id="cit13"><label>13</label><citation-alternatives><mixed-citation xml:lang="ru">Fan M., Xu C., Xu K., Hu Y. LATERAL ORGAN BOUNDARIES DOMAIN transcription factors direct callus formation in Arabidopsis regeneration. Cell Res. 2012;22(7):1169-1180. doi 10.1038/cr.2012.63</mixed-citation><mixed-citation xml:lang="en">Fan M., Xu C., Xu K., Hu Y. LATERAL ORGAN BOUNDARIES DOMAIN transcription factors direct callus formation in Arabidopsis regeneration. Cell Res. 2012;22(7):1169-1180. doi 10.1038/cr.2012.63</mixed-citation></citation-alternatives></ref><ref id="cit14"><label>14</label><citation-alternatives><mixed-citation xml:lang="ru">Frame B., Main M., Schick R., Wang K. Genetic transformation using maize immature zygotic embryos. In: Thorpe T., Yeung E. (Eds) Plant Embryo Culture. Methods in Molecular Biology. Vol. 710. Humana Press, 2011;327-341. https://doi10.1007/978-1-61737-988-8_22</mixed-citation><mixed-citation xml:lang="en">Frame B., Main M., Schick R., Wang K. Genetic transformation using maize immature zygotic embryos. In: Thorpe T., Yeung E. (Eds) Plant Embryo Culture. Methods in Molecular Biology. Vol. 710. Humana Press, 2011;327-341. https://doi10.1007/978-1-61737-988-8_22</mixed-citation></citation-alternatives></ref><ref id="cit15"><label>15</label><citation-alternatives><mixed-citation xml:lang="ru">Ge F., Luo X., Huang X., Zhang Y., He X., Liu M., Lin H., Peng H., Li L., Zhang Z., Pan G., Shen Y. Genome-wide analysis of transcription factors involved in maize embryonic callus formation. Physiol Plant. 2016;158(4):452-462. doi 10.1111/ppl.12470</mixed-citation><mixed-citation xml:lang="en">Ge F., Luo X., Huang X., Zhang Y., He X., Liu M., Lin H., Peng H., Li L., Zhang Z., Pan G., Shen Y. Genome-wide analysis of transcription factors involved in maize embryonic callus formation. Physiol Plant. 2016;158(4):452-462. doi 10.1111/ppl.12470</mixed-citation></citation-alternatives></ref><ref id="cit16"><label>16</label><citation-alternatives><mixed-citation xml:lang="ru">Gordon-Kamm W., Spencer T.M., Mangano M.L., Adams T.R., Daines R.J., Start W.G., O’Brien J.V., Chambers S.A., Adams W.R. Jr., Willetts N.G., Rice T.B., Mackey C.J., Krueger R.W., Kausch A.P., Lemaux P.G. Transformation of maize cells and regeneration of fertile transgenic plants. Plant Cell. 1990;2(7):603-618. doi 10.1105/tpc.2.7.603</mixed-citation><mixed-citation xml:lang="en">Gordon-Kamm W., Spencer T.M., Mangano M.L., Adams T.R., Daines R.J., Start W.G., O’Brien J.V., Chambers S.A., Adams W.R. Jr., Willetts N.G., Rice T.B., Mackey C.J., Krueger R.W., Kausch A.P., Lemaux P.G. Transformation of maize cells and regeneration of fertile transgenic plants. Plant Cell. 1990;2(7):603-618. doi 10.1105/tpc.2.7.603</mixed-citation></citation-alternatives></ref><ref id="cit17"><label>17</label><citation-alternatives><mixed-citation xml:lang="ru">Green C.E., Phillips R.L. Plant regeneration from tissue cultures of maize. Crop Sci. 1975;15(3):417-421. doi 10.2135/cropsci1975.0011183X001500030040x</mixed-citation><mixed-citation xml:lang="en">Green C.E., Phillips R.L. Plant regeneration from tissue cultures of maize. Crop Sci. 1975;15(3):417-421. doi 10.2135/cropsci1975.0011183X001500030040x</mixed-citation></citation-alternatives></ref><ref id="cit18"><label>18</label><citation-alternatives><mixed-citation xml:lang="ru">Hao Q., Zhang L., Yang Y., Shan Z., Zhou X.A. Genome-wide analysis of the WOX gene family and function exploration of GmWOX18 in soybean. Plants. 