Targeted Protection of Mitochondria of Mesophyll Cells in Transgenic CYP11A1 CDNA Expressing Tobacco Plant Leaves After NaCl-Induced Stress Damage

Acosta-Motos, J. R., Ortuńo, M. F., Bernal-Vicente, A., Diaz-Vivancos, P., Sanchez-Blanco, M. J., Hernandez, J. A. (2017). Plant responses to salt stress: Adaptive mechanisms. Agronomy, 7 (1), 18.10.3390/agronomy7010018Search in Google Scholar

Baranova, E. N., Christov, N. K., Kurenina, L. V., Khaliluev, M. R., Todorovska, E. G., Smirnova, E. A. (2016). Formation of atypical tubulin structures in plant cells as a nonspecific response to abiotic stress. Bulg. J. Agric. Sci., 22 (6), 987–992.Search in Google Scholar

Baranova, E. N., Gulevich, A. A., Maisuryan, A. N., Lavrova, N. V. (2011). Ultrastructure of the cells of tomato transgenic plants with gene FeSOD after salinization of nutrient medium. [Баранова, E. H., Гулевич, А. А., Майсурян, A. H., Лаврова, H. В. Ультраструктурная организация клеток трансгенных растений томата с геном Fe-SOD при засолении питательной среды]. Izv. Timiryazevsk. Skh. Akad. [Известия Тимирязевской сельскохозяйственной академии], No. 1, 90-96 (in Russian).Search in Google Scholar

Baranova, E. N., Kurenina, L. V., Smirnov, A. N., Beloshapkina, O. O., Gulevich, A. A. (2017). Formation of the hypersensitivity response due to the expression of FeSODl gene in tomato when it is inoculated with Phytophthora infestans. [Баранова, E. H., Куренина, Л. В., Смирнов, A. H., Белошапкина, О. О., Гулевич, А. А. Формирование реакции сверхчувствительности в результате экспрессии гена FeSODl у томата при инфицировании Phytophthora infestans.] Russian Agricultural Sciences [Российская сельскохозяйственная наука]. 43 (1), 15-21 (in Russian).Search in Google Scholar

Baranova, E. N., Nodel’man, E. K., Kurenina, L. V., Gulevich, A. A., Baranova, G. B., Bogoutdinova, L. R., Khaliluev, M. R. (2014). Ultrastructural organization of chloroplasts and mitochondria of transgenic tomato plants expressing the FeSOD1 gene from Arabidopsis thaliana (L.) Heynh. under salt stress. Russian Agric. Sci., 40 (6), 426–431.Search in Google Scholar

Corpas, F. J., Barroso, J. B., Sandalio, L. M., Palma, J. M., Lupiáñez, J. A., del Río, L.A. (1999). Peroxisomal NADP-dependent isocitrate dehydrogenase. Characterization and activity regulation during natural senescence. Plant Physiol., 121 (3), 921–928.Search in Google Scholar

Foyer, C. H., Noctor, G. (2000). Oxygen processing in photosynthesis: Regulation and signalling. New Phytol., 146, 359–388.10.1046/j.1469-8137.2000.00667.xSearch in Google Scholar

Gerszberg, A., Hnatuszko-Konka, K. (2017). Tomato tolerance to abiotic stress: A review of most often engineered target sequences. Plant Growth Regul., 17, 1–24.10.1007/s10725-017-0251-xSearch in Google Scholar

Hammani, K., Giegé, P. (2014). RNA metabolism in plant mitochondria. Trends Plant Sci., 19 (6), 380–389.10.1016/j.tplants.2013.12.00824462302Search in Google Scholar

Huang, A. H. C. (Ed.). Plant Peroxisomes. Elsevier, 2012.Search in Google Scholar

