Genetic control of plant morphogenesis in in vitro culture

  • O. V. Dubrovna Institute of Plant Physiology and Genetics, NAS of Ukraine, Ukraine, 03022, Kyiv, Vasylkivska str., 31/17
  • S. I. Mykhalska Institute of Plant Physiology and Genetics, NAS of Ukraine, Ukraine, 03022, Kyiv, Vasylkivska str., 31/17 https://orcid.org/0000-0002-6644-5921
  • A. H. Komisarenko Institute of Plant Physiology and Genetics, NAS of Ukraine, Ukraine, 03022, Kyiv, Vasylkivska str., 31/17 https://orcid.org/0000-0003-2081-4055
DOI: https://doi.org/10.7124/visnyk.utgis.22.1-2.1688
Keywords: morphogenesis, genetic control, callusogenesis, somatic embryogenesis, de novo organogenesis

Abstract

Plant morphogenesis is the result of complex interactions of genetic, epigenetic and hormonal factors that determine the development of cells and tissues in in vitro culture. In recent decades, basic research has greatly advanced the understanding of the genetic mechanisms that control key processes of morphogenesis, such as callusogenesis, somatic embryogenesis, and de novo organogenesis. It was found that certain structural and regulatory genes play a crucial role in reprogramming cells to a totipotent state, where they are able to form various morphological structures. Hormones, such as auxins and cytokinins, contribute to the induction of these processes by changing the expression of genes responsible for division, differentiation and other aspects of morphogenesis. The literature review presents modern ideas on genetic control of morphogenesis in plant culture in vitro. A wide range of key genes that determine callus formation is given; participate in somatic embryogenesis and enhancement of the somatic embryogenic response; involved in the ectopic formation of somatic embryos or meristems; control de novo organogenesis and participate in hormone signal transduction. The interaction of various transcription factors, which participate in the induction of morphogenesis and are involved in the signaling pathway of hormones, is shown.

References

Adamczyk B. J., Lehti-Shiu M. D., Fernandez D. E. The MADS domain factors AGL15 and AGL18 act redundantly as repressors of the floral transition in Arabidopsis. Plant J. 2007. Vol. 50. P. 1007–1019. doi: 10.1111/j.1365-313X.2007.03105.x.

Aida M., Ishida Т., Tasaka M. Shoot apical meristem and cotyledon formation during Arabidopsis embryogenesis: interaction among the CUP-SHAPED COTYLEDON and SHOOT MERISTEMLESS genes. Development. 1999. Vol. 126(8). P. 1563–1570. doi: 10.1242/dev.126.8.1563.

Arroyo-Herrera A., Ku Gonzalez A., Canche Moo R., Quiroz-Figueroa F. R., Loyola-Vargas V. M., Rodriguez-Zapata L. C., Burgeff D’Hondt C., Suárez-Solís V. M., Castaño E. Expression of WUSCHEL in Coffea canephora causes ectopic morphogenesis and increases somatic embryogenesis. Plant Cell, Tissue Organ Culture. 2008. Vol. 94. P. 171–180. doi: 10.1007/s11240-008-9401-1.

Ayil-Gutiérrez B., Galaz-Avalos R.M., Peña-Cabrera E., Loyola-Vargas V.M. Dynamics of the concentration of IAA and some of its conjugates during the induction of somatic embryogenesis in Coffea canephora. Plant Signal. Behav. 2013, Vol.8(11), e26998. doi: 10.4161/psb.26998.

Baud S., Kelemen Z., Thévenin J., Boulard C., Blanchet S., To A., Payre M., Berger N., Effroy-Cuzzi D., Franco-Zorrilla J. M., Godoy M., Solano R., Thevenon E., Parcy F., Lepiniec L., Dubreucq B. Deciphering the molecular mechanisms underpinning the transcriptional control of gene expression by master transcriptional regulators in Arabidopsis seed. Plant Physiol. 2016. Vol. 171(2). P. 1099–1112. doi: 10.1104/pp.16.00034.

Belide S., Zhou X. R., Kennedy Y., Lester G., Shrestha P., Petrie J. R., Singh S. P. Rapid expression and validation of seed-specific constructs in transgenic LEC2 induced somatic embryos of Brassica napus. Plant Cell. Tissue Organ Cult. 2013. Vol. 113. P. 543–553. doi: 10.1007/s11240-013-0295-1.

Berckmans, B., Vassileva, V., Schmid, S.P., Maes, S., Parizot, B., Naramoto, S., Magyar Z., Alvim Kamei C. L., Koncz C., Bögre L., Persiau G., De Jaeger G., Friml J., Simon R., Beeckman T., De Veylder L. Auxin-dependent cell cycle reactivation through transcriptional regulation of Arabidopsis E2Fa by lateral organ boundary proteins. Plant Cell. 2011. Vol. 23(10). Р. 3671–3683. doi: 10.1105/tpc.111.088377.

Bidabadi S. S., Jain S. M. Cellular, Molecular, and Physiological Aspects of In Vitro Plant Regeneration. Plants. 2020. Vol. 9(6). P. 702. doi: 10.3390/plants9060702.

Blakeslee J. J., Spatola Rossi T., Kriechbaumer V. Auxin biosynthesis: Spatial regulation and adaptation to stress. J Exp Bot. 2019. Vol. 70(19). P. 5041–5049. doi: 10.1093/jxb/erz283.

Bouchabké-Coussa O., Obellianne M., Linderme D., Montes E., Maia-Grondard A., Vilaine F., Pannetier C. WUSCHEL overexpression promotes somatic embryogenesis and induces organogenesis in cotton (Gossypium hirsutum L.) tissues cultured in vitro. Plant Cell Rep. 2013, Vol. 32(5). P. 675–686. doi: 10.1007/s00299-013-1402-9.

Boutilier K., Offringa R., Sharma V. K., Kieft H., Ouellet T., Zhang L., Hattori J., Liu C.-M., van Lammeren A. A. M., Miki B. L. A., Custers J. B., van Lookeren Campagne M. M. Ectopic expression of BABY-BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell. 2002. Vol. 14(8). P. 1737–1749. doi: 10.1105/tpc.001941.

