Genetic control of regeneration processes of radish plants in vitro: from phenotype to genotype
DOI:
https://doi.org/10.21638/spbu03.2019.204Abstract
This review highlights the years of research on the genetics of in vitro regeneration in higher plants conducted at the Department of Genetics and Biotechnology of Saint Petersburg State University. The genetic collection of radish (Raphanus sativus) created at the department by selfing of individual plants from three cultivars was used as a model in these studies. Some radish inbred lines from the genetic collection form spontaneous tumors in the roots and are also used to study mechanisms of tumor growth in higher plants. It was revealed that radish lines that differed in the ability to form tumors also contrastingly differed in the reaction of their explants to auxin and cytokinin in vitro, which reflects a difference in the levels of these hormones in the tissues of related tumorous and non-tumorous radish lines. Moreover, high concentrations of cytokinins in cultural medium induced tumor formation in the regenerated plants of tumorous radish lines. The presence of meristematic zones in spontaneous tumors in radish lines, as well as in crown gall tumors induced by Agrobacterium tumefaciens and cytokinin-induced tumors made it possible to reveal the role of the main meristem regulators, such as KNOX and WOX family transcription factors and the CLAVATA system, in both the process of tumor growth and regeneration in plants. Analysis of the expression of meristem-specific genes during the development of spontaneous and induced tumors in radish as well as in regenerated radish plants confirmed this assumption.
Keywords:
Raphanus sativus, regeneration, tumors, meristems, phytohormones
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References
Ahuja, M. R. 1998. Genetic tumors in Nicotiana and other plants. Quarterly Review of Biology 73:439–459. https://doi.org/10.1086/420413
Atta, R., Laurens, L., Boucheron-Dubuisson, E., Guivarc'h, A., Carnero, E., Giraudat-Pautot, V., Rech, P., and Chriqui, D. 2009. Pluripotency of Arabidopsis xylem pericycle underlies shoot regeneration from root and hypocotyl explants grown in vitro. Plant Journal 57(4):626–644. https://doi.org/10.1111/j.1365-313X.2008.03715
Azarakhsh, M., Kirienko, A. N., Zhukov, V. A., Lebedeva, M. A., Dolgikh, E. A., and Lutova, L. A. 2015. KNOTTED1-LIKE HOMEOBOX 3: a new regulator of symbiotic nodule development. Journal of Experimental Botany 66(22):7181–7195. https://doi.org/10.1093/jxb/erv414
Azmi, A., Dewitte, W., Van Onckelen, H., and Chriqui, D. 2001. In situ localization of endogenous cytokinins during shooty tumor development in Eucalyptus globulus Labill. Planta 213(1):29–36. https://doi.org/10.1007/s004250000476
Bolduc, N. and Hake, S. 2009. The maize transcription factor KNOTTED1 directly regulates the gibberellin catabolism gene ga2ox1. Plant Cell 21(6):1647–1658. https://doi.org/10.1105/tpc.109.068221
Buzovkina, I. S., Kneshke, I., and Lutova, L. A. 1993a. Genetic analysis of the trait "cytokinin sensitivity" in radish in vitro. Genetika 29(6):995–1001.
Buzovkina, I. S., Kneshke, I., and Lutova, L. A. 1993b. In vitro modeling of tumor formation in radish lines and hybrids. Genetika 29(6):1002–1008.
Buzovkina, I. S. and Lutova, L. A. 2007. Genetic collection of radish inbred lines: history and perspectives. Russian Journal of Genetics 43(10):1411–1423. https://doi.org/10.1134/S1022795407100134
Dodueva, I. E., Frolova, N. V., and Lutova, L. A. 2007. Plant tumorigenesis: different ways for shifting systemic control of plant cell division and differentiation. Transgenic Plant Journal 1:17–38.
Dodueva, I. E., Ilyina, E. L., Arkhipova, T. N., Frolova, N. V., Monakhova, V. A., Kudoyarova, G. R., and Lutova, L. A. 2008. Influence of Agrobacterium tumefaciens ipt and Agrobacterium rhizogenes rolC genes on spontaneous tumor formation and endogenous cytokinins content in radish (Raphanus sativus) inbred lines. Transgenic Plant Journal 2:45–53.
Dodueva, I. E. and Lutova, L. A. 2011. Tumors of higher plants: the problem of systemic control of cell proliferation. Lambert Academic Publishing.
