Abstract
Effects of 5-aminolevulinic acid (ALA) at 200 mg/L on photosynthesis, structural organization of photosynthetic apparatus, oxygen uptake rate by the leaf tissue, contents of key respiratory enzymes—cytochrome c-oxidase (COX) and alternative oxidase (AOX)—and COX activity in winter rape plants (Brassica napus L.) were studied. It was found that 4–7-day-old seedlings grown on ALA solution accumulated phenols and their derivatives anthocyanins; the composition of the latter compounds was the same as in the control seedlings. Photosynthesis was inhibited in the ALA-treated plants since their capability to form structural the components of the photosynthetic apparatus—pigment–protein complexes (PPC) of the photosystems I and II—was reduced. In these plants, oxygen uptake by the leaf tissue increased under dark conditions. Simultaneously, the activity of the terminal COX of the cytochrome part of the respiratory path also increased as did the activity of another terminal respiratory enzyme, AOX, which is usually activated under stress, including oxidative.
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REFERENCES
Chupakhina, G.N., Maslennikov, P.V., and Skrypnik, L.N., Prirodnye antioksidanty (ekologicheskii aspekt) (Natural Antioxidants (Environmental Aspect)), Kaliningrad, 2011.
Gould, K.S., Markham, K.R., Smith, R.H., and Goris, J.J., Functional role of anthocyanins in the leaves of Quintinia serrata A. Cunn., J. Exp. Bot., 2000, vol. 51, pp. 1107–1115.
Feild, T.S., Lee, D.W., and Holbrook, N.M., Why leaves turn red in autumn. The role of anthocyanins in senescing leaves of red-osier dogwood, Plant Physiol., 2001, vol. 127, pp. 566–574.
Neill, S.O. and Gould, K.S., Anthocyanins in leaves: light attenuators or antioxidants? Funct. Plant Biol., 2003, vol. 30, pp. 865–873.
Wang, H., Cao, G., and Prior, R.L., Oxygen radical absorbing capacity of anthocyanins, J. Agric. Food Chem., 1997, vol. 45, pp. 304–309.
Giusti, M.M., Rodriguez-Saona, L.E., and Wrolstad, R.E., Molar absorptivity and color characteristics of acylated and non-acylated pelargonidin-based anthocyanins, J. Agric. Food Chem., 1999, vol. 47, pp. 4631–4637.
Xie, L., Wang, Z.H., Cheng, X.H., Gao, J.J., Zhang, Z.P., and Wang, L.J., 5-Aminolevulinic acid promotes anthocyanin accumulation in Fuji apples, Plant Growth Regul., 2013, vol. 69, pp. 295–303.
Chen, L., Guo, Y., Bai, G., and Li, Y., Effect of 5-aminolevulinic acid and genistein on accumulation of polyphenol and anthocyanin in qinyang apples, J. Anim. Plant Sci., 2015, vol. 25, pp. 68–79.
Feng, X., An, Y., Zheng, J., Sun, M., and Wang, L., Proteomic and SSH analyses of ALA-promoted fruit coloration and evidence for the involvement of a MADS-BOX gene, MdMADS1,Front. Plant Sci., 2016, vol. 7: 1615.
Feng, X., Chang, J., Cheng, S.Y., Zhu, J., Li, L.L., Wang, Y., and Cheng, H., Promotive effect of 5-aminolevulinic acid on the antioxidant system in Ginkgo bil-oba leaves, Afr. J. Biotechnol., 2009, vol. 8, pp. 3769–3776.
Xu, F., Cheng, S., Zhu, J., Zhang, W., and Wang, Y., Effect of 5-aminolevulinic acid on chlorophyll, photosynthesis, soluble sugar and flavonoids of Ginkgo biloba,Not. Bot. Horti Agrobot. Cluj-Napoca, 2011, vol. 39, pp. 41–47.
Averina, N.G. and Yaronskaya, E.B., Biosintez tetrapirrolov v rasteniyakh (Biosynthesis of Tetrapyrroles in Plants), Minsk: Belaruskaya Navuka, 2012.
Beizai, Z., Sherbakov, R.A., and Averina, N.G., Response of nitrate reductase to exogenous application of 5-aminolevulinic acid in barley plants, J. Plant Growth Regul., 2014, vol. 33, pp. 745–750.
Averina, N.G., Emel’yanova, A.V., Shcherbakov, R.A., Domanskaya, I.N., and Usatov, A.V., Induction of anthocyanin accumulation and status of protective system in winter rape plants treated with 5-aminolevulinic acid, Russ. J. Plant Physiol., 2017, vol. 64, pp. 310–318.
Singleton, V.L. and Rossi, J.A., Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents, Am. J. Enol. Vitic., 1965, vol. 16, pp. 144–158.