2019;8(7):215. doi 10.3390/plants8070215</mixed-citation><mixed-citation xml:lang="en">Hao Q., Zhang L., Yang Y., Shan Z., Zhou X.A. Genome-wide analysis of the WOX gene family and function exploration of GmWOX18 in soybean. Plants. 2019;8(7):215. doi 10.3390/plants8070215</mixed-citation></citation-alternatives></ref><ref id="cit19"><label>19</label><citation-alternatives><mixed-citation xml:lang="ru">He Y., Guo X., Lu R., Niu B., Pasapula V., Hou P., Cai F., Xu Y., Chen F. Changes in morphology and biochemical indices in browning callus derived from Jatropha curcas hypocotyls. Plant Cell Tiss Organ Cult. 2009;98:11-17. doi 10.1007/s11240-009-9533-y</mixed-citation><mixed-citation xml:lang="en">He Y., Guo X., Lu R., Niu B., Pasapula V., Hou P., Cai F., Xu Y., Chen F. Changes in morphology and biochemical indices in browning callus derived from Jatropha curcas hypocotyls. Plant Cell Tiss Organ Cult. 2009;98:11-17. doi 10.1007/s11240-009-9533-y</mixed-citation></citation-alternatives></ref><ref id="cit20"><label>20</label><citation-alternatives><mixed-citation xml:lang="ru">Hisano H., Sato K. Genomic regions responsible for amenability to Agrobacterium-mediated transformation in barley. Sci Rep. 2016; 6(1):37505. doi 10.1038/srep37505</mixed-citation><mixed-citation xml:lang="en">Hisano H., Sato K. Genomic regions responsible for amenability to Agrobacterium-mediated transformation in barley. Sci Rep. 2016; 6(1):37505. doi 10.1038/srep37505</mixed-citation></citation-alternatives></ref><ref id="cit21"><label>21</label><citation-alternatives><mixed-citation xml:lang="ru">Hisano H., Meints B., Moscou M.J., Cistue L., Echávarri B., Sato K., Hayes P.M. Selection of transformation-efficient barley genotypes based on TFA (transformation amenability) haplotype and higher resolution mapping of the TFA loci. Plant Cell Rep. 2017;36(4):611- 620. doi 10.1007/s00299-017-2107-2</mixed-citation><mixed-citation xml:lang="en">Hisano H., Meints B., Moscou M.J., Cistue L., Echávarri B., Sato K., Hayes P.M. Selection of transformation-efficient barley genotypes based on TFA (transformation amenability) haplotype and higher resolution mapping of the TFA loci. Plant Cell Rep. 2017;36(4):611- 620. doi 10.1007/s00299-017-2107-2</mixed-citation></citation-alternatives></ref><ref id="cit22"><label>22</label><citation-alternatives><mixed-citation xml:lang="ru">Jiang Y., Wei X., Zhu M., Zhang X., Jiang Q., Wang Z., Cao Y., An X., Wan X. Developmental regulators in promoting genetic transformation efficiency in maize and other plants. Curr Plant Biol. 2024; 40:100383. doi 10.1016/j.cpb.2024.100383</mixed-citation><mixed-citation xml:lang="en">Jiang Y., Wei X., Zhu M., Zhang X., Jiang Q., Wang Z., Cao Y., An X., Wan X. Developmental regulators in promoting genetic transformation efficiency in maize and other plants. Curr Plant Biol. 2024; 40:100383. doi 10.1016/j.cpb.2024.100383</mixed-citation></citation-alternatives></ref><ref id="cit23"><label>23</label><citation-alternatives><mixed-citation xml:lang="ru">Kamolsukyeunyong W., Dabbhadatta Y., Jaiprasert A., Thunnom B., Poncheewin W., Wanchana S., Ruanjaichon V., Toojinda T., Burns P. Genome-wide association analysis identifies candidate loci for callus induction in rice (Oryza sativa L.). Plants. 