Kartel, N. A. Shpakovski, G. V., Spivak, S. G., Brichkova, G. G., Yarmolinsky, D. G., Berdichevets, I. N., Maneshina, T. V. (2004). Recombinant plasmid pGBP450f to obtain transgenic plants and a method of producing transgenic plants with improved productivity and resistance to fungal phytopathogens. [Картель, H. А., Шпаковский, Г. В., Спивак, С. Г., Бричкова, Г. Г., Ярмолинский, Д. Г., Бердичевец, И. Н., Манешина, Т. В. Рекомбинантная плазмида pGBP450f для получения трансгенных растений и способ получения трансгенных растений табака с повышенной продуктивностью и устойчивостью к грибным фитопатогенам]. Patent of the Russian Federation No. 2237717 [Патент Российской Федерации № 2237717]. Priority from 20.12.2002. Issued 10.10.2004. Bulletin of Inventions, No. 10.Search in Google Scholar

Kartel, N. A. Spivak, S. G., Shpakovski, G. V., Maneshina, T. V., Brichkova, G. G., Yarmolinsky, D. G., Berdichevets, I. N. (2007). Genetic engineering construction expressing cDNA of CYP11A1 gene of animal origin in plants, and a method for producing transgenic plants with increased yield and resistance to phytopathogens. [Генно-инженерная конструкция, экспрессирующая кДНК гена CYP11A1 животного происхождения в растениях, и метод получения трансгенных растений с повышенной урожайностью и устойчивостью к фитопатогенам]. Patent of the Republic of Belarus No. 9201. [Патент Республики Беларусь № 9201]. Priority from 30.12.2002. Issued 25.01.2007.Search in Google Scholar

Koyro, H. W. (1997). Ultrastructural and physiological changes in root cells of Sorghum plants (Sorghum bicolor × S. sudanensis cv. Sweet Sioux) induced by NaCl. J. Exper. Bot., 48 (3), 693–706.Search in Google Scholar

Lee, J., Kim, D. H., Hwang, I. (2014). Specific targeting of proteins to outer envelope membranes of endosymbiotic organelles, chloroplasts, and mitochondria. Frontiers Plant Sci., 5, 111–116.10.3389/fpls.2014.00173401079524808904Search in Google Scholar

Lindemann, P. (2015). Steroidogenesis in plants – Biosynthesis and conversions of progesterone and other pregnane derivatives. Steroids, 103, 145–152.10.1016/j.steroids.2015.08.00726282543Search in Google Scholar

Luzikov, V. N., Novikova, L. A., Spiridonova, V. A., Isaeva, L. V., Whelan, J., Hugosson M., Glazer E. (1994). Design of heterologous mitochondria: Import of cattle cytochrome P-450scc precursor into plant mitochondria. Biochemistry (Moscow), 59 (7), 1098–1101.Search in Google Scholar

Mittova, V., Guy, M., Tal, M., Volokita, M. (2004). Salinity up-regulates the antioxidative system in root mitochondria and peroxisomes of the wild salt-tolerant tomato species Lycopersicon pennellii. J. Exper. Bot., 55 (399), 1105–1113.10.1093/jxb/erh11315047761Search in Google Scholar

Møller, I. M. (2001). Plant mitochondria and oxidative stress: Electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu. Rev. Plant Physiol. Plant Mol. Biol., 52, 561–591.10.1146/annurev.arplant.52.1.56111337409Search in Google Scholar

Murashige, T., Skoog, F. A. (1962). Revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol. Plant., 15 (3), 473–497.10.1111/j.1399-3054.1962.tb08052.xSearch in Google Scholar

Pauli, G. F., Friesen, J. B., Gödecke, T., Farnsworth, N. R., Glodny, B. (2010). Occurrence of progesterone and related animal steroids in two higher plants. J. Nat. Prod., 73 (3), 338–345.10.1021/np900741520108949Search in Google Scholar

Perry, A. J., Hulett, J. M., Likić V. A., Lithgow T., Gooley P. R. (2006). Convergent evolution of receptors for protein import into mitochondria. Curr. Biol., 16 (3), 221–229.10.1016/j.cub.2005.12.03416461275Search in Google Scholar