Lee, J., Rennaker, C., and Wrolstad, R., Correlation of two anthocyanin methods: HPLC and spectrophotometric methods, Food Chem., 2008, vol. 110, pp. 782–786.
Akinshina, N.G., Azizov, A.A., Karaseva, T.A., and Kloze, E., New possibilities for plant state, Sib. J. Ecol., 2008, vol. 2, pp. 249–254.
Jansson, S., Stefansson, H., Nystrom, U., Gustafsson, P., and Albertsson, P.-A., Antenna protein composition of PS I and PS II in thylakoid sub-domains, Biochim. Bi-ophys. Acta, 1997, vol. 1320, pp. 297–394.
Edmands S. and Burton, R.S., Cytochrome C oxidase activity in interpopulation hybrids of a marine copepod: a test for nuclear–nuclear or nuclear–cytoplasmic coadaptation, Evolution, 1999, vol. 53, pp. 1972–1978.
Ermakov, A.I., Arasimovich, V.V, Smirnova-Ikonnikova, M.I., Yarosh, N.P., and Lukovnikova, G.A., Metody biokhimicheskogo issledovaniya rastenii (Methods for the Biochemical Study of Plants), Leningrad: Kolos, 1972.
Borovik, O.A., Grabel’nykh, O.I., Koroleva, N.A., and Pobezhimova, T.P., The relationships among an activity of the alternative pathway respiratory flux, a content of carbohydrates and a frost-resistance of winter wheat, J. Stress Biol. Biochem., 2013, vol. 9, no. 4, pp. 241–250.
Forni, E., Ghezzi, M., and Polesello, A., HPLC separation and fluorimetric estimation of chlorophylls and pheophytins in fresh and frozen peas, Chromatographia, 1988, vol. 26, pp. 120–124.
Shemin, D., Delta-aminolevulinic acid degydrase from Rhodopseudomonas sphaeroides, in Methods in Enzymology, Colowick, S.P., Koplan, N.O., Eds., New York: Academic, 1962, vol. 5, pp. 883–884.
Chen, L., Guo, Y., Bai, G., and Li, Y., Effect of 5-aminolevulinic acid and genistein on accumulation of polyphenol and anthocyanin in 'Qinyang' apples, J. Anim. Plant Sci., 2015, vol. 25, pp. 68–79.
Guo, L., Cai, Z.X., Zhang, B.B., Xu, J.L., Song, H.F., and Ma, R.J., The mechanism analysis of anthocyanin accumulation in peach accelerated by ALA, Acta H-ortic., 2013, vol. 40, no. 6: 1043. https://doi.org/10.16420/j.issn.0513-353x.2013.06.004
Nagahatenna, D.S.K., Langridge, P., and Whitford, R., Tetrapyrrole-based drought stress signaling, Plant Bi-otechnol. J., 2015, vol. 13, pp. 447–459.
Larkin, R., Tetrapyrrole signaling in plants, Front. Plant Sci., 2016, vol. 7: 1586. https://doi.org/10.3389/fpls.2016.01586
Rogov, A.G., Sukhanova, E.I., Ural’skaya, L.A., Aliverdieva, D.A., and Zvyagil’skaya, R.A., Alternative oxidase: distribution, induction, properties, structure, regulation, and functions, Biochemistry (Moscow), 2014, vol. 79, no. 15, pp. 1615–1634. https://doi.org/10.1134/S0006297914130112
Cvetkovska, M. and Vanlerberghe, G.S., Alternative oxidase modulates leaf mitochondrial concentration of superoxide and nitric oxide, New Phytol., 2012, vol. 195, pp. 32–39.
Duggan, J.X., Meller, E., and Gassman, M.L., Catabolism of 5-aminolevulinic acid to CO2 by etiolated barley leaves, Plant Physiol., 1982, vol. 69, pp. 19–22. https://doi.org/10.1104/pp.69.3.602
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The work was supported by the Belarusian Republican Foundation for Fundamental Research (grant no. B17MS-019).
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Translated by A. Aver’yanov
Abbreviations: ALA—5-aminolevulinic acid; ALAD—5-aminolevulinate dehydratase; AOX—alternative oxidase; COX—cytochrome c-oxidase; PBG—porphobilinogen; PPC—pigment–protein complex of PSI or PSII; UPG III—uroporphyrinogen III.
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Averina, N.G., Yemelyanava, H.V., Sherbakov, R.A. et al. Photosynthesis and Oxygen Uptake Rate in Winter Rape Plants Treated with 5-Aminolevulinic Acid. Russ J Plant Physiol 66, 966–975 (2019). https://doi.org/10.1134/S1021443719060037
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DOI: https://doi.org/10.1134/S1021443719060037