Skip to main content
SpringerLink
Log in

Low Molecular Weight Antioxidants in Cyanobacteria and Plant Cells

  • Published:
Biology Bulletin Reviews Aims and scope Submit manuscript

Abstract

Oxygenic photosynthesis is one of the main sources of reactive oxygen species (ROS). In the cells of photosynthetic organisms, the mechanism of maintaining a balance between oxidative and antioxidant processes includes both enzymatic and nonenzymatic defense systems that are already formed in prokaryotic cells. The review presents current data on the main mechanisms of ROS formation in cyanobacteria and plant cells, a comparative analysis of the main groups of low molecular weight antioxidants (ascorbic acid, glutathione, tocopherols, carotenoids, anthocyanins, polyamines, etc.) and their contribution to ROS detoxification and cellular protection from oxidative stress.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.

Similar content being viewed by others

REFERENCES

  1. Abogadallah, G.M., Antioxidative defense under salt stress, Plant Signaling Behav., 2010, vol. 5, pp. 369–374.

    Article  CAS  Google Scholar 

  2. Alcázar, R., Altabella, T., Marco, F., et al., Polyamines: molecules with regulatory functions in plant abiotic stress tolerance, Planta, 2010, vol. 231, pp. 1237–1249. https://doi.org/10.1007/s00425-010-1130-0

    Article  CAS  PubMed  Google Scholar 

  3. Alonso, R., Elvira, S., Castillo, F.J., and Gimeno, B.S., Interactive effects of ozone and drought stress on pigments and activities of antioxidative enzymes in Pinus halepensis,Plant Cell Environ., 2001, vol. 24, pp. 905–916.

    Article  CAS  Google Scholar 

  4. Asensi-Fabaldo, M.A., Ammon, A., Sonnewald, U., et al., Tocopherol deficiency reduces sucrose export from salt-stressed potato leaves independently of oxidative stress and symplastic obstruction by callose, J. Exp. Bot., 2015, vol. 66, pp. 957–971. https://doi.org/10.1093/jxb/eru453

    Article  CAS  Google Scholar 

  5. Bartoli, C.G., Yu, J., Gómez, F., et al., Interrelationships between light and respiration in the control of ascorbic acid synthesis and accumulation in Arabidopsis thaliana leaves, J. Exp. Bot., 2006, vol. 57, pp. 1621–1631.

    Article  CAS  PubMed  Google Scholar 

  6. Bekker, D., Holland, H.D., Wang, P.L., et al., Dating the rise of atmospheric oxygen, Nature, 2004, vol. 427, pp. 117–120. https://doi.org/10.1038/nature02260

    Article  CAS  PubMed  Google Scholar 

  7. Bieza, K. and Lois, R., An Arabidopsis mutant tolerant to lethal ultraviolet B levels shows constitutively elevated accumulation of flavonoids and other phenolics, Plant Physiol., 2001, vol. 126, pp. 1105–1115. https://doi.org/10.1104/pp.126.3.1105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Blokhina, O., Virolainen, E., and Fagerstedt, K.V., Antioxidants, oxidative damage and oxygen deprivation stress: a review, Ann. Bot., 2003, vol. 91, pp. 179–194.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Bors, W., Langebartels, C., Michel, C., and Sandermann, H., Polyamines as radical scavengers and protectants against ozone damage, Phytochemistry, 1989, vol. 28, pp. 1589–1595.

    Article  CAS  Google Scholar 

  10. Bouchereau, A., Aziz, A., Larher, F., and Martin-Tanguy, J., Polyamines and environmental challenges: recent development, Plant Sci., 1999, vol. 140, pp. 103–125.

    Article  CAS  Google Scholar 

  11. Britton, G., The Biochemistry of Natural Pigments, Cambridge: Cambridge Univ. Press, 1983.

    Google Scholar 

  12. Campanella, J.J., Smalley, J.V., and Dempsey, M.E., A phylogenetic examination of the primary anthocyanin production pathway of the Plantae, Bot. Stud., 2014, vol. 55, p. 10. https://doi.org/10.1186/1999-3110-55-10

    Article  PubMed  PubMed Central  Google Scholar 

  13. Cheeseman, J.M., Hydrogen peroxide and plant stress: a challenging relationship, Plant Stress, 2007, vol. 1, pp. 4–15.