Brand A., Quimbaya M., Tohme J., Chavarriaga-Aguirre P. Arabidopsis LEC1 and LEC2 orthologous genes are key regulators of somatic embryogenesis in cassava. Front Plant Sci. 2019. Vol. 10. P. 673. doi: 10.3389/fpls.2019.00673.

Brandstatter I., Kieber J. J. Two genes with similarity to bacterial response regulators are rapidly and specifically induced by cytokinin in Arabidopsis. Plant Cell. 1998. Vol. 10(6). P. 1009–1019. doi: 10.1105/tpc.10.6.1009.

Cao A., Zheng Y., Yu Y., Wang X., Shao D., Sun J., Cui B. Comparative transcriptome analysis of SE initial dedifferentiation in cotton of different SE capability. Sci. Rep. 2017. Vol. 7(1). P. 8583–8595. doi: 10.1038/s41598-017-08763-8.

Carbonero P., Iglesias-Fernández R., Vicente-Carbajosa J. The AFL subfamily of B3 transcription factors: Evolution and function in angiosperm seeds. J Exp Bot. 2017. Vol. 68(4). P. 871–880. doi: 10.1093/jxb/erw458.

Cary A. J., Che P., Howell S. H. Developmental events and shoot apical meristem gene expression patterns during shoot development in Arabidopsis thaliana. Plant J. 2002. Vol. 32(6). P. 867–877. doi: 10.1046/j.1365-313X.2002.01479.x

Cary A. J., Che P., Howell S. H. Developmental events and shoot apical meristem gene expression patterns during shoot development in Arabidopsis thaliana. Plant J. 2002. Vol. 32(6). P. 867–877. doi: 10.1046/j.1365-313x.2002.01479.x.

Chen Y., Xu X., Liu Z., Zhang Z., Han X., Lin Y., Lai Z. Global scale transcriptome analysis reveals differentially expressed genes involve in early somatic embryogenesis in Dimocarpus longan Lour. Bmc Genom. 2020. Vol. 21(1). P. 1–22. doi: 10.1186/s12864-019-6393-7.

Chen L., Tong J., Xiao L., Ruan Y., Liu J., Zeng M., Huang H., Wang J-W., Xu L. YUCCA-mediated auxin biogenesis is required for cell fate transition occurring during de novo root organogenesis in Arabidopsis. J. Exp. Bot. 2016. Vol. 67(14). P. 4273–4284. doi: 10.1093/jxb/erw213.

Ckurshumova W., Smirnova T., Marcos D., Zayed Y., Berleth T. Irrepressible MONOPTEROS/ARF5 promotes de novo shoot formation. New Phytol. 2014. Vol. 204. P. 556–566. doi: 10.1111/nph.13014.

Daimon Y., Takabe K., Tasaka M. The CUP-SHAPED COTYLEDON genes promote adventitious shoot formation on calli. Plant Cell Physiol. 2003. Vol. 44(2). P. 113–121. doi: 10.1093/pcp/pcg038

De Rybel B., Audenaert D., Beeckman T., Kepinski S. The past, present, and future of chemical biology in auxin research. Acs Chem Biol. 2009. Vol. 4(12). P. 987–998. doi: 10.1021/cb9001624.

Dolzblasz A., Nardmann J., Clerici E., Causier B., Van der Graaff E., Chen J., Davies B., Werr W., Laux, T. Stem cell regulation by Arabidopsis WOX genes. Mol. Plant. 2016. Vol. 9(7). P. 1028–1039. doi: 10.1016/j.molp.2016.04.007.

El Ouakfaoui S., Schnell J., Abdeen A., Colville A., Labbé H., Han S., Baum B., Laberge S., Miki B. Control of somatic embryogenesis and embryo development by AP2 transcription factors. Plant Mol Biol. 2010. Vol. 74(4-5). P. 313–326. doi: 10.1007/s11103-010-9674-8.

Elhiti M., Tahir M., Gulden R. H., Khamiss K., Stasolla C. Modulation of embryo-forming capacity in culture through the expression of Brassica genes involved in the regulation of the shoot apical meristem. J Exp Bot. 2010. Vol. 61(14). P. 4069–4085. doi: 10.1093/jxb/erq222.

Emery J. F., Floyd S. K., Alvarez J., Eshed Y., Hawker N. P., Izhaki A., Baum S. F., Bowman J. L. Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. Curr Biol. 2003. Vol. 13(20). P. 1768–1774. doi: 10.1016/j.cub.2003.09.035.

Fan M., Xu C., Xu K., Hu Y. LATERAL ORGAN BOUNDARIES DOMAIN transcription factors direct callus formation in Arabidopsis regeneration. Cell Res. 2012. Vol. 22(7). Р. 1169–1180. doi: 10.1038/cr.2012.63.

Fister A. S., Landherr L., Perryman M., Zhang Y., Guiltinan M. J., Maximova S. N. Glucocorticoid receptor-regulated TcLEC2 expression triggers somatic embryogenesis in Theobroma cacao leaf tissue. PLoS ONE. 2018. Vol. 13(11). e0207666. doi: 10.1371/journal.pone.0207666.

Florez S. L., Erwin R. L., Maximova S. N., Guiltinan M. J., Curtis W. R. Enhanced somatic embryogenesis in Theobroma cacao using the homologous BABY BOOM transcription factor. BMC Plant Biol. 2015. Vol. 15. P. 121. doi: 10.1186/s12870-015-0479-4.

Frank M., Guivarch A., Krupkova E., Lorenz-Meyer I., Chriqui D., Schmülling T. Tumorous shoot development (TSD) genes are required for co-ordinated plant shoot development. Plant J. 2002. Vol. 29(1). P. 73–85. doi: 10.1046/j.1365-313x.2002.01197.x.