2024;13(15):2112. doi 10.3390/plants13152112</mixed-citation><mixed-citation xml:lang="en">Kamolsukyeunyong W., Dabbhadatta Y., Jaiprasert A., Thunnom B., Poncheewin W., Wanchana S., Ruanjaichon V., Toojinda T., Burns P. Genome-wide association analysis identifies candidate loci for callus induction in rice (Oryza sativa L.). Plants. 2024;13(15):2112. doi 10.3390/plants13152112</mixed-citation></citation-alternatives></ref><ref id="cit24"><label>24</label><citation-alternatives><mixed-citation xml:lang="ru">Kausch A.P., Wang K., Kaeppler H.F., Gordon-Kamm W. Maize transformation: history, progress, and perspectives. Mol Breed. 2021; 41(6):38. doi 10.1007/s11032-021-01225-0</mixed-citation><mixed-citation xml:lang="en">Kausch A.P., Wang K., Kaeppler H.F., Gordon-Kamm W. Maize transformation: history, progress, and perspectives. Mol Breed. 2021; 41(6):38. doi 10.1007/s11032-021-01225-0</mixed-citation></citation-alternatives></ref><ref id="cit25"><label>25</label><citation-alternatives><mixed-citation xml:lang="ru">Lardon R., Geelen D. Natural variation in plant pluripotency and regeneration. Plants. 2020;9(10):1261. doi 10.3390/plants9101261</mixed-citation><mixed-citation xml:lang="en">Lardon R., Geelen D. Natural variation in plant pluripotency and regeneration. Plants. 2020;9(10):1261. doi 10.3390/plants9101261</mixed-citation></citation-alternatives></ref><ref id="cit26"><label>26</label><citation-alternatives><mixed-citation xml:lang="ru">Lowe B.A., Way M.M., Kumpf J.M., Rout J., Warner D., Johnson R., Armstrong C.L., Spencer M.T., Chomet P.S. Marker assisted breeding for transformability in maize. Mol Breed. 2006;18:229-239. doi 10.1007/s11032-006-9031-4</mixed-citation><mixed-citation xml:lang="en">Lowe B.A., Way M.M., Kumpf J.M., Rout J., Warner D., Johnson R., Armstrong C.L., Spencer M.T., Chomet P.S. Marker assisted breeding for transformability in maize. Mol Breed. 2006;18:229-239. doi 10.1007/s11032-006-9031-4</mixed-citation></citation-alternatives></ref><ref id="cit27"><label>27</label><citation-alternatives><mixed-citation xml:lang="ru">Lowe K., Wu E., Wang N., Hoerster G., Hastings C., Cho M.J., Scelonge C., Lenderts B., Chamberlin M., Cushatt J., Wang L., Ryan L., Khan T., Chow-Yiu J., Hua W., Yu M., Banh J., Bao Z., Brink K., Igo E., Rudrappa B., Shamseer P.M., Bruce W., Newman L., Shen B., Zheng P., Bidney D., Falco C., Register J., Zhao Z.Y., Xu D., Jones T., Gordon-Kamm W. Morphogenic regulators Baby boom and Wuschel improve monocot transformation. Plant Cell. 2016;28(9):1998-2015. doi 10.1105/tpc.16.00124</mixed-citation><mixed-citation xml:lang="en">Lowe K., Wu E., Wang N., Hoerster G., Hastings C., Cho M.J., Scelonge C., Lenderts B., Chamberlin M., Cushatt J., Wang L., Ryan L., Khan T., Chow-Yiu J., Hua W., Yu M., Banh J., Bao Z., Brink K., Igo E., Rudrappa B., Shamseer P.M., Bruce W., Newman L., Shen B., Zheng P., Bidney D., Falco C., Register J., Zhao Z.Y., Xu D., Jones T., Gordon-Kamm W. Morphogenic regulators Baby boom and Wuschel improve monocot transformation. Plant Cell. 2016;28(9):1998-2015. doi 10.1105/tpc.16.00124</mixed-citation></citation-alternatives></ref><ref id="cit28"><label>28</label><citation-alternatives><mixed-citation xml:lang="ru">Liu X., Bie X.M., Lin X., Li M., Wang H., Zhang X., Yang Y., Zhang C., Zhang X.S., Xiao J. Uncovering the transcriptional regulatory network involved in boosting wheat regeneration and transformation. Nat Plants. 