Abstract
Anthocerotophyta (hornworts) belong to a group of ancient nonvascular plants and originate from a common ancestor with contemporary vascular plants. Hornworts represent a unique model for investigating mechanisms of formation of stress resistance in higher plants due to their high tolerance to the action of adverse environmental factors. In this work, we demonstrate that the thallus of Anthoceros natalensis exhibits high redox activity changing under stress. Dehydration of the thallus is accompanied by the decrease in activities of intracellular peroxidases, DOPA-peroxidases, and tyrosinases, while catalase activity increases. Subsequent rehydration results in the increase in peroxidase and catalase activities. Kinetic features of peroxidases and tyrosinases were characterized as well as the peroxidase isoenzyme composition of different fractions of the hornwort cell wall proteins. It was shown that the hornwort peroxidases are functionally similar to peroxidases of higher vascular plants including their ability to form superoxide anion-radical. The biochemical mechanism was elucidated, supporting the possible participation of peroxidases in the formation of reactive oxygen species (ROS) via substrate—substrate interactions in the hornwort thallus. It has been suggested that the ROS formation by peroxidases is an evolutionarily ancient process that emerged as a protective mechanism for enhancing adaptive responses of higher land plants and their adaptation to changing environmental conditions and successful colonization of various ecological niches.
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Abbreviations
- CW:
-
cell wall
- DOPA:
-
3,4-dihydroxyphenylalanine
- ECS:
-
extracellular solution
- O2 -̣ :
-
superoxide anion-radical
- PIB:
-
post-infiltration buffer
- ROS:
-
reactive oxygen species
- SOD:
-
superoxide dismutase
- XTT:
-
2,3-bis-(2-methoxy-4nitro-5-sulfophenyl)-2H-tetrazolium-5-carboxanilide
References
Villarreal, J. C., Cargill, D. C., Söderström, L., Hagborg, A., and Renzaglia, K. S. (2010) A synthesis of hornwort diversity: patterns, causes and future work, Phytotaxa, 9, 150–166.
Asakawa, Y. (1995) in Progress in the Chemistry of Organic Natural Products (Herz, W., Kirby, G. W., Moore, R. E., Steglich, W., and Tamm, Ch., eds.) Vol. 65, Springer, Vienna, pp. 1–562.
Troitsky, A. V., Ignatov, M. S., Bobrova, V. K., and Milyutina, I. A. (2007) Contribution of genosystematics to current concepts of phylogeny and classification of bryophytes, Biochemistry (Moscow), 72, 1368–1376.
Chang, Y., and Graham, S. W. (2011) Inferring the higherorder phylogeny of mosses (Bryophyta) and relatives using a large, multigene plastid data set, Am. J. Bot., 98, 839–849.
Qiu, Y.-L., Li, L., Wang, B., Chen, Z., Knoop, V., Groth Malonek, M., Dombrovska, O., Lee, J., Kent, L., Rest, J., Estabrook, G. F., Hendry, T. A., Taylor, D. W., Testa, C. M., Ambros, M., Crandall-Stotler, B., Duff, R. J., Stech, M., Frey, W., Quandt, D., and Davis, C. C. (2006) The deepest divergences in land plants inferred from phylogenomic evidence, PNAS, 103, 15511–15516.
Adams, D. G., and Duggan, P. S. (2008) Cyanobacteria–bryophyte symbioses, J. Exp. Bot., 59, 1047–1058.
Wood, A. J. (2007) The nature and distribution of vegetative desiccation-tolerance in hornworts, liverworts and mosses, Bryologist, 110, 163–177.
Minibayeva, F., and Beckett, R. P. (2001) High rates of extracellular superoxide production in bryophytes and lichens, and an oxidative burst in response to rehydration following desiccation, New Phytologist, 152, 333–341.
Chasov, A. V., and Minibayeva, F. V. (2009) Effect of exogenous phenols on superoxide production by extracellular peroxidase from wheat seedling roots, Biochemistry (Moscow), 74, 766–774.
Minibayeva, F., Kolesnikov, O., Chasov, A., Beckett, R. P., Lüthje, S., Vylegzhanina, N., Buck, F., and Böttger, M. (2009) Wound-induced apoplastic peroxidase activities: their roles in the production and detoxification of reactive oxygen species, Plant Cell Environ., 32, 497–508.
Passardi, F., Longet, D., Penel, C., and Dunand, C. (2004) The class III peroxidase multigenic family in rice and its evolution in land plants, Phytochemistry, 65, 1879–1893.
Almagro, L., Gómez Ros, L. V., Belchi-Navarro, S., Bru, R., Ros Barceló, A., and Pedreño, M. A. (2009) Class III peroxidases in plant defense reactions, J. Exp. Bot., 60, 377–390.
Mathé, C., Barre, A., Jourda, C., and Dunand, C. (2010) Evolution and expression of class III peroxidases, Arch. Biochem. Biophys., 500, 58–65.
Mayaba, N., and Beckett, R. P. (2003) Increased activities of superoxide dismutase and catalase are not the mechanism of desiccation tolerance induced by hardening in the moss Atrichum androgynum, J. Bryol., 25, 281–286.