Dodueva, I. E., Kiryushkin, A. S., Osipova, M. A., Yurlova, E. V., Buzovkina, I. S., and Lutova L. A. 2013. Effect of cytokinins on the expression of radish CLE radish. Russian Journal of Plant Physiology 60(3):388–395. https://doi.org/10.1134/S1021443713020052
Dodueva, I. E., Gancheva, M. S., Osipova, M. A., Tvorogova, V. E., and Lutova, L. A. 2014. Lateral meristems of higher plants: Phytohormonal and genetic control. Russian Journal of Plant Physiology 61(5):571–589. https://doi.org/10.1134/S1021443714050069
Dodueva, I. E., Tvorogova, V. E., Azarakhsh, M., and Lutova, L. A. 2017. Plant stem cells: unity and diversity. Russian Journal of Genetics: Applied Research 7(4):385–403. https://doi.org/10.1134/S2079059717040025
Dolzblasz, A., Nardmann, J., Clerici, E., Causier, B., van der Graaff, E., Chen, J., Davies, B., Werr, W., and Laux, T. 2016. Stem cell regulation by Arabidopsis WOX genes. Molecular Plant 9(7):1028–1039. https://doi.org/10.1016/j.molp.2016.04.007
Doonan, J. and Hunt, T. 1996. Cell cycle. Why don’t plants get cancer? Nature 380(6574):481–482. https://doi.org/10.1038/380481a0
Fadeeva, T. S., Narbut, S. I., and Lutova, L. A. 1975. Regeneration and callus formation in plants as a genetic trait. III. Variability on the basis of root and callus formation in isolated radish cotyledons and morphological features of plants. Research on Genetics 6:135–145.
Fadeeva, T. S., Kozyreva, O. G., and Lutova, L. A. 1979. Regeneration in plants as a genetic trait. Research on Genetics 8:160–170.
Frank M., Guiv’Arch, A., Krupkova, E., Lorenz-Meyer, I., Chriqui, D., and Schmulling, T. 2002. TUMOROUS SHOOT DEVELOPMENT (TSD) genes are required for co-ordinated plant shoot development. Plant Journal 29(1):73–85. https://doi.org/10.1046/j.1365-313x.2002.01197.x
Frolova, N. V., Matveeva, T. V., and Lutova, L. A. 2004. Using the method of agrobacterial transformation in vivo to obtain phenocopies of tumor formation in a non-tumor line of radish (Raphanus sativus L.). Biotechnologia 4:3–7.
Gancheva, M. S., Dodueva, I. E., Lebedeva, M. A., Tvorogova, V. E., Tkachenko, A. A., and Lutova, L. A. 2016. Identification, expression, and functional analysis of CLE genes in radish (Raphanus sativus L.) storage root. BMC Plant Biology 16(Suppl 1):7. https://doi.org/10.1186/s12870-015-0687-y
Gancheva, M. S., Dodueva, I. E., and Lutova, L. A. 2018. Role of CLE41 peptide in the development of root storage parenchyma in the species of genus Raphanus. Russian Journal of Plant Physiology 65(4):279–293. https://doi.org/10.1134/S1021443718030032
Ilina, E. L., Dodueva, I. E., Ivanova, N. M., and Lutova, L. A. 2006. The effect of cytokinins on in vitro cultured inbred lines of Raphanus sativus var. radicula Pers. with genetically determined tumorigenesis. Russian Journal of Plant Physiology 53(4):514–522. https://doi.org/10.1134/S1021443706040133
Intrieri, M. C. and Buiatti, M. 2001. The horizontal transfer of Agrobacterium rhizogenes genes and the evolution of the genus Nicotiana. Molecular Phylogenetics and Evolution 20(1):100–110. https://doi.org/10.1006/mpev.2001.0927
Ito, Y., Nakanomyo, I., Motose, H., Iwamoto, K., Sawa, S., Dohmae, N., and Fukuda, H. 2006. Dodeca-CLE peptides as suppressors of plant stem cell differentiation. Science 313(5788):842–845. https://doi.org/10.1126/science.1128436
Jasinski, S., Piazza, P., Craft, J., Hay, A., Woolley, L., Rieu, I., Phillips A., Hedden, P., and Tsiantis, M. 2005. KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities. Current Biology 15(17):1560–1565. https://doi.org/10.1016/j.cub.2005.07.023
Kiyohara, S. and Sawa, S. 2012. CLE signaling systems during plant development and nematode infection. Plant Cell Physiology 53(12):1989–1999. https://doi.org/10.1093/pcp/pcs136
Krupková, E., Immerzeel, P., Pauly, M., and Schmülling, T. 2007. The TUMOROUS SHOOT DEVELOPMENT2 gene of Arabidopsis encoding a putative methyltransferase is required for cell adhesion and coordinated plant development. Plant Journal 50(4):735–750. https://doi.org/10.1111/j.1365-313X.2007.03123.x
Kuznetsova, X. A., Dodueva, I. E., Gancheva, M. S., and Lutova, L. A. 2018. Role of CLE peptides in storage root formation among plants of Raphanus, Beta and Brassica species. Materials of International PhD School of Plant Development, Zellingen-Retzbach, Germany.