    Google Scholar 

  14. Chen, Q., Zhang, M., and Shen, S., Effect of salt on malondialdehyde and antioxidant enzymes in seedling roots of Jerusalem artichoke (Helianthus tuberosus L.), Acta Physiol. Plant., 2010, vol. 33, pp. 273–278.

    Article  CAS  Google Scholar 

  15. Cohen, M.F. and Yamasaki, H., Flavonoid-induced expression of a symbiosis-related gene in the Cyanobacterium Nostoc punctiforme,J. Bacteriol., 2000, vol. 182, pp. 4644–4646.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Cooper, S.K., Pandhare, J., Donald, S.P., and Phang, J.M., A novel function of hydroxyproline oxidase in apoptosis through generation of reactive oxygen species, J. Biol. Chem., 2008, vol. 283, pp. 485–492. https://doi.org/10.1074/jbc.M702181200

    Article  CAS  Google Scholar 

  17. Dat, J., Vandenabeele, S., Vranová, E., et al., Dual action of active oxygen species during plant stress responses, Cell. Mol. Life Sci., 2000, vol. 57, pp. 779–795.

    Article  CAS  PubMed  Google Scholar 

  18. Deniz, F., Saygideger, S.D., and Karaman, S., Response to copper and sodium chloride excess in Spirulina sp. (Cyanobacteria), Bull. Environ. Contam. Toxicol., 2011, vol. 87, pp. 11–15.

    Article  CAS  PubMed  Google Scholar 

  19. Do, P.T., Drechsel, O., Heyer, A.G., et al., Changes in free polyamine levels, expression of polyamine biosynthesis genes, and performance of rice cultivars under salt stress: a comparison with responses to drought, Front. Plant Sci., 2014, vol. 5, pp. 182–192. https://doi.org/10.3389/fpls.2014.00182

    Article  PubMed  PubMed Central  Google Scholar 

  20. Fahey, R.C., Glutathione analogs in prokaryotes, Biochim. Biophys. Acta, Gen. Subj., 2013, vol. 1830, pp. 3182–3198.

    Article  CAS  Google Scholar 

  21. Fichman, Y., Gerdes, S.Y., Kovasc, H., et al., Evolution of proline biosynthesis: enzymology, bioinformatics, genetics and transcriptional regulation, Biol. Rev. Camb. Phylos. Sci., 2015, vol. 90, pp. 1065–1089. https://doi.org/10.1111/brv.12146

    Article  Google Scholar 

  22. Foyer, C.H. and Noctor, G., Oxidant and antioxidant signaling in plants: a reevaluation of the concept of oxidative stress in a physiological context, Plant Cell Environ., 2005, vol. 28, pp. 1056–1071.

    Article  CAS  Google Scholar 

  23. Foyer, C.H. and Noctor, G., Ascorbate and glutathione: the heart of the redox hub, Plant Physiol., 2011, vol. 155, pp. 2–18.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Foyer, C.H., Lelandais, M., and Kunert, K., Photooxidative stress in plant, Physiol. Plant., 1994, vol. 92, pp. 696–717.

    Article  CAS  Google Scholar 

  25. Fryzova, R., Pohanka, M., Martinkova, P., et al., Oxidative stress and heavy metals in plants, Rev. Environ. Contam. Toxicol., 2018, vol. 245, pp. 129–156. https://doi.org/10.1007/398_2017_7

    Article  CAS  PubMed  Google Scholar 

  26. Fu, J. and Huang, B., Involvement of antioxidants and lipid peroxidation in the adaptation of two cool-season grasses to localized drought stress, Environ. Exp. Bot., 2001, vol. 45, pp. 105–114.