Li, J. L., Sulaiman, M., Beckett, R. P., and Minibayeva, F. V. (2010) Cell wall peroxidases in the liverwort Dumortiera hirsuta are responsible for extracellular superoxide production, and can display tyrosinase activity, Physiol. Plant., 138, 474–484.
Chasov, A. V., and Minibayeva, F. V. (2014) Methodological approaches for studying apoplastic redox activity: 1. Mechanisms of peroxidase release, Russ. J. Plant Physiol., 61, 556–563.
Chasov, A. V., and Minibayeva, F. V. (2014) Methodological approaches for studying apoplastic redox activity: 2. Regulation of peroxidase activity, Russ. J. Plant Physiol., 61, 626–633.
Sutherland, M. W., and Learmonth, B. A. (1997) The tetrazolium dyes MTS and XTT provide new quantitative assays for superoxide and superoxide dismutase, Free Rad. RPS, 27, 283–289.
Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature, 227, 680–685.
Hirata, T., Ashida, Y., Mori, H., Yoshinaga, D., and Goad, L. J. (2000) A 37-kDa peroxidase secreted from liverworts in response to chemical stress, Phytochemistry, 55, 197–202.
Lehtonen, M. T., Akita, M., Kalkkinen, N., Ahola-Iivarinen, E., Rönnholm, G., Somervuo, P., Thelander, M., and Valkonen, J. P. (2009) Quickly-released peroxidase of moss in defense against fungal invaders, New Phytol., 183, 432–443.
Van Loon, L. C., Rep, M., and Pieterse, C. M. J. (2006) Significance of inducible defence-related proteins in infected plants, Ann. Rev. Phytopathol., 44, 135–162.
Pshenichnov, E., Khashimova, N., Akhunov, A., Golubenko, Z., and Stipanovic, R. D. (2011) Participation of chitin-binding peroxidase isoforms in the wilt pathogenesis of cotton, AJPS, 2, 43–49.
O’Brien, J. A., Daudi, A., Butt, V. S., and Bolwell, G. P. (2012) Reactive oxygen species and their role in plant defense and cell wall metabolism, Planta, 236, 765–779.
Tognolli, M., Penel, C., Greppin, H., and Simon, P. (2002) Analysis and expression of the class III peroxidase large gene family in Arabidopsis thaliana, Gene, 288, 129–138.
Bolwell, G. P., Bindschedler, L. V., Blee, K. A., Butt, V. S., Davies, D. R., Gardner, S. L., Gerrish, C., and Minibayeva, F. (2002) The apoplastic oxidative burst in response to biotic stress in plants: a three-component system, J. Exp. Bot., 53, 1367–1376.
Lehtonen, M. T., Akita, M., Frank, W., Reski, R., and Valkonen, J. P. T. (2012) Involvement of a class III peroxidase and the mitochondrial protein TSPO in oxidative burst upon treatment of moss plants with a fungal elicitor, MPMI, 25, 363–371.
Tarchevskii, I. A. (2001) Metabolism of Plants under Stress [in Russian], Fen, Kazan.
Roach, T., Colville, L., Beckett, R. P., Minibayeva, F. V., Havaux, M., and Kranner, I. (2015) A proposed interplay between peroxidase, amine oxidase and lipoxygenase in the wounding-induced oxidative burst in Pisum sativum seedlings, Phytochemistry, 112, 130–138.
Mayer, A. M. (2006) Polyphenol oxidases in plants and fungi: going places? A review, Phytochemistry, 67, 2318–2331.
Lee, B. R., Kim, K. Y., Jung, W. J., Avice, J. C., Ourry, A., and Kim, T. H. (2007) Peroxidases and lignification in relation to the intensity of water-deficit stress in white clover (Trifolium repens L.), J. Exp. Bot., 58, 1271–1279.
Chen, Q., Yang, L., Ahmad, P., Wan, X., and Hu, X. (2011) Proteomic profiling and redox status alteration of recalcitrant tea (Camellia sinensis) seed in response to desiccation, Planta, 233, 583–592.
Halliwell, B. (1978) Lignin synthesis: the generation of hydrogen peroxide and superoxide by horseradish peroxidase and its stimulation by manganese (II) and phenols, Planta, 140, 81–88.
Lebedeva, O. V., and Ugarova, N. N. (1997) Steady-state kinetics of NADH oxidation by hydrogen peroxide in the presence of horseradish peroxidase, Biochemistry (Moscow), 62, 212–216.
Lebedeva, O. V., and Ugarova, N. N. (1996) Mechanism of peroxidase-catalyzed oxidation. Substrate–substrate activation in horseradish peroxidase-catalyzed reactions, Russ. Chem. Bull., 45, 18–25.
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Original Russian Text © A. V. Chasov, R. P. Beckett, F. V. Minibayeva, 2015, published in Biokhimiya, 2015, Vol. 80, No. 9, pp. 1391–1404.
Originally published in Biochemistry (Moscow) On-Line Papers in Press, as Manuscript BM15-017, June 21, 2015.
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Chasov, A.V., Beckett, R.P. & Minibayeva, F.V. Activity of redox enzymes in the thallus of Anthoceros natalensis . Biochemistry Moscow 80, 1157–1168 (2015). https://doi.org/10.1134/S0006297915090060
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DOI: https://doi.org/10.1134/S0006297915090060