Frank M., Rupp H-M., Prinsen E., Motyka V., Van Onckelen H., Schmülling T. Hormone autotrophic growth and differentiation identifies mutant lines of Arabidopsis with altered cytokinin and auxin content or signaling. Plant Phsiol. 2000. Vol. 122(3). P. 721–9. doi: 10.1104/pp.122.3.721.

Galinha C., Hofhuis H., Luijten M., Willemsen V., Blilou I., Heidstra R., Scheres B. PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development. Nature. 2007. Vol. 449(7165). P. 1053–1057. doi: 10.1038/nature06206.

Gallois J. L., Nora F. R., Mizukami Y., Sablowski R. WUSCHEL induces shoot stem cell activity and developmental plasticity in the root meristem. Genes Dev. 2004. Vol. 18(4). P. 375–380. doi: 10.1101/gad.291204.

Gallois J. L., Woodward C., Reddy G. V., Sablowski R. Combined SHOOT MERISTEMLESS and WUSCHEL trigger ectopic organogenesis in Arabidopsis. Development. 2002. Vol. 129(13). P. 3207–3217. doi: 10.1242/dev.129.13.3207.

Gambino G., Minuto M., Boccacci P., Perrone I., Vallania R., Gribaudo I. Characterization of expression dynamics of WOX homeodomain transcription factors during somatic embryogenesis in Vitis vinifera. J Exp Bot. 2010. Vol. 62(3). P. 1089–1101. doi: 10.1093/jxb/erq349.

Gazzarrini S., Tsuchiya Y., Lumba S., Okamoto M., McCourt P. The transcription factor FUSCA3 controls developmental timing in Arabidopsis through the hormones gibberellin and abscisic acid. Dev Cell. 2004. Vol. 7(3). P. 373–385. doi: 10.1016/j.devcel.2004.06.017.

Gliwicka M., Nowak K., Balazadeh S., Mueller-Roeber B., Gaj M. D. Extensive Modulation of the transcription factor transcriptome during somatic embryogenesis in Arabidopsis thaliana. PLoS ONE. 2013. Vol. 8(7). e69261. doi: 10.1371/journal.pone.0069261.

Gordon S. P., Heisler M. G., Reddy G. V., Ohno C., Das P., Meyerowitz E. M. Pattern formation during de novo assembly of the Arabidopsis shoot meristem. Development. 2007. Vol. 134(19). Р. 3539–3548. doi: 10.1242/dev.010298.

Gordon-Kamm B., Sardesai N., Arling M., Lowe K., Hoerster G., Betts S., Jones T. Using Morphogenic Genes to Improve Recovery and Regeneration of Transgenic Plants. Plants. 2019. Vol. 8(2). Р. 38. doi: 10.3390/plants8020038.

Grafi G., Chalifa-Caspi V., Nagar T., Plaschkes I., Barak S., Ransbotyn V. Plant response to stress meets dedifferentiation. Planta. 2011. Vol. 233. P. 433–438. doi: 10.1007/s00425-011-1366-3.

Grienenberger E., Fletcher J. C. Polypeptide signaling molecules in plant development. Curr. Opin. Plant Biol. 2015. Vol. 23. Р. 8–14. doi: 10.1016/j.pbi.2014.09.013.

Guo F., Liu C., Xia H. Induced expression of AtLEC1 and AtLEC2 differentially promotes somatic embryogenesis in transgenic tobacco plants. PLoS ONE. 2013. Vol 8(8). e71714. doi: 10.1371/journal.pone.0071714.

Haecker A., Groß-Hardt R., Geiges B., Sarkar A., Breuninger H., Herrmann M., Laux T. Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana. Development. 2004. Vol. 131(3). P. 657–668. doi: 10.1242/dev.00963.

Harding E. W., Tang W., Nichols K. W., Fernandez D. E., Perry S. E. Expression and maintenance of embryogenic potential is enhanced through constitutive expression of AGAMOUS-LIKE15. Plant Physiol. 2003. Vol. 133(2). P. 653–663. doi: 10.1104/pp.103.023499.

Hecht V., Vielle-Calzada J.-P., Hartog M. V., Schmidt E. D., Boutilier K., Grossniklaus U., de Vries S. C. The Arabidopsis Somatic Embryogenesis Receptor Kinase I gene is expressed in developing ovules and embryos and enhances embryogenic competence in culture. Plant Physiol. 2001. Vol. 127(3). P. 803–816. doi: 10.1104/pp.010324.

Heyman, J., Cools, T., Canher, B., Shavialenka, S., Traas, J., Vercauteren, I., Van den Daele H., Persiau G., De Jaeger G., Sugimoto K., De Veylder L. The heterodimeric transcription factor complex ERF115–PAT1 grants regeneration competence. Nat Plants. 2016. Vol. 2(11). P. 16165–16167. doi: 10.1038/nplants.2016.165.

Horstman A., Bemer M., Boutilier K. A transcriptional view on somatic embryogenesis. Regeneration. 2017a. Vol. 4(4). P. 201–216. doi: 10.1002/reg2.91.

Horstman A., Li M., Heidmann I., Weemen M., Chen B., Muino J. M., Angenent G. C., Boutiliera K. The BABY BOOM transcription factor activates the LEC1-ABI3-FUS3-LEC2 network to induce somatic embryogenesis. Plant Physiol. 2017b. Vol. 175(2). P. 848–857. doi: 10.1104/pp.17.00232.

Hu B., Zhang G., Liu W., Shi J., Wang H., Qi M., Li J., Qin P., Ruan Y., Huang H., Zhang Y., Xu L. Divergent regenerationcompetent cells adopt a common mechanism for callus initiation in angiosperms. Regeneration. 2017. Vol. 4(3). Р. 132–139. doi: 10.1002/reg2.82.

Ibanez S., Carneros E., Testillano P. S., Perez-Perez J. M. Advances in Plant Regeneration: Shake, Rattle and Roll. Plants. 2020. Vol. 9(7). P. 897. doi: 10.3390/plants9070897.