    Article  CAS  PubMed  Google Scholar 

  27. Galston, A.W., Kaur-Sawhney, R., Altabella, T., and Tiburcio, A.F., Plant polyamines in reproductive activity and response to abiotic stress, Bot. Acta, 1997, vol. 110, pp. 197–207. https://doi.org/10.1111/j.1438-8677.1997.tb00629.x

    Article  CAS  Google Scholar 

  28. Gechev, T.S., van Breusegem, F., Stone, J.M., et al., Reactive oxygen species as signals that modulate plant stress responses and programmed cell death, BioEssays, 2006, vol. 28, pp. 1091–1101.

    Article  CAS  PubMed  Google Scholar 

  29. Goiris, K., Muylaert, K., Voorspoels, S., et al., Detection of flavonoids in microalgae of different evolutionary lineages, J. Phycol., 2014, vol. 50, no. 3, pp. 483–492. https://doi.org/10.1111/jpy.12180

    Article  CAS  PubMed  Google Scholar 

  30. Gotz, T., Windhovel, U., Boger, P., and Sandmann, G., Protection of photosynthesis against ultraviolet-B radiation by carotinoids in transformants of cyanobacteria Synechoccocus PCC 7942, Plant Physiol., 1999, vol. 120, pp. 599–604. https://doi.org/10.1104/pp.120.2.599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Groppa, M.D. and Benavides, M.P., Polyamines and abiotic stress: recent advances, Amino Acids, 2008, vol. 34, pp. 35–45. https://doi.org/10.1007/s00726-007-0501-8

    Article  CAS  PubMed  Google Scholar 

  32. Gross, F., Durner, J., and Gaupels, F., Nitric oxide, antioxidants and prooxidants in plant defense response, Front. Plant Sci., 2013, vol. 4, art. ID 419. https://doi.org/10.3389/fpls.2013.00419

    Article  PubMed  PubMed Central  Google Scholar 

  33. Halliwell, B., Reactive speces and antioxidants. Redox biology is a fundamental theme of aerobic life, Plant Physiol., 2006, vol. 141, pp. 312–322.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Hamana, K. and Matsuzaki, S., Polyamines as a chemotaxonomic marker in bacterial systematic, Crit. Rev. Microbiol., 1992, vol. 18, pp. 261–283. https://doi.org/10.3109/10408419209113518

    Article  CAS  PubMed  Google Scholar 

  35. He, Y.Y. and Häder, D.P., Reactive oxygen species and UVB: effect on cyanobacteria, Photochem. Photobiol. Sci., 2002, vol. 1, pp. 729–736.

    Article  CAS  PubMed  Google Scholar 

  36. Ignatova, Z. and Gierasch, L.M., Inhibition of protein aggregation in vitro and in vivo by a natural osmoprotectant, Proc. Natl. Acad. Sci. U.S.A., 2006, vol. 103, pp. 13357–13361.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Iori, V., Pietrini, F., Cheremisina, A., et al., Growth responses, metal accumulation and phytoremoval capability in Amaranthus plants exposed to nickel under hydroponics, Water, Air Soil Pollut., 2013, vol. 224, p. 1450. https://doi.org/10.1007/s11270-013-1450-3

    Article  CAS  Google Scholar 

  38. Jimenez-Del-Rio, M. and Velez-Pardo, C., The bad, the good, and the ugly about oxidative stress, Oxid. Med. Cell. Longevity, 2012, art. ID 163913. https://doi.org/10.1155/2012/163913

    Article  CAS  Google Scholar 

  39. Kakkar, R.K. and Sawhney, V.K., Polyamine research in plants—a changing perspective, Physiol. Plant., 2003, vol. 116, pp. 281–292. https://doi.org/10.1034/j.1399-3054.2002.1160302.x

    Article  Google Scholar 

  40. Kaur-Sawhney, R., Tiburcio, A.F., Altabella, T., and Galston, A.W., Polyamines in plants: an overview, J. Cell Mol. Biol., 2003, vol. l, pp. 1–12.

    Google Scholar 

  41. Kavi Kishor, P.B., Sangam, S., Amrutha, R.N., et al., Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: Its implications in plant growth and abiotic stress tolerance, Curr. Sci., 2005, vol. 88, pp. 424–438.