2023;9(6):908-925. doi 10.1038/s41477-023-01406-z</mixed-citation><mixed-citation xml:lang="en">Liu X., Bie X.M., Lin X., Li M., Wang H., Zhang X., Yang Y., Zhang C., Zhang X.S., Xiao J. Uncovering the transcriptional regulatory network involved in boosting wheat regeneration and transformation. Nat Plants. 2023;9(6):908-925. doi 10.1038/s41477-023-01406-z</mixed-citation></citation-alternatives></ref><ref id="cit29"><label>29</label><citation-alternatives><mixed-citation xml:lang="ru">Luo D., Shi L., Sun Z., Qi F., Liu H., Xue L., Li X., Liu H., Qu P., Zhao H., Dai X., Dong W., Zheng Z., Huang B., Fu L., Zhang X. Genome-wide association studies of embryogenic callus induction rate in peanut (Arachis hypogaea L.). Genes. 2024;15(2):160. doi 10.3390/genes15020160</mixed-citation><mixed-citation xml:lang="en">Luo D., Shi L., Sun Z., Qi F., Liu H., Xue L., Li X., Liu H., Qu P., Zhao H., Dai X., Dong W., Zheng Z., Huang B., Fu L., Zhang X. Genome-wide association studies of embryogenic callus induction rate in peanut (Arachis hypogaea L.). Genes. 2024;15(2):160. doi 10.3390/genes15020160</mixed-citation></citation-alternatives></ref><ref id="cit30"><label>30</label><citation-alternatives><mixed-citation xml:lang="ru">Maren N.A., Duan H., Da K., Yencho G.C., Ranney T.G., Liu W. Genotype-independent plant transformation. Hortic Res. 2022;9: uhac047. doi 10.1093/hr/uhac047</mixed-citation><mixed-citation xml:lang="en">Maren N.A., Duan H., Da K., Yencho G.C., Ranney T.G., Liu W. Genotype-independent plant transformation. Hortic Res. 2022;9: uhac047. doi 10.1093/hr/uhac047</mixed-citation></citation-alternatives></ref><ref id="cit31"><label>31</label><citation-alternatives><mixed-citation xml:lang="ru">McFarland F.L., Collier R., Walter N., Martinell B., Kaeppler S.M., Kaeppler H.F. A key to totipotency: Wuschel-like homeobox 2a unlocks embryogenic culture response in maize (Zea mays L.). Plant Biotechnol J. 2023;21(9):1860-1872. doi 10.1111/pbi.14098</mixed-citation><mixed-citation xml:lang="en">McFarland F.L., Collier R., Walter N., Martinell B., Kaeppler S.M., Kaeppler H.F. A key to totipotency: Wuschel-like homeobox 2a unlocks embryogenic culture response in maize (Zea mays L.). Plant Biotechnol J. 2023;21(9):1860-1872. doi 10.1111/pbi.14098</mixed-citation></citation-alternatives></ref><ref id="cit32"><label>32</label><citation-alternatives><mixed-citation xml:lang="ru">Menz J., Modrzejewski D., Hartung F., Wilhelm R., Sprink T. Genome edited crops touch the market: a view on the global development and regulatory environment. Front Plant Sci. 2020;11:586027. doi 10.3389/fpls.2020.586027</mixed-citation><mixed-citation xml:lang="en">Menz J., Modrzejewski D., Hartung F., Wilhelm R., Sprink T. Genome edited crops touch the market: a view on the global development and regulatory environment. Front Plant Sci. 2020;11:586027. doi 10.3389/fpls.2020.586027</mixed-citation></citation-alternatives></ref><ref id="cit33"><label>33</label><citation-alternatives><mixed-citation xml:lang="ru">Nagle M.F., Yuan J., Kaur D., Ma C., Peremyslova E., Jiang Y., Niño de Rivera A., Jawdy S., Chen J.G., Feng K., Yates T.B., Tuskan G.A., Muchero W., Fuxin L., Strauss S.H. GWAS supported by computer vision identifies large numbers of candidate regulators of in planta regeneration in Populus trichocarpa. G3. 