Ikeda Y., Banno H., Niu Q. W., Howell S. H., Chua N. H. The enhancer of shoot regeneration 2 gene in Arabidopsis regulates cup-shaped cotyledon 1 at the transcriptional level and controls cotyledon development. Plant Cell Physiol. 2006. Vol. 47(11). P. 1443–1456. doi: 10.1093/pcp/pcl023.

Ikeuchi M., Iwase A., Rymen B., Lambolez A., Kojima M., Takebayashi Y., Heyman J., Watanabe S., Seo M., De Veylder L, Sakakibara H., Sugimoto K. Wounding triggers callus formation via dynamic hormonal and transcriptional changes. Plant Physiol. 2017. Vol. 175(3). Р. 1158–1174. doi: 10.1104/pp.17.01035.

Ikeuchi M., Ogawa Y., Iwase A., Sugimoto K. Plant regeneration: Cellular origins and molecular mechanisms. Development. 2016. Vol. 143(9). Р. 1442–1451. doi: 10.1242/dev.134668.

Ikeuchi M., Sugimoto K., Iwase A. Plant callus: mechanisms of induction and repression. Plant Cell. 2013. Vol. 25(9). Р. 3159–3173. doi: 10.1105/tpc.113.116053.

Ishihara H., Sugimoto K., Tarr P., T., Temman H., Kadokura S., Inui Y., Sakamoto T., Sasaki T., Aida M., Suzuki T., Inagaki S., Morohashi K., Seki M., Kakutani T., Meyerowitz E. M., Matsunaga S. Primed histone demethylation regulates shoot regenerative competency. Nat Commun. 2019. Vol. 10(1). P. 1786. doi: 10.1038/s41467-019-09386-5.

Iwase A., Harashima H., Ikeuchi M., Rymen B., Ohnuma M., Komaki S., Morohashi K., Kurata T., Nakata M., Ohme-Takagi M. WIND1 promotes shoot regeneration through transcriptional activation of ENHANCER OF SHOOT REGENERATION1 in Arabidopsis. Plant Cell. 2017. Vol. 29(1). P. 54–69. doi: 10.1105/tpc.16.00623.

Jha P., Ochatt S. J., Kumar V. WUSCHEL: A master regulator in plant growth signaling. Plant Cell Rep. 2020. Vol. 39(4). P. 431–444. doi: 10.1007/s00299-020-02511-5.

Jo L., Pelletier J. M., Harada J. J. Central role of the LEAFY COTYLEDON1 transcription factor in seed development. J Integr Plant Biol. 2019. Vol. 61(5). P. 564–580. doi: 10.1111/jipb.12806.

Junker A., Mönke G., Rutten T., Keilwagen J., Seifert M., Thi T. M. N., Renou J-P., Balzergue S., Viehöver P., Hähnel U., Ludwig-Müller J. Elongation-related functions of LEAFY COTYLEDON1 during the development of Arabidopsis thaliana. Plant J. 2012. Vol. 71(3). P. 427–442. doi: 10.1111/j.1365-313X.2012.04999.x.

Kakimoto T. CKI1, a histidine kinase homolog implicated in cytokinin signal transduction. Science. 1996. Vol. 274(5289). P. 982–985. doi: 10.1126/science.274.5289.982

Karami O., Rahimi A., Mak P., Horstman A., Boutilier K., Compier M., van der Zaal B., Offringa R. An Arabidopsis AT-hook motif nuclear protein mediates somatic embryogenesis and coinciding genome duplication. Nat. Commun. 2021. Vol. 12(1). 2508. doi: 10.1038/s41467-021-22815-8.

Kareem A, Durgaprasad K, Sugimoto K, Du Y, Pulianmackal AJ, Trivedi ZB, Abhayadev P. V., Pinon V., Meyerowitz E. M., Scheres B., Prasad K. PLETHORA genes control regeneration by a two-step mechanism. Curr Biol. 2015. Vol. 25(8). Р. 1017–1030. doi: 10.1016/j.cub.2015.02.022.

Karlova R., Boeren S., Russinova E., Aker J., Vervoort J., de Vries S. The Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASE1 protein complex includes brassinosteroid-insensitive1. Plant Cell. 2006. Vol. 18(3). P. 626–638. doi: 10.1105/tpc.105.039412.

Kunakh V. A. Biotechnology of medicinal plants. Genetic, physiological and biochemical basis. Kyiv: Logos, 2005. 730 p. [in Ukrainian].

Kyo M., Maida K., Nishioka Y., Matsui K. Coexpression of WUSCHEL related homeobox (WOX) 2 with WOX8 or WOX9 promotes regeneration from leaf segments and free cells in Nicotiana tabacum L. Plant Biotechnol. 2018. Vol. 35(1). P. 23–30. doi: 10.5511/plantbiotechnology.18.0126a.

Laux T., Mayer K. F., Berger J., Jurgens G. The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development. 1996. Vol. 122(1). P. 87–96. doi: 10.1242/dev.122.1.87.

Ledwo´n A., Gaj M. D. LEAFY COTYLEDON1, FUSCA3 expression and auxin treatment in relation to somatic embryogenesis induction in Arabidopsis. Plant Growth Regul. 2011. Vol. 65. P. 157–167. doi: 10.1007/s10725-011-9585-y.

Lee K., Kim J. H., Park O. S., Jung Y. J., Seo P. Ectopic expression of WOX5 promoters cytokinin signaling and de novo shoot regeneration. Plant Cell Rep. 2022. Vol. 41(12). P. 2415–2422. doi: 10.1007/s00299-022-02932-4.

Lee K., Seo P. J. Dynamic epigenetic changes during plant regeneration. Trends Plant Sci. 2018. Vol. 23(3). Р. 235–247. doi: 10.1016/j.tplants.2017.11.009.

Li J., Wang M., Li Y., Zhang Q., Lindsey K., Daniell H., Jin S., Zhang X. Multi-omics analyses reveal epigenomics basis for cotton somatic embryogenesis through successive regeneration acclimation process. Plant Biotechnol. J. 2019. Vol. 17. P. 435–450. doi: 10.1111/pbi.12988.