    Google Scholar 

  42. Kerfeld, Ch.A., Melnicki, M.R., Sutter, M., and Domingues-Martin, M.A., Structure, function and evolution of the cyanobacteria orange carotenoid protein and its homologs, New Phytol., 2017, vol. 215, pp. 937–951.

    Article  CAS  PubMed  Google Scholar 

  43. Kirilovsky, D. and Kerfeld, Ch., The orange carotenoid protein in photoprotection of photosysteme II in cyanobacteria, Biochim. Biophys. Acta,Bioenerg., 2012, vol. 1817, pp. 158–166.

    Article  CAS  Google Scholar 

  44. Kumar, S. and Pandey, A.K., Chemistry and biological activities of flavonoids: an overview, Sci. World J., 2013, vol. 2013, art. ID 162750. https://doi.org/10.1155/2013/162750

    Article  CAS  Google Scholar 

  45. Kumar, N., Pal, M., Singh, A., et al., Exogenous proline alleviates oxidative stress and increase vase life in rose (Rosa hybrida L. ‘Grand Gala’), Sci. Hort., 2010, vol. 127, pp. 79–85.

    Article  CAS  Google Scholar 

  46. Kuznetsov, Vl.V. and Shevyakova, N.I., Polyamines and plant adaptation to saline environment, in Desert Plants: Biology and Biotechnology, Ramawat, K.B., Ed., Heidelberg: Springer-Verlag, 2011, pp. 261–297.

    Google Scholar 

  47. Larcher, W., Physiological Plant Ecology: Ecophysiology and Stress Physiology of Functional Groups, Berlin: Springer-Verlag, 2003.

    Book  Google Scholar 

  48. Latifi, A., Ruiz, M., and Zhang, Ch.-C., Oxidative stress in cyanobacteria, FEMS Microbiol. Rev., 2009, vol. 33, pp. 258–278.

    Article  CAS  PubMed  Google Scholar 

  49. Leisso, R.S., Buchanan, D.A., Lee, J., et al., Chilling related cell damage of apple (Malus × domestica Borkh.) fruit cortical tissue impacts antioxidant, lipid and phenolic metabolism, Physiol. Plant., 2015, vol. 153, pp. 204–220. https://doi.org/10.1111/ppl.12244

    Article  CAS  PubMed  Google Scholar 

  50. Li, J., OuLee, T.M., and Raba, R., Arabidopsis flavonoid mutants are hypersensitive to ultraviolet B radiation, Plant Cell., 1993, vol. 5, pp. 171–179.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Mackerness, S.A.H., Plant responses to ultraviolet B (UVB: 280–320 nm) stress: what are the key regulators? Plant Growth Reg., 2000, vol. 32, pp. 27–39. https://doi.org/10.1023/A:1006314001430

    Article  CAS  Google Scholar 

  52. Maeda, H., Sakuragi, Y., Bryant, D.A., and DellaPenna, D., Tocopherols protect Synechocystis sp. strain PCC 6803 from lipid peroxidation, Plant Physiol., 2005, vol. 135, pp. 1422–1432.

    Article  CAS  Google Scholar 

  53. Mapelli, S., Brambilla, I.M., Radyukina, N.L., et al., Free and bound polyamines changes in different plants as a consequence of UVB light irradiation, Gen. Appl. Plant Physiol., 2008, vol. 34, pp. 55–66.

    CAS  Google Scholar 

  54. Matysik, J., Alia, B., Bhalu, B., and Mohanty, P., Molecular mechanism of quenching of reactive oxygen species by proline under stress in plant, Curr. Sci., 2002, vol. 82, pp. 525–532.

    CAS  Google Scholar 

  55. McClure, J.W., Physiology of flavonoids in plants, Prog. Clin. Biol. Res., 1986, vol. 213, pp. 525–532.

    Google Scholar 

  56. Minocha, R., Majumbar, R., and Minocha, S.C., Poliamines and abiotic stress in plants: a complex relationship, Front. Plant Sci., 2014, vol. 5, pp. 1–17. https://doi.org/10.3389/fpls.2014.00175

    Article  Google Scholar 

  57. Miret, J.A. and MunnéBosch, S., Redox signaling and stress tolerance in plants: a focus on vitamin E, Ann. N.Y. Acad. Sci., 2015, vol. 1340, pp. 29–38.