Poljakoff-Mayber, A. (1975). Morphological and anatomical changes in plants as a response to salt stress. In: Poljakoff-Mayber, A., Gale, J. (eds.). Plants in Saline Environments. Springer-Verlag, Berlin, pp. 97–117.Search in Google Scholar

Rahman, S., Matsumuro, T., Miyake H., Takeoka Y. (2000). Salinity-induced ultrastructural alterations in leaf cells of rice (Oryza sativa L.). Plant Prod. Sci., 3 (4), 422–429.10.1626/pps.3.422Search in Google Scholar

Rejeb, I. B., Pastor V., Mauch-Mani B. (2014). Plant responses to simultaneous biotic and abiotic stress: Molecular mechanisms. Plants, 3 (4), 458–475.10.3390/plants3040458484428527135514Search in Google Scholar

del Rio, L. A., Corpas, F. J., Sandalio, L. M., Palma, J. M., Gomez, M., Barroso, J. B. (2002). Reactive oxygen species, antioxidant systems and nitric oxide in peroxisomes. J. Exper. Bot., 53, 1255–1272.10.1093/jxb/53.372.1255Search in Google Scholar

Saxena, B., Shukla, K., Giri, B. (2017). Arbuscular mycorrhizal fungi and tolerance of salt stress in plants. In: Wu, Qiang-Sheng (Ed.). Arbuscular Mycorrhizas and Stress Tolerance of Plants. Springer, Singapore, pp. 67–97.10.1007/978-981-10-4115-0_4Search in Google Scholar

Serenko, E. K., Baranova, E. N., Balakhnina, T. I., Kurenina, L. V., Gulevich, A. A., Kosobruhov, A. A., Polyakov, V. Y. (2011). Structural organization of chloroplast of tomato plants Solanum lycopersicum transformed by Fe-containing superoxide dismutase. Biochemistry (Moscow). Supplemental Series A: Membrane and Cell Biology, 5 (2), 177–184.10.1134/S1990747811020073Search in Google Scholar

Shematorova, E. K., Slovokhotov, I. Yu., Baranova, E. N., Khaliluev, M. R., Babak, O. G., Klykov, V. N., Shpakovski, D. G., Spivak, S. G., Shpakovski, G. V. The role of organelles in the functioning of steroid hormonal systems in animals and higher plants. [Шематорова, E. K., Словохотов, И. Ю., Баранова, E. Н., Халилуев, М. Р., Бабак, О. Г., Клыков, В. Н., Шпаковский, Д. Г., Спивак, С. Г., Шпаковский, Г. В. Роль органелл в функционировании стероидных гормональных систем у животных и высших растений]. Proceedings of the International Conference “Mechanisms of regulation of eukaryotic cell organelles functions” [Механизмы регуляции функций органелл эукариотической клетки], Irkutsk, 22-24 May 2018), pp. 155-157 (in Russian).10.31255/978-5-94797-318-1-155-157Search in Google Scholar

Shematorova, E. K., Slovokhotov, I. Y., Khaliluev, M. R., Berdichevets, I. N., Baranova, E. N., Babak, O. G., Shpakovski, D. G., Spivak, S. G., Shpakovski, G. V. (2014). Mitochondria as a possible place for initial stages of steroid biosynthesis in plants. [Шематорова, E. К., Словохотов, И. Ю., Халилуев, М. Р., Бердичевец, И. Н., Баранова, E. Н., Бабак, О. Г., Шпаковский, Д. Г., Спивак, С. Г., Шпаковский, Г.В. Митохондрии как возможное место инициации синтеза стероидных гормонов в растениях]. J. Stress Physiol. Biochem. [Журнал стресс-физиологии и биохимии], 10 (4), 85-97 (in Russian).Search in Google Scholar