Liao Y. K., Liao C. K., Ho Y. L. Maturation of somatic embryos in two embryogenic cultures of Picea morrisonicola Hayata as affcted by alternation of endogenous IAA content. Plant Cell Tissue Organ Cult. 2008. Vol. 93(3). P. 257–268. doi: 10.1007/s11240-008-9371-3.

Liu J., Hu X., Qin P. The WOX11-LBD16 pathway promotes pluripotency acquisition in callus cells during de novo shoot regeneration in tissue culture. Plant Cell Physiol. 2018. Vol. 59. Р. 734–743. doi: 10.1093/pcp/pcy010.

Liu J., Sheng L., Xu Y., Li J., Yang Z., Huang H., Xu L. WOX11 and 12 are involved in the first-step cell fate transition during de novo root organogenesis in Arabidopsis. Plant Cell. 2014. Vol. 26(3). P. 1081–1093. doi: 10.1105/tpc.114.122887.

Liu Z., Ge X. X., Qiu W. M., Long J. M, Jia H. H., Yang W., Dutt M., Wu X. M., Guo W. W. Overexpression of the CsFUS3 gene encoding a B3 transcription factor promotes somatic embryogenesis in Citrus. Plant Sci. 2018. Vol. 277. P. 121–131. doi: 10.1016/j.tplants.2018.10.015.

Long J. A., Moan E. I., Medford J. I., Barton M. K. A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature. 1996. Vol. 379(6560). P. 66–69. doi: 10.1038/379066a0.

Lotan Т., Ohto M., Yee K. M., West M. A., Lo R., Kwong R. W., Yamagishi K., Fischer R. L., Goldberg R. B., Harada J. J. Arabidopsis LEAFY COTYLEDON 1 is sufficient to induce embryo development in vegetative tissue. Cell. 1998. Vol. 93(7). P. 1195–1205. doi: 10.1016/s0092-8674(00)81463-4.

Lund S. T., Smith A. G., Hackett W. P. Cuttings of a tobacco mutant, rac, undergo cell divisions but do not initiate adventitious roots in response to exogenous auxin. Physiologia Plantarum. 1996. Vol. 97. P. 372–380. doi: 10.1034/j.1399-3054.1996.970223.x.

Lund S. T., Smith A. G., Hackett W. P. Differential gene expression in response to auxin treatment in the wild-type and rac, an adventitious rooting-incompetent mutant of tobacco. Plant Physiol. 1997. Vol. 114(4). P. 1197–1206. doi: 10.1104/pp.114.4.1197.

Luo K., Zheng X., Chen Y., Xiao Y., Zhao D., McAvoy R., Pei Y., Li Y. The maize Knotted1 gene is an effective positive selectable marker gene for Agrobacterium-mediated tobacco transformation. Plant Cell Rep. 2006. Vol. 25(5). P. 403–409. doi: 10.1007/s00299-005-0051-z.

Ma Y., Miotk A., Šutikovi´c Z., Ermakova O., Wenzl C., Medzihradszky A., Gaillochet C., Forner J., Utan G., Brackmann K., Galván-Ampudia C. S., Vernoux T., Greb T., Lohmann J. U. WUSCHEL acts as an auxin response rheostat to maintain apical stem cells in Arabidopsis. Nat Commun. 2019. Vol. 10(1). P. 5093. doi: 10.1038/s41467-019-13074-9.

Magnani E., Jiménez-Gómez J. M., Soubigou-Taconnat L., Lepiniec L., Fiume E. Profiling the onset of somatic embryogenesis in Arabidopsis. Bmc Genom. 2017. Vol. 18. P. 1–12. doi: 10.1186/s12864-017-4391-1.

Mayran A., Drouin J. Pioneer transcription factors shape the epigenetic landscape. J Biol Chem. 2018. Vol. 293(36). P. 13795–13804. doi: 10.1074/jbc.R117.001232.

Méndez-Hernández H. A., Ledezma-Rodríguez M., Avilez-Montalvo R. N., Juárez-Gómez Y. L., Skeete A., Avilez-Montalvo J., De-La-Peña C., Loyola-Vargas V. M. Signaling overview of plant somatic embryogenesis. Front. Plant Sci. 2019. Vol. 10. P. 77. doi: 10.3389/fpls.2019.00077.

Meng W. J., Cheng Z. J., Sang Y. L., Zhang M. M., Rong X. F., Wang Z. W., Tang Y. Y. Zhang X. S. Type-B ARABIDOPSIS RESPONSE REGULATORs specify the shoot stem cell niche by dual regulation of WUSCHEL. Plant Cell. 2017. Vol. 29(6). Р. 1357–1372. doi: 10.1105/tpc.16.00640.

Morcillo F., Gallard A., Pillot M., Jouannic S., Aberlenc-Bertossi F., Collin M., Verdeil J. L., Tregear J. W. EgAP2-1, an AINTEGUMENTA-like (AIL) gene expressed in meristematic and proliferating tissues of embryos in oil palm. Planta. 2007. Vol. 226(6). P. 1353–1362. doi: 10.1007/s00425-007-0574-3.

Mordhorst A. P., Voerman K. J., Hartog M.V., Meijer E. A., van Went J., Koornneef M., de Vries S. C. Somatic embryogenesis in Arabidopsis thaliana is facilitated by mutations in genes repressing meristematic cell divisions. Genetics. 1998. Vol. 149(2). Р. 549–563. doi: 10.1093/genetics/149.2.549.

Mursyanti E., Purwantoro A., Moeljopawiro S., Semiarti E. Induction of Somatic Embryogenesis through Overexpression of ATRKD4 Genes in Phalaenopsis “Sogo Vivien”. Indones J Biotechnol. 2015. Vol. 20(1). P. 42–53. doi: 10.22146/ijbiotech.15276

Nishimura A., Tamaoki M., Sakamoto T., Matsuoka M. Over-Expression of Tobacco knotted 1-Type Classl Homeobox Genes Alters Various Leaf Morphology. Plant Cell Physiol. 2000. Vol. 41(5). P. 583–590. doi: 10.1093/pcp/41.5.583.