    Article  CAS  PubMed  Google Scholar 

  58. Mittova, V., Tal, M., Volokita, M., and Guy, M., Upregulation of the leaf mitochondrial and peroxisomal antioxidative systems in response to salt induced oxidative stress in the wild salt-tolerant tomato species Lycopersicon pennellii,Plant Cell Environ., 2003, vol. 26, pp. 845–856.

    Article  CAS  PubMed  Google Scholar 

  59. Miura, K. and Tada, Y., Regulation of water, salinity, and cold stress responses by salicylic acid, Front. Plant Sci., 2014, vol. 5, art. ID 4. https://doi.org/10.3389/fpls.2014.00004

    Article  PubMed  PubMed Central  Google Scholar 

  60. Moschou, P., Paschalidis, K., and Roubelakis-Angelakis, K.A., Plant polyamine catabolism: the state of the art, Plant Signaling Behav., 2008, vol. 12, pp. 1061–1066.

    Article  Google Scholar 

  61. Mpoloka, S.W., Effects of prolonged UVB exposure in plants, Afr. J. Biotechnol., 2008, vol. 7, no. 25, pp. 4874–4883.

    CAS  Google Scholar 

  62. Nakabayashi, R., Yonekura-Sakakibara, K., Urano, K., et al., Enhancement of oxidative and drought tolerance in Arabidopsis by overaccumulation of antioxidant flavonoids, Plant J., 2014, vol. 77, pp. 367–379.

    Article  CAS  PubMed  Google Scholar 

  63. Nishiyama, Y. and Murata, N., Revised scheme for the mechanism of photoinhibition and its application to enhance the abiotic stress tolerance of the photosynthetic machinery, Appl. Microbiol. Biotechnol., 2014, vol. 98, pp. 8777–8796. https://doi.org/10.1007/s00253-014-6020-0

    Article  CAS  PubMed  Google Scholar 

  64. Poduslo, J.F. and Curran, G.L., Increased permeability of superoxide dismutase at the blood-nerve and blood-brain barriers with retained enzymatic activity after covalent modification with the naturally occurring polyamine, putrescine, J. Neurochem., 1996, vol. 67, pp. 734–741.

    Article  CAS  PubMed  Google Scholar 

  65. Polesskaya, O.G., Rastitel’naya kletka i aktivnye formy kisloroda (The Plant Cell and Active Oxygen Species), Ermakov, I.P., Ed., Moscow: KDU, 2007.

    Google Scholar 

  66. Radyukina, N.L., Shashukova, A.V., Shevyakova, N.I., and Kuznetsov, Vl.V., Proline involvement in the common sage antioxidant system in the presence of NaCl and paraquat, Russ. J. Plant Physiol., 2008, vol. 55, no. 5, pp. 649–656.

    Article  CAS  Google Scholar 

  67. Radyukina, N.L., Ivanov, Yu.V., Kartashov, A.V., et al., Regulation of gene expression governing proline metabolism in Thellungiella salsuginea by NaCl and paraquat, Russ. J. Plant Physiol., 2011, vol. 58, pp. 643–652.

    Article  CAS  Google Scholar 

  68. Rayapati, P.J. and Stewart, C.R., Solubilization of a proline dehydrogenase from maize (Zea mays L.) mitochondria, Plant. Physiol., 1991, vol. 95, pp. 787–791.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Rodríguez-Pérez, C., Segura-Carretero, A., and Del Mar Contreras, M., Phenolic compounds as natural and multifunctional antiobesity agents: a review, Crit. Rev. Food Sci. Nutr., 2017, vol. 11, pp. 1–18. https://doi.org/10.1080/10408398.2017.1399859

    Article  CAS  Google Scholar 

  70. Satkoski, A.M., Beukes, M.J., Li, W., et al., A redox-stratified ocean 3.2 billion years ago, Earth Planet. Sci. Lett., 2015, vol. 430, pp. 43–53. https://doi.org/10.1016/j.epsl.2015.08.007

    Article  CAS  Google Scholar 

  71. Scandalias, J.G., Response of plant antioxidant defense genes to environmental stress, Adv. Genet., 1990, vol. 28, pp. 1–41.