2024;14(4):jkae026. doi 10.1093/g3journal/jkae026</mixed-citation><mixed-citation xml:lang="en">Nagle M.F., Yuan J., Kaur D., Ma C., Peremyslova E., Jiang Y., Niño de Rivera A., Jawdy S., Chen J.G., Feng K., Yates T.B., Tuskan G.A., Muchero W., Fuxin L., Strauss S.H. GWAS supported by computer vision identifies large numbers of candidate regulators of in planta regeneration in Populus trichocarpa. G3. 2024;14(4):jkae026. doi 10.1093/g3journal/jkae026</mixed-citation></citation-alternatives></ref><ref id="cit34"><label>34</label><citation-alternatives><mixed-citation xml:lang="ru">Nam J., Matthysse A.G., Gelvin S.B. Differences in susceptibility of Arabidopsis ecotypes to crown gall disease may result from a deficiency in T-DNA integration. Plant Cell. 1997;9:317-333. doi 10.1105/tpc.9.3.317</mixed-citation><mixed-citation xml:lang="en">Nam J., Matthysse A.G., Gelvin S.B. Differences in susceptibility of Arabidopsis ecotypes to crown gall disease may result from a deficiency in T-DNA integration. Plant Cell. 1997;9:317-333. doi 10.1105/tpc.9.3.317</mixed-citation></citation-alternatives></ref><ref id="cit35"><label>35</label><citation-alternatives><mixed-citation xml:lang="ru">Nishimura A., Ashikari M., Lin S., Takashi T., Angeles E.R., Yamamoto T., Matsuoka M., Khush G.S. Isolation of a rice regeneration quantitative trait loci gene and its application to transformation systems. Proc Natl Acad Sci USA. 2005;102(33):11940-11944. doi 10.1073/pnas.0504220102</mixed-citation><mixed-citation xml:lang="en">Nishimura A., Ashikari M., Lin S., Takashi T., Angeles E.R., Yamamoto T., Matsuoka M., Khush G.S. Isolation of a rice regeneration quantitative trait loci gene and its application to transformation systems. Proc Natl Acad Sci USA. 2005;102(33):11940-11944. doi 10.1073/pnas.0504220102</mixed-citation></citation-alternatives></ref><ref id="cit36"><label>36</label><citation-alternatives><mixed-citation xml:lang="ru">Nivya V.M., Shah J.M. Recalcitrance to transformation, a hindrance for genome editing of legumes. Front Genome Ed. 2023;5:1247815. doi 10.3389/fgeed.2023.1247815</mixed-citation><mixed-citation xml:lang="en">Nivya V.M., Shah J.M. Recalcitrance to transformation, a hindrance for genome editing of legumes. Front Genome Ed. 2023;5:1247815. doi 10.3389/fgeed.2023.1247815</mixed-citation></citation-alternatives></ref><ref id="cit37"><label>37</label><citation-alternatives><mixed-citation xml:lang="ru">Omidbakhshfard M.A., Proost S., Fujikura U., Mueller-Roeber B. Growth-regulating factors (GRFs): a small transcription factor family with important functions in plant biology. Mol Plant. 2015;8(7): 998-1010. doi 10.1016/j.molp.2015.01.013</mixed-citation><mixed-citation xml:lang="en">Omidbakhshfard M.A., Proost S., Fujikura U., Mueller-Roeber B. Growth-regulating factors (GRFs): a small transcription factor family with important functions in plant biology. Mol Plant. 2015;8(7): 998-1010. doi 10.1016/j.molp.2015.01.013</mixed-citation></citation-alternatives></ref><ref id="cit38"><label>38</label><citation-alternatives><mixed-citation xml:lang="ru">Pixley K.V., Falck-Zepeda J.B., Paarlberg R.L., Phillips P.W., SlametLoedin I.H., Dhugga K.S., Campos H., Gutterson N. Genome-edited crops for improved food security of smallholder farmers. Nat Genet. 