Shpakovski, G. V., Spivak, S. G., Berdichevets, I. N., Babak, O. G., Kubrak, S. V., Kilchevsky, A. V., Aralov, A. V., Slovokhotov, I. Yu., Shpakovski, D. G., Baranova, E. N., Khaliluev, M. R., Shematorova, E. K. (2017). A key enzyme of animal steroidogenesis can function in plants enhancing their immunity and accelerating the processes of growth and development. BMC Plant Biol., 17 (Suppl 1): 189, pp. 120–131.10.1186/s12870-017-1123-2568847629143658Search in Google Scholar

Simerský, R., Novák, O., Morris, D. A., Pouzar, V., Strnad, M. (2009). Identification and quantification of several mammalian steroid hormones in plants by UPLC-MS/MS. J. Plant Growth Regul., 28 (2), 125–136.10.1007/s00344-009-9081-zSearch in Google Scholar

Spivak, S. G., Berdichevets, I. N., Litvinovskaya, R. P., Drach, S. V., Kartel, N. A., Shpakovski, G. V. (2010). Some peculiarities of steroid metabolism in transgenic Nicotiana tabacum plants bearing the CYP11A1 cDNA of cytochrome P450scc from the bovine adrenal cortex. Russ. J. Bioorg. Chem., 36 (2), 224–232.10.1134/S1068162010020123Search in Google Scholar

Spivak, S. G., Berdichevets, I. N., Yarmolinsky, D. G., Maneshina, T. V., Shpakovski, G. V., Kartel, N. A. (2009). Construction and characteristics of transgenic tobacco Nicotiana tabacum L. plants expressing CYP11A1 cDNA encoding cytochrome P450scc. Russ. J. Gen., 45 (9), 1067–1073.Search in Google Scholar

Tenberge, K. B., Ruholl, C., Heinze, M., Eising, R. (1997). Purification and immuno-electron microscopical characterization of crystalline inclusions from plant peroxisomes. Protoplasma, 196 (3), 142–154.10.1007/BF01279563Search in Google Scholar

Verma, V., Ravindran, P., Kumar, P. P. (2016). Plant hormone-mediated regulation of stress responses. BMC Plant Biol., 16 (1), 86.10.1186/s12870-016-0771-y483111627079791Search in Google Scholar

Vinocur, B., Altman, A. (2005). Recent advances in engineering plant tolerance to abiotic stress: Achievements and limitations. Curr. Opin. Biotechnol., 16 (2), 123–132.10.1016/j.copbio.2005.02.00115831376Search in Google Scholar

Wang, W., Vinocur, B., Altman, A. (2003). Plant responses to drought, salinity and extreme temperatures: Towards genetic engineering for stress tolerance. Planta, 218 (1), 1–14.10.1007/s00425-003-1105-514513379Search in Google Scholar

van Wijk, K. J. (2015). Protein maturation and proteolysis in plant plastids, mitochondria, and peroxisomes. Annu. Rev. Plant Biol., 66, 75–111.10.1146/annurev-arplant-043014-11554725580835Search in Google Scholar

Yang, X. H., Xu, Z. H., Xue, H. W. (2005). Arabidopsis membrane steroid binding protein 1 is involved in inhibition of cell elongation. Plant Cell, 17 (1), 116–131.10.1105/tpc.104.02838154449415608331Search in Google Scholar

Ylstra, B., Touraev, A., Brinkmann, A. O., Heberle-Bors, E., Tunen, A. (1995). Steroid hormones stimulate germination and tube growth of in vitro matured tobacco pollen. Plant Physiol., 107 (2), 639–643.10.1104/pp.107.2.63915716812228388Search in Google Scholar

Yoshida, T., Furihata, H. Y., Kawabe, A. (2017). Analysis of nuclear mitochondrial DNAs and factors affecting patterns of integration in plant species. Genes Genetic Syste., 92 (1), 27–33.10.1266/ggs.16-0003928228607Search in Google Scholar

Zlobin, I. E., Kartashov A. V., Shpakovski, G. V. (2017). Different roles of glutathione in copper and zinc chelation in Brassica napus roots. Plant Physiol. Biochem., 118 (9), 333–341.10.1016/j.plaphy.2017.06.02928683402Search in Google Scholar