Nowak K., Gaj M. D. Transcription factors in the regulation of somatic embryogenesis. In book: Somatic Embryogenesis: Fundamental Aspects and Applications; Springer International Publishing: Cham, Switzerland. 2016. P. 53–79. ISBN 9783319337050. doi:10.1007/978-3-319-33705-0_5.

Ogas J., Cheng J-C., Sung Z. R., Somerville С. Cellular differentiation regulated by gibberellin in the Arabidopsis thaliana pickle Mutant. Science. 1997. Vol. 277(5322). P. 91–94. doi: 10.1126/science.277.5322.91.

Okushima Y., Fukaki H., Onoda M., Theologis A., Tasaka M. ARF7 and ARF19 regulate lateral root formation via direct activation of BD/ASL genes in Arabidopsis. Plant Cell. 2007. Vol. 19(1). Р. 118–130. doi: 10.1105/tpc.106.047761.

Orłowska A., K˛epczy´nska E. Identification of Polycomb Repressive Complex1, Trithorax group genes and their simultaneous expression with WUSCHEL, WUSCHEL-related Homeobox5 and SHOOT MERISTEMLESS during the induction phase of somatic embryogenesis in Medicago truncatula Gaertn. Plant Cell Tissue Organ Cult. 2018. Vol. 134. P. 345–356. doi: 10.1007/s11240-018-1425-6.

Palovaara J., Hallberg H., Stasolla C., Hakman I. Comparative expression pattern analysis of WUSCHEL-related homeobox 2 (WOX2) and WOX8/9 in developing seeds and somatic embryos of the gymnosperm Picea abies. New Phytol. 2010. Vol. 188. P. 122–135. doi: 10.1111/j.1469-8137.2010.03336.x.

Pan J., Zhao F., Zhang G., Pan Y., Sun L., Bao N., Qin P., Chen L., Yu J., Zhang Y., Xu L. Control of de novo root regeneration efficiency by developmental status of Arabidopsis leaf explants. J Genet Genomics. 2019. Vol. 46(3). P. 133–40. doi: 10.1016/j.jgg.2019.03.001

Pasternak T., Dudits D. Epigenetic clues to better understanding of the asexual embryogenesis in planta and in vitro. Front Plant Sci. 2019. Vol. 10. Р. 778. doi: 10.3389/fpls.2019.00778.

Pelletier J. M., Kwong R. W., Park S., Le B. H., Baden R., Cagliaria A. Hashimoto M., Munoz M. D., Fischer R. L., Goldberg R. B., Harada J. J. L EC1 sequentially regulates the transcription of genes involved in diverse developmental processes during seed development. Proc. Natl. Acad. Sci. USA. 2017. Vol. 114(32). E6710–E6719. doi: 10.1073/pnas.1707957114.

Pérez-Pascual D., Jiménez-Guillen D., Villanueva-Alonzo H., Souza-Perera R., Godoy-Hernández G., Zúñiga-Aguilar J. J. Ectopic expression of the Coffea canephora SERK1 homolog-induced differential transcription of genes involved in auxin metabolism and in the developmental control of embryogenesis. Physiol Plant. 2018. Vol. 163(4). P. 530–551. doi: 10.1111/ppl.12709.

Perry S. E., Zheng Q., Zheng Y. Transcriptome analysis indicates that GmAGAMOUS-Like 15 may enhance somatic embryogenesis by promoting a dedifferentiated state. Plant Signal Behav. 2016. Vol. 11(7). e1197463. doi: 10.1080/15592324.2016.1197463.

Rashid S. Z., Yamaji N., Kyo M. Shoot formation from root tip region: A developmental alteration by WUS in transgenic tobacco. Plant Cell Rep. 2007. Vol. 26(9). P. 1449–1455. doi: 10.1007/s00299-007-0342-7.

Rupp H. M., Frank M., Werner T., Strnad M., Schmülling T. Increased steady state mRNA levels of the STM and KNAT1 homeobox genes in cytokinin overproducing Arabidopsis thaliana indicate a role for cytokinins in the shoot apical meristem. Plant J. 1999. Vol. 18(5). P. 557–563. doi: 10.1046/j.1365-313X.1999.00472.x.

Rupps A., Raschke J., Rümmler M., Linke B., Zoglauer K. Identification of putative homologs of Larix decidua to BABY BOOM (BBM), LEAFY COTYLEDON1 (LEC1), WUSCHEL-related HOMEOBOX2 (WOX2) and SOMATIC EMBRYOGENESIS RECEPTOR-like KINASE (SERK) during somatic embryogenesis. Planta. 2016. Vol. 243(2). P. 473–488. doi: 10.1007/s00425-015-2409-y.

Salaün C., Lepiniec L., Dubreucq B. Genetic and molecular control of somatic embryogenesis. Plants. 2021. Vol. 10(7). P. 1467. doi: 10.3390/plants10071467.

Santiago J., Henzler C., Hothorn M. Molecular mechanism for plant steroid receptor activation by somatic embryogenesis co-receptor kinases. Science. 2013. Vol. 341(6148). P. 889–892. doi: 10.1126/science.1242468.

Santos Mendoza M., Dubreucq B., Miquel M., Caboche M., Lepiniec L. LEAFY COTYLEDON 2 activation is sufficient to trigger the accumulation of oil and seed specific mRNAs in Arabidopsis leaves. FEBS Lett. 2005. Vol. 579(21). P. 4666–4670. doi: 10.1016/j.febslet.2005.07.037.

Schmidt E. D., Guzzo F., Toonen M. A., de Vries S. C. A leucine-rich repeat containing receptor-like kinase marks somatic plant cells competent to form embryos. Development. 1997. Vol. 124(10). P. 2049–2062. doi: 10.1242/dev.124.10.2049.