2022;54(4):364-367. doi 10.1038/s41588-022-01046-7</mixed-citation><mixed-citation xml:lang="en">Pixley K.V., Falck-Zepeda J.B., Paarlberg R.L., Phillips P.W., SlametLoedin I.H., Dhugga K.S., Campos H., Gutterson N. Genome-edited crops for improved food security of smallholder farmers. Nat Genet. 2022;54(4):364-367. doi 10.1038/s41588-022-01046-7</mixed-citation></citation-alternatives></ref><ref id="cit39"><label>39</label><citation-alternatives><mixed-citation xml:lang="ru">Ricroch A., Clairand P., Harwood W. Use of CRISPR systems in plant genome editing: toward new opportunities in agriculture. Emerg Top Life Sci. 2017;1(2):169-182. doi 10.1042/etls20170085</mixed-citation><mixed-citation xml:lang="en">Ricroch A., Clairand P., Harwood W. Use of CRISPR systems in plant genome editing: toward new opportunities in agriculture. Emerg Top Life Sci. 2017;1(2):169-182. doi 10.1042/etls20170085</mixed-citation></citation-alternatives></ref><ref id="cit40"><label>40</label><citation-alternatives><mixed-citation xml:lang="ru">Russell W.A. Registration of B70 and B73 parental lines of maize (Reg. Nos. PL16 and PL17). Crop Sci. 1972;12:721. doi 10.2135/cropsci1972.0011183X001200050085x</mixed-citation><mixed-citation xml:lang="en">Russell W.A. Registration of B70 and B73 parental lines of maize (Reg. Nos. PL16 and PL17). Crop Sci. 1972;12:721. doi 10.2135/cropsci1972.0011183X001200050085x</mixed-citation></citation-alternatives></ref><ref id="cit41"><label>41</label><citation-alternatives><mixed-citation xml:lang="ru">Salvo S., Cook J., Carlson A.R., Hirsch C.N., Kaeppler S.M., Kaeppler H.F. Genetic fine-mapping of a quantitative trait locus (QTL) associated with embryogenic tissue culture response and plant regeneration ability in maize (Zea mays L.). Plant Genome. 2018; 11(2):170111. doi 10.3835/plantgenome2017.12.0111</mixed-citation><mixed-citation xml:lang="en">Salvo S., Cook J., Carlson A.R., Hirsch C.N., Kaeppler S.M., Kaeppler H.F. Genetic fine-mapping of a quantitative trait locus (QTL) associated with embryogenic tissue culture response and plant regeneration ability in maize (Zea mays L.). Plant Genome. 2018; 11(2):170111. doi 10.3835/plantgenome2017.12.0111</mixed-citation></citation-alternatives></ref><ref id="cit42"><label>42</label><citation-alternatives><mixed-citation xml:lang="ru">Song X., Han Y., Teng W., Sun G., Li W. Identification of QTL underlying somatic embryogenesis capacity of immature embryos in soybean (Glycine max (L.) Merr.). Plant Cell Rep. 2010;29(2):125-131. doi 10.1007/s00299-009-0804-1</mixed-citation><mixed-citation xml:lang="en">Song X., Han Y., Teng W., Sun G., Li W. Identification of QTL underlying somatic embryogenesis capacity of immature embryos in soybean (Glycine max (L.) Merr.). Plant Cell Rep. 2010;29(2):125-131. doi 10.1007/s00299-009-0804-1</mixed-citation></citation-alternatives></ref><ref id="cit43"><label>43</label><citation-alternatives><mixed-citation xml:lang="ru">Timonova E.M., Kiseleva A.A., Berezhnaia A.A., Nesterov M.A., Adonina I.G., Kochetov A.V., Salina E.A. Modification of agricultural traits in cultivated varieties of barley and wheat. Ecol Genet. 2023; 21:24-25. doi 10.17816/ecogen568184</mixed-citation><mixed-citation xml:lang="en">Timonova E.M., Kiseleva A.A., Berezhnaia A.A., Nesterov M.A., Adonina I.G., Kochetov A.V., Salina E.A. Modification of agricultural traits in cultivated varieties of barley and wheat. Ecol Genet. 