    Article  Google Scholar 

  72. Schagerl, M. and Muller, B., Acclimation of chlorophyll a and carotinoid levels to different irradiances in four freshwater, J. Plant Physiol., 2006, vol. 163, pp. 709–716. https://doi.org/10.1016/j.jplph.2005.09.015

    Article  CAS  PubMed  Google Scholar 

  73. Sells, G.D. and Koeppe, D.E., Oxidation of proline by mitochondria isolated from water-stressed maize shoots, Plant. Physiol., 1981, vol. 68, pp. 1058–1063.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Shah, Z.H., Rehman, H.M., Akhtar, T., et al., Redox and ionic homeostasis regulations against oxidative, salinity and drought stress in wheat (a systems biology approach), Front. Genet., 2017, vol. 8, art. ID 141. https://doi.org/10.3389/fgene.2017.00141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Sheeba, Singh, V.P., Srivastava, P.K., and Prasad, S.M., Differential physiological and biochemical responses of two cyanobacteria Nostoc muscorum and Phormidium foveolarum against oxyfluorfen and UV-B radiation, Ecotoxicol. Environ. Saf., 2011, vol. 74, no. 7, pp. 1981–1993.

    Article  CAS  PubMed  Google Scholar 

  76. Sheo, M.P., Dwivedi, R., Zeeshan, M., and Singh, R., UVB and cadmium induced changes in pigments, photosynthetic electron transport activity, antioxidant levels and antioxidative enzyme activities of Riccia sp., Acta Physiol. Plant., 2004, vol. 26, pp. 423–430.

  77. Shestakov, S.V. and Karbysheva, E.A., The origin and evolution of cyanobacteria, Biol. Bull. Rev., 2017, vol. 7, no. 4, pp. 259–272.

    Article  Google Scholar 

  78. Singh, D.P., Srivastava, P.K., and Prasad, S.M., Differential effect of UV-B radiation on growth, oxidative stress and ascorbat-glutathion cycle in two cyanobacteria under copper toxicity, Plant. Physiol. Biochem., 2012, vol. 61, pp. 61–67.

    Article  CAS  PubMed  Google Scholar 

  79. Singh, D.P., Prabha, R., Meena, K.K., et al., Induced accumulation of polyphenolics and flavonoids in Cyanobacteria under salt stress protects organisms through enhanced antioxidant activity, Am. J. Plant Sci., 2014, vol. 5, pp. 726–735. https://doi.org/10.4236/ajps.2014.55087

    Article  CAS  Google Scholar 

  80. Singh, D.P., Prabha, P., Verma, S., et al., Antioxidant properties and polyphenolic content in terrestrial cyanobacteria, 3 Biotech, 2017, vol. 7, no. 134, pp. 1–14.

  81. Slocum, R.D., Kaur-Sawhney, R., and Galston, A.W., The physiology and biochemistry of polyamines in plants, Arch. Biochem. Biophys., 1984, vol. 35, pp. 283–303.

    Article  Google Scholar 

  82. Sobieszczuk-Nowicka, E. and Legocka, J., Plastid-associated polyamines: their role in differentiation structure, functioning, stress response and senescence, Plant Biol., 2014, vol. 16, pp. 297–305. https://doi.org/10.1111/plb.12058

    Article  CAS  PubMed  Google Scholar 

  83. Solovchenko, A.E. and Merzlyak, M.N., Screening of visible and UV radiation as a photoprotective mechanism in plants, Russ. J. Plant Physiol., 2008, vol. 55, no. 6, pp. 719–737.