Schoof H., Lenhard M., Haecker A., Mayer K. F., Jürgens G., Laux T. The stem cell pop-ulation of Arabidopsis shoot meristems is maintained by a regulatury loop between the CLAVATA and WUSCHEL genes. Cell. 2000. Vol. 100(6). P. 635–644. doi: 10.1016/S0092-8674(00)80700-X.

Sengupta S., Nag Chaudhuri R. ABI3 plays a role in de-novo root regeneration from Arabidopsis thaliana callus cells. Plant Signal Behav. 2020. Vol. 15(9). P. 1794147. doi: 10.1080/15592324.2020.1794147.

Shani E., Salehin M., Zhang Y., Sanchez S. E., Doherty C., Wang R., Mangado C. C., Song L., Tal I., Pisanty O., Ecker J. R., Kay S. A., Pruneda-Paz J., Estelle M. Plant Stress Tolerance Requires Auxin-Sensitive Aux/IAA Transcriptional Repressors. Curr Biol. 2017. Vol. 27(3). P. 437–444. doi: 10.1016/j.cub.2016.12.016.

Shaul O., Montagu M. V., Inzé D. Cell cycle control in Arabidopsis. Annal Bot. 1996. Vol. 78. Р. 283–288.

Sheng L., Hu X., Du Y., Zhang G., Huang H., Scheres B., Xu L. Non-canonical WOX11-mediated root branching contributes to plasticity in Arabidopsis root system architecture. Development. 2017. Vol. 144(17). P. 3126–3133. doi: 10.1242/dev.152132.

Shin S. Y., Choi Y., Kim S.-G., Park S.-J., Moon K.-B., Kim H.-S., Jeon J.H., Cho H.S., Lee H.-J. Submergence promotes auxin-induced callus formation through ethylene-mediated post-transcriptional control of auxin receptors. Mol. Plant. 2022. Vol. 15(12). P. 1947–1961. doi: 10.1016/j.molp.2022.11.001.

Snipes S. A., Rodriguez K., DeVries A. E. Miyawaki K. N., Perales M., Xie M., Reddy G.V. Cytokinin stabilizes WUSCHEL by acting on the protein domains required for nuclear enrichment and transcription. PLOS Genet. 2018. Vol. 14(4). e1007351. doi: 10.1371/journal.pgen.1007351.

Srinivasan C., Liu Z., Heidmann I., Supena E. D., Fukuoka H., Joosen R., Lambalk J., Angenent G., Scorza R., Custers J. B., Boutilier K. Heterologous expression of the BABY BOOM AP2/ERF transcription factor enhances the regeneration capacity of tobacco (Nicotiana tabacum L.). Planta. 2007. Vol. 225(2). P. 341–351. doi: 10.1007/s00425-006-0358-1.

Stone S. L., Kwong L. W., Yee K. M., Pelletier J., Lepiniec L., Fischer R. L., Goldberg R. B., Harada J. J. LEAFY COTYLEDON2 encodes a B3 domain transcription factor that induces embryo development. Proc. Natl. Acad. Sci. USA. 2001. Vol. 98(20). P. 11806–11811. doi: 10.1073/pnas.201413498.

Sugiyama M. Genetic analysis of plant morphogenesis in vitro. International Review of Cytology. 2000. Vol. 196. Р. 67–84. doi: 10.1016/S0074-7696(00)96002-9.

Tao Z., Hu H., Luo X., Jia B., Du J., He Y. Embryonic resetting of the parental vernalized state by two B3 domain transcription factors in Arabidopsis. Nat Plants. 2019. Vol. 5(4). P. 424–435. doi: 10.1038/s41477-019-0402-3.

Teale W. D., Paponov I. A., Palme K. Auxin in action: Signalling, transport and the control of plant growth and development. Nat Rev Mol Cell Biol. 2006. Vol. 7(11). P. 847–859. doi: 10.1038/nrm2020.

Thakare D., Tang W., Hill K., Perry S. E. The MADS-domain transcriptional regulator AGAMOUS-LIKE15 promotes somatic embryo development in Arabidopsis and soybean. Plant Physiol. 2008. Vol. 146(4). P. 1663–1672. doi: 10.1104/pp.108.115832.

Tian R., Paul P., Joshi S., Perry S. Genetic activity during early plant embryogenesis. Biochemical Journal. 2020. Vol. 477. Р. 3743–3767. doi: 10.1042/BCJ20190161.

Tsuwamoto R., Yokoi S., Takahata Y. Arabidopsis EMBRYOMAKER encoding an AP2 domain transcription factor plays a key role in developmental change from vegetative to embryonic phase. Plant Mol Biol. 2010. Vol. 73(4). P. 481–492. doi: 10.1007/s11103-010-9634-3.

Twaij B. M., Jazar Z. H., Hasan M. N. Trends in the Use of Tissue Culture, Applications and Future Aspects. Int. J Plant Biol. 2020. Vol. 11(1). P. 8385. doi: 10.4081/pb.2020.8385.

Uddenberg D., Abrahamsson M., von Arnold S. Overexpression of PaHAP3A stimulates differentiation of ectopic embryos from maturing somatic embryos of Norway spruce. Tree Genet Genomes. 2016. Vol. 12. P. 18. doi: 10.1007/s11295-016-0974-2.

Waki T., Kiki T., Watanabe R., Hashimoto T., Nakajima K. The Arabidopsis RWP-RK Protein RKD4 Triggers Gene Expression and Pattern Formation in Early Embryogenesis. Curr Biol. 2011. Vol. 21(15). P. 1277–1281. doi: 10.1016/j.cub.2011.07.001.

Wan Q., Zhai N., Xie D., Liu W., Xu L. WOX11: The founder of plant organ regeneration. Cell Regen. 2023. Vol. 12(1). P. 1. doi: 10.1186/s13619-022-00140-9.

Wang B., Chu J., Yu T., Xu Q., Sun X., Yuan J., Xiong G., Wang G., Wang Y., Li J. Tryptophan-independent auxin biosynthesis contributes to early embryogenesis in Arabidopsis. Proc. Natl. Acad. Sci. USA. 2015. Vol. 112(15). P. 4821–4826. doi: 10.1073/pnas.1503998112.