Laux, T., Mayer, K. F., Berger, J., and Jurgens, G. 1996. The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122(1):87–96.
Lebedeva, M. A., Tvorogova, V. E., Vinogradova, A. P., Gancheva, M. A., Azarakhsh, M., Ilina, E. L., Demchenko, K. N., Dodueva, I. E., and Lutova, L. A. 2015. Initiation of spontaneous tumors in radish (Raphanus sativus): Cellular, molecular and physiological events. Journal of Plant Physiology 173:97–104. https://doi.org/10.1016/j.jplph.2014.07.030
Leibfried, A., To, J. P., Busch, W., Stehling, S., Kehle, A., Demar, M., Kieber, J. J., and Lohmann, J. U. 2005. WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators. Nature 438(7071):1172–1175. https://doi.org/10.1038/nature04270
Liebsch, D., Sunaryo, W., Holmlund, M., Norberg, M., Zhang, J., Hall, H.C., Helizon, H., Jin, X., Helariutta, Y., Nilsson, O., Polle, A., and Fischer, U. 2014. Class I KNOX transcription factors promote differentiation of cambial derivatives into xylem fibers in the Arabidopsis hypocotyl. Development 141(22):4311–4319. https://doi.org/10.1242/dev.111369
Lutova, L. A., Buzovkina, I. S., and Shishkova, S. O. 1988. The relationship between tumor formation and in vitro differentiation type of radish inbred lines. Cruciferae Newsletters 13:97.
Lutova, L. A., Bondarenko, L. V., Buzovkina, I. S., Levashina, E. A., Tikhodeyev, O. N., Khodzhayova, L. T., Sharova, N. V., and Shishkova, S. O. 1994. Effect of plant genotype on regeneration processes. Genetika 30(1):1065–1074.
Lutova, L. A., Buzovkina, I. S., Smirnova, O. A., Tikhodeev, O. N., Shishkova, S. O., and Trifonova, I. M. 1997. Genetic control of in vitro differentiation processes in radish. In vitro Cellular and Developmental Biology 33(4):269–274. https://doi.org/10.1007/s11627-997-0048-0
Lutova, L. A., Dolgikh, E. A., Dodueva, I. E., Osipova, M. A., Ilina, E. L. 2008. Investigation of systemic control of plant cell division and differentiation in the model of tumor growth in radish. Russian Journal of Genetics 44(8):936–943. https://doi.org/10.1134/S1022795408080073
Lutova, L. A., Dodueva, I. E., Lebedeva, M. A., and Tvorogova, V. E. 2015. Transcription factors in developmental genetics and the evolution of higher plants. Russian Journal of Genetics 51(5):449–466. https://doi.org/10.1134/S1022795415030084
Malovichko, Y., Tkachenko, A., Dodueva, I., and Lutova, L. 2017. Localization of CLE peptide receptors in radish (Raphanus sativus L.). Materials of the 5th European Workshop on Peptide Signaling in Plants, Copenhagen, Denmark.
Matveeva, T. V., Dodueva, I. E., Wood, D., Lutova, L. A., and Nester, Y. 2000. Studying the role of phytohormones in the tumor formation process in radish. Genetika 36(2):203–208.
Matveeva, T. V., Frolova, N. V., Smets, R., Dodueva, I. E., Buzovkina, I. S., Van Onckelen, H., and Lutova, L. A. 2004. Hormonal control of tumor formation in radish. Journal of Plant Growth Regulation 23(1):37–43. https://doi.org/10.1007/s00344-004-0004-8
Narbut, S. I. 1966. Genetic collection of inbred lines of radish. Genetika 5:89–100.
Narbut, S. I. 1967. Genetic tumor obtained by inbreeding in radish. Vestnik Leningradskogo Universiteta 15:144–149.