    Article  CAS  Google Scholar 

  84. Stapleton, A.E. and Walbot, V., Flavonoids can protect maize DNA from the induction of ultraviolet radiation damage, Plant Physiol., 1994, vol. 105, pp. 881–889.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Storme, J.Y., Golubic, S., Wilmotte, A., et al., Raman characterization of the UV-protective pigment gloeocapsin and its role in the survival of Cyanobacteria, Astrobiology, 2015, vol. 10, pp. 843–857.

    Article  CAS  Google Scholar 

  86. Szarka, A., Tomasskovics, B., and Banhegyi, G., The ascorbate-glutathione-α-tocopherol triad in abiotic stress response, Int. J. Mol. Sci., 2012, vol. 13, pp. 4458–4483.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Tanner, J.J., Structural biology of proline catabolism, Amino Acids, 2008, vol. 35, pp. 719–730. https://doi.org/10.1007/s00726-008-0062-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Tanou, G., Ziogas, V., Belghazi, M., et al., Polyamines reprogram oxidative and nitrosative status and the proteome of citrus plants exposed to salinity stress, Plant Cell Environ., 2014, vol. 37, pp. 864–885. https://doi.org/10.1111/pce.12204

    Article  CAS  PubMed  Google Scholar 

  89. Tichy, M. and Vermaas, W., In vivo role of catalase-peroxidase in Synechocystis sp. strain PCC 6803, J. Bacteriol., 1999, vol. 181, pp. 1875–1882.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Tomitani, A., Knoll, A.H., Cavanaugh, C.M., and Ohno, T., The evolutionary diversification of cyanobacteria: molecular-phylogenetic and paleontological perspectives, Proc. Natl. Acad. Sci. U.S.A., 2006, vol. 103, no. 14, pp. 5442–5447.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Verbruggen, N. and Hermans, C., Proline accumulation in plants: a review, Amino Acids, 2008, vol. 35, pp. 753–759. https://doi.org/10.1007/s00726-008-0061-6

    Article  CAS  PubMed  Google Scholar 

  92. Verslues, P.E. and Sharma, S., Proline metabolism and its implications for plant-environment interaction, Arabidopsis Book, 2010, vol. 8, p. e0140. https://doi.org/10.1199/tab.0140

    Article  PubMed  PubMed Central  Google Scholar 

  93. Urano, K., Yoshiba, Y., Nanjo, T., et al., Characterization of Arabidopsis genes involved in biosynthesis of polyamines in abiotic stress responses and developmental stages, Plant Cell Environ., 2003, vol. 26, pp. 1917–1926. https://doi.org/10.1046/j.1365-3040.2003.01108.x

    Article  CAS  Google Scholar 

  94. Xue, Y. and He, Q., Cyanobacteria as cell factories to produce plant secondary metabolites, Front. Bioeng. Biotechnol., 2015, vol. 3, pp. 57–64.

    Article  PubMed  PubMed Central  Google Scholar 

  95. Zhu, X., Li, Q., Yin, Ch., et al., Role of spermidine in overwintering of cyanobacteria, J. Bacteriol., 2015, vol. 197, pp. 2325–2334. https://doi.org/10.1128/JB.00153-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

The work was supported by the Russian Foundation for Basic Research (project no. 17-04-01-098).

Author information

Authors and Affiliations

  1. Biology Department, Moscow State University, Moscow, Russia

    N. L. Radyukina, L. E. Mikheeva & E. A. Karbysheva

Authors
  1. N. L. Radyukina
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. L. E. Mikheeva
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. E. A. Karbysheva
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to E. A. Karbysheva.

Ethics declarations

Conflict of interest. The authors declare that they have no conflict of interest.

Statement of the welfare of animals. This article does not contain any studies involving animals or human participants performed by any of the authors.

Additional information

Translated by E.V. Makeeva

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Radyukina, N.L., Mikheeva, L.E. & Karbysheva, E.A. Low Molecular Weight Antioxidants in Cyanobacteria and Plant Cells. Biol Bull Rev 9, 520–531 (2019). https://doi.org/10.1134/S2079086419060045

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S2079086419060045

Keywords:

Search

Navigation