Wang F.-X., Shang G.-D., Wu L.-Y., Xu Z.-G., Zhao X.-Y., Wang J.-W. Chromatin accessibility dynamics and a hierarchical transcriptional regulatory network structure for plant somatic embryogenesis. Dev Cell. 2020. Vol. 54. P. 742–757. doi: 10.1016/j.devcel.2020.07.003.

Wang X., Niu Q.-W., Teng C., Li C., Mu J., Chua N.-H., Zuo J. Overexpression of PGA37/MYB118 and MYB115 promotes vegetative-to-embryonic transition in Arabidopsis. Cell Res. 2009. Vol. 19(2). P. 224–235. doi: 10.1038/cr.2008.276.

White D., Woodfield D., Caradus J. Mortal: A Mutant of White Clover Defective in Nodal Root Development. Plant Physiol. 1998. Vol. 116(3). P. 913–921. doi: 10.1104/pp.116.3.913.

Wickramasuriya A. M., Dunwell J. M. Global scale transcriptome analysis of Arabidopsis embryogenesis in vitro. Bmc Genom. 2015 Vol. 16(1). P. 301. doi: 10.1186/s12864-015-1504-6.

Winkelmann T. Somatic versus zygotic embryogenesis: Learning from seeds. Methods Mol Biol. 2016. Vol. 1359. P. 25–46. doi: 10.1007/978-1-4939-3061-6_2.

Wójcik A. M., Gaj M. D. miR393 contributes to the embryogenic transition induced in vitro in Arabidopsis via the modification of the tissue sensitivity to auxin treatment. Planta. 2016. Vol. 244(1. P. 231–243. doi: 10.1007/s00425-016-2505-7

Wójcik A. M., Nodine M. D., Gaj M. D. miR160 and miR166/165 contribute to the LEC2-mediated auxin response involved in the somatic embryogenesis induction in Arabidopsis. Front Plant Sci. 2017. Vol. 8. P. 2024. doi: 10.3389/fpls.2017.02024.

Wójcik A. M., Wójcikowska B., Gaj M. D. Current perspectives on the auxin-mediated genetic network that controls the induction of somatic embryogenesis in plants. Int J Mol Sci. 2020. Vol. 21. P. 1333. doi: 10.3390/ijms21041333.

Wójcikowska B., Gaj M. D. Expression profiling of AUXIN RESPONSE FACTOR genes during somatic embryogenesis induction in Arabidopsis. Plant Cell Rep. 2017. Vol. 36(6). P. 843–858. doi: 10.1007/s00299-017-2114-3.

Wójcikowska B., Wójcik A. M., Gaj M. D. Epigenetic regulation of auxin-induced somatic embryogenesis in plants. Int. J. Mol. Sci. 2020. Vol. 21(7). Р. 2307. doi: 10.3390/ijms21072307.

Wu L-Y., Shang G-D., Wang F-X., Gao J., Wan M-C., Xu Z-G., Wang J-W. Dynamic chromatin state profiling reveals regulatory roles of auxin and cytokinin in shoot regeneration. Dev Cell. 2022. Vol. 57(4). P. 526–542. doi: 10. 1016/j.devcel.2021.12.019.

Yang Z., Li C., Wang Y., Zhang C., Wu Z., Zhang X., Liu C., Li F. GhAGL15s, preferentially expressed during somatic embryogenesis, promote embryogenic callus formation in cotton (Gossypium hirsutum L.). Mol Genet Genomics. 2014. Vol. 289(5). P. 873–883. doi: 10.1007/s00438-014-0856-y.

Yu J., Liu W., Liu J., Qin P., Xu L. Auxin control of root organogenesis from callus in tissue culture. Front Plant Sci. 2017 Vol 8. Р. 1–4. doi: 10.3389/fpls.2017.01385.

Zhang S., Williams-Carrier R., Jackson D., Lemaux P. G. Expression of CDC2Zm and KNOTTED1 during in vitro axillary shoot meristem proliferation and adventitious shoot meristem formation in maize (Zea mays L.) and barley (Hordeum vulgare L.). Planta. 1998. Vol. 204(4). P. 542–549. doi: 10.1007/s004250050289.

Zhang Z., Tucker E., Hermann M., Laux T. A molecular framework for the embryonic initiation of shoot meristem stem cells. Dev Cell. 2017. Vol. 40(3). P. 264–277. doi: 10.1016/j.devcel.2017.01.002.

Zheng Q., Zheng Y., Ji H., Burnie W., Perry S. E. Gene regulation by the AGL15 transcription factor reveals hormone interactions in somatic embryogenesis. Plant Physiol. 2016. Vol. 172(4). P. 2374–2387. doi: 10.1104/pp.16.00564

Zheng W., Zhang X., Yang Z., Wu J., Li F., Duan L., Liu C., Lu L., Zhang C., Li F. AtWUSCHEL promotes formation of the embryogenic callus in Gossypium hirsutum. PLoS ONE. Vol. 2014, Vol. 9(1). e87502. doi: 10.1371/journal.pone.0087502

Zheng Y., Ren N., Wang H., Stromberg A. J., Perry S. E. Global identification of targets of the Arabidopsis MADS domain protein AGAMOUS-like15. Plant Cell. 2009. Vol. 21(9). P. 2563–2577. doi: 10.1105/tpc.109.068890.

Zhu S.-P., Wang J., Ye J.-L., Zhu A.-D., Guo W.-W., Deng X.-X. Isolation and characterization of LEAFY COTYLEDON 1-LIKE gene related to embryogenic competence in Citrus sinensis. Plant Cell Tiss Organ Cult. 2014. Vol. 119(1). P. 1–13. doi: 10.1007/s11240-014-0509-1.

Zuo J., Niu Q. W., Frugis G., Chua N. H. The WUSCHEL gene promotes vegetative-to-embryonic transition in Arabidopsis. Plant J. 2002. Vol. 30(3). P. 349–359. doi: 10.1046/j.1365-313X.2002.01289.x