Narbut, S. I., Voilokov, A. V., Rakhman, M. I., and Maksimenko, O. E. 1995. Biometric analysis of the frequency of spontaneous tumor formation in the inbred lines of radish. Genetika 31:1268–1271.
Osipova, M. A., Mortier, V., Demchenko, K. N., Tsyganov, V. E., Tikhonovich, I. A., Lutova, L. A., Dolgikh, E. A., and Goormachtig, S. 2012. WUSCHEL-RELATED HOMEOBOX5 gene expression and interaction of CLE peptides with components of the systemic control add two pieces to the puzzle of autoregulation of nodulation. Plant Physiology 158(3):1329–1341. https://doi.org/10.1104/pp.111.188078
Paponova, S. S., Chetverikov, P. E., Pautov, A. A., Yakovleva, O. V., Zukoff, S., Vishnyakov, A. E., Sukhareva, S. I., Krylova, E. G., Dodueva, I. E., and Lutova, L. A. 2017. Gall mite Fragariocoptes setiger (Eriophyoidea) changes leaf developmental program and regulates gene expression in the leaf tissues of Fragaria viridis (Rosaceae). Annals of applied biology 172(1):33–46. https://doi.org/10.1111/aab.12399
Perez-Garcia, P. and Moreno-Risueno, M. A. 2018. Stem cells and plant regeneration. Developmental Biology 442(1):3–12. https://doi.org/10.1016/j.ydbio.2018.06.021
Qu, G., Heo, S., Yoon, B.-S., and Wang, M. H. 2006. The effects of exogenous hormones on genetic tumor formation in Nicotiana hybrids. EXCLI Journal 5:33–41.
Reiser, L., Sanchez-Baracaldo, P., and Hake, S. 2000. Knots in the family tree: evolutional relationship and functions of KNOX homeobox genes. Plant Molecular Biology 42(1):151–166. https://doi.org/10.1023/A:1006384122567
Samorodova, A. P., Tvorogova, V. E., Tkachenko, A. A., Potsenkovskaya, E. A., Lebedeva, М. А., Tikhonovich, I. A., and Lutova, L. А. 2018. Agrobacterial tumors interfere with nodulation and demonstrate the expression of nodulation-induced CLE genes in pea. Journal of Plant Physiology 221:94–100. https://doi.org/10.1016/j.jplph.2017.12.005
Sugimoto, K., Jiao, Y., and Meyerowitz, E. M. 2010. Arabidopsis regeneration from multiple tissues occurs via a root development pathway. Developmental Cell 18(3):463–471. https://doi.org/10.1016/j.devcel.2010.02.004
Tkachenko, A., Predeus, A., Dodueva, I., and Lutova, L. 2016. RNA-Seq analysis of radish (Raphanus sativus L.) agrobacterial tumours. Materials of 22nd International Conference on Plant Growth Substances, Toronto, Canada.
Tsuda, K. and Hake, S. 2015. Diverse functions of KNOX transcription factors in the diploid body plan of plants. Current Opinion in Plant Biology 27:91–96. https://doi.org/10.1016/j.pbi.2015.06.015
Tvorogova, V. E., Osipova, M. A., Dodueva, I. E., and Lutova, L. A. 2013. Interaction of transcription factors and phytohormones in the regulation of plant meristem activity. Russian Journal of Genetics: Applied Research 3(5):325–337. https://doi.org/10.1134/S2079059713050110
Tvorogova, V. E., Kurmazov, N. S., Potsenkovskaya, E. A., and Lutova, L. A. 2018a. MtWOX9-1 gene in the somatic embryogenesis in Medicago truncatula. Materials of the International conference “Advances in plant reproduction — from gametes to seeds”, Florence, Italy.
Tvorogova, V. E., Potsenkovskaya, E. A., and Lutova, L. A. 2018b. NF-Y genes in Medicago truncatula somatic embryogenesis. Materials of the International conference “Advances in plant reproduction — from gametes to seeds”, Florence, Italy.
Whitford, R., Fernandez, A., De Groodt, R., Ortega, E., and Hilson P. 2008. Plant CLE peptides from two distinct functional classes synergistically induce division of vascular cells. Proceedings of the National Academy of Sciences of the USA 105(47):18625–18630. https://doi.org/10.1073/pnas.0809395105
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Published
2019-08-27
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Lutova, L., & Dodueva, I. (2019). Genetic control of regeneration processes of radish plants <em>in vitro</em>: from phenotype to genotype. Biological Communications, 64(2), 124–132. https://doi.org/10.21638/spbu03.2019.204
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