2023; 21:24-25. doi 10.17816/ecogen568184</mixed-citation></citation-alternatives></ref><ref id="cit44"><label>44</label><citation-alternatives><mixed-citation xml:lang="ru">Xu H., Guo Y., Qiu L., Ran Y. Progress in soybean genetic transformation over the last decade. Front Plant Sci. 2022;13:900318. doi 10.3389/fpls.2022.900318</mixed-citation><mixed-citation xml:lang="en">Xu H., Guo Y., Qiu L., Ran Y. Progress in soybean genetic transformation over the last decade. Front Plant Sci. 2022;13:900318. doi 10.3389/fpls.2022.900318</mixed-citation></citation-alternatives></ref><ref id="cit45"><label>45</label><citation-alternatives><mixed-citation xml:lang="ru">Yang C., Zhao T., Yu D., Gai J. Somatic embryogenesis and plant regeneration in Chinese soybean (Glycine max (L.) Merr.) – impacts of mannitol, abscisic acid, and explant age. In Vitro Cell Dev Biol Plant. 2009;45:180-188. doi 10.1007/s11627-009-9205-y</mixed-citation><mixed-citation xml:lang="en">Yang C., Zhao T., Yu D., Gai J. Somatic embryogenesis and plant regeneration in Chinese soybean (Glycine max (L.) Merr.) – impacts of mannitol, abscisic acid, and explant age. In Vitro Cell Dev Biol Plant. 2009;45:180-188. doi 10.1007/s11627-009-9205-y</mixed-citation></citation-alternatives></ref><ref id="cit46"><label>46</label><citation-alternatives><mixed-citation xml:lang="ru">Yang C., Zhao T., Yu D., Gai J. Mapping QTLs for tissue culture response in soybean (Glycine max (L.) Merr.). Mol Cells. 2011; 32(4):337-342. doi 10.1007/s10059-011-0063-1</mixed-citation><mixed-citation xml:lang="en">Yang C., Zhao T., Yu D., Gai J. Mapping QTLs for tissue culture response in soybean (Glycine max (L.) Merr.). Mol Cells. 2011; 32(4):337-342. doi 10.1007/s10059-011-0063-1</mixed-citation></citation-alternatives></ref><ref id="cit47"><label>47</label><citation-alternatives><mixed-citation xml:lang="ru">Zhang K., Su J., Xu M., Zhou Z., Zhu X., Ma X., Hou J., Tan L., Zhu Z., Cai H., Liu F., Sun H., Gu P., Li C., Liang Y., Zhao W., Sun C., Fu Y. A common wild rice-derived BOC1 allele reduces callus browning in indica rice transformation. Nat Commun. 2020;11(1):443. doi 10.1038/s41467-019-14265-0</mixed-citation><mixed-citation xml:lang="en">Zhang K., Su J., Xu M., Zhou Z., Zhu X., Ma X., Hou J., Tan L., Zhu Z., Cai H., Liu F., Sun H., Gu P., Li C., Liang Y., Zhao W., Sun C., Fu Y. A common wild rice-derived BOC1 allele reduces callus browning in indica rice transformation. Nat Commun. 2020;11(1):443. doi 10.1038/s41467-019-14265-0</mixed-citation></citation-alternatives></ref><ref id="cit48"><label>48</label><citation-alternatives><mixed-citation xml:lang="ru">Zhang Z., Zhao H., Li W., Wu J., Zhou Z., Zhou F., Chen H., Lin Y. Genome-wide association study of callus induction variation to explore the callus formation mechanism of rice. J Integr Plant Biol. 2019;61(11):1134-1150. doi 10.1111/jipb.12759</mixed-citation><mixed-citation xml:lang="en">Zhang Z., Zhao H., Li W., Wu J., Zhou Z., Zhou F., Chen H., Lin Y. Genome-wide association study of callus induction variation to explore the callus formation mechanism of rice. J Integr Plant Biol. 2019;61(11):1134-1150. doi 10.1111/jipb.12759</mixed-citation></citation-alternatives></ref></ref-list><fn-group><fn fn-type="conflict"><p>The authors declare that there are no conflicts of interest present.</p></fn></fn-group></back></article>
