ISSN 2415-8860 (online), ISSN 0372-4123 (print)
logoUkrainian Botanical Journal
  • 9 of 9
Ukr. Bot. J. 2020, 77(4): 331–343
Cell Biology and Molecular Biology

Lipid peroxidation of cell membranes in the formation and regulation of plant protective reactions

Mamenko T.P., Kots S.Ya.

This review summarizes the most recent information on the role of lipid peroxidation processes in cell membranes and lipid peroxidation products in the regulation and formation of plant metabolism under the influence of stress factors. It is emphasized that plasmalemma permeability is an integral indicator of determining the functional state of plant cells under stress. The importance of the processes of lipoperoxidation in the formation of protective reactions and maintenance of homeostasis of plants under adverse effects is considered. It is concluded that activation of lipid peroxidation can cause the development of cell damage and then cell death, and at the same time induce the activation of protective mechanisms and the development of adaptive responses aimed at increasing stress resistance. The tasks and prospects of further research of cell membrane lipid peroxide oxidation processes are discussed in order to clarify the role of lipoperoxidation products in signaling, regulation, and maintenance of homeostasis by stressors.

Keywords: adaptive reactions, homeostasis, lipid peroxidation, plasmalemma, stress resistance

Full text: PDF (Ukr) 951K

  1. Agadjanyan Z.S., Dmitriev L.F., Dugin S.F. 2005. A new role of phosphoglucose isomerase. involvement of the glycolytic enzyme in aldehyde metabolism. Biochemistry, 70(11): 1251–1255.
  2. Agarwal S., Shaheen, R. 2007. Stimulation of antioxidant system and lipid peroxidation by abiotic stresses in leaves of Momordica charantia. Brazilian Journal of Plant Physiology, 19(2): 149–161.
  3. Apel K., Hirt H. 2004. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology, 5: 373–399.
  4. Argüelles S., García S., Maldonado M., Machado A., Ayala A. 2004. Do the serum oxidative stress biomarkers provide a reasonable index of the general oxidative stress status? Biochimica et Biophysica Acta: General Subjects, 1674(3): 251–259.
  5. Argüelles S., Gómez A., Machado A., Ayala A. 2007. A preliminary analysis of within-subject variation in human serum oxidative stress parameters as a function of time. Rejuvenation Research, 10(4): 621–636.
  6. Ashraf M.A., Ashraf M., Ali Q. 2010. Response of two genetically diverse wheat cultivars to salt stress at different growth stages: leaf lipid peroxidation and phenolic contents. Pakistan Journal of Botany, 42(1): 559–565.
  7. Ashraf M., Foolad M.R. 2013. Crop breeding for salt tolerance in the era of molecular markers and markerassisted selection. Plant Breeding, 132(1): 10–20.
  8. Auler P.A., do Amaral M.N., Rossatto T., Vighi I.L., Benitez L.C., da Maia L.C., Braga E.J.B. 2019. Expression of transcription factors involved with dehydration in contrasting rice genotypes submitted to different levels of soil moisture. Genetics and Molecular Research, 18 (1): 1–15.
  9. Ayala A., Muñoz M.F., Argüelles S. 2014. Lipid peroxidation: Production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxidative Medicine and Cellular Longevity, 2014(6): 360–438.
  10. Bagam P., Singh D.P., Inda M.E., Batra S. 2017. Unraveling the role of membrane microdomains during microbial infection. Cell Biology and Toxicology, 33(5): 429–455.
  11. Barrera G., Pizzimenti S., Daga M., Dianzani C., Arcaro A., Cetrangolo G.P., Giordano G., Cucci M.A., Graf M., Gentile F. 2018. Lipid peroxidation-derived aldehydes, 4-hydroxynonenal and malondialdehyde in agingrelated disorders. Antioxidants, 7(8): 1–17.
  12. Bandurka N.M. 2014. Biomedical and Biosocial Anthropology, 23: 263–269.
  13. Baraboi V.A. 1991. Uspekhi Sovremennoi Biologii, 111(6): 923–932.
  14. Baranenko V.V. 2009. Ukrainian Botanical Journal, 66(5): 713–721.
  15. Cacas J.-L., Furt F., Le Guédard M., Schmitter J.M., Buré C., Gerbeau-Pissot P., Moreau P., Bessoule J.J., Simon-Plas F., Mongrand S. 2012. Lipids of plant membrane rafts. Progress in Lipid Research, 51(3): 272–299.
  16. Chaves M.M., Maroco J.P., Pereira J.S. 2003. Understanding plant responses to drought – from genes to the whole plant. Functional Plant Biology, 30(3): 239–264.
  17. Chen C., Smye S.W., Robinson M.P., Evans J.A. 2006. Membrane electroporation theories: a review. Medical and Biological Engineering and Computer, 44(1–2): 5–14.
  18. Chirkova T.V. 1997. Sorosovskiy obrazovatel'nyy zhurnal, 9: 12–17.
  19. Cerezini P., Riar M.K., Sinclair T.R. 2016. Transpiration and nitrogen fixation recovery capacity in soybean following drought stress. Journal of Crop Improvement, 30(5): 562– 571.
  20. DaCosta M., Huang B. 2007. Changes in antioxidant enzyme activities and lipid peroxidation for bentgrass species in response to drought stress. Journal of the American Society for Horticultural Science, 132(3): 319–326.
  21. Deka D., Singh A.K., Singh A.K. 2018. Effect of drought stress on crop plants with special reference to drought avoidance and tolerance mechanisms. International Journal of Current Microbiology and Applied Sciences, 7(9): 2703– 2721.
  22. Demir F., Horntrich C., Blachutzik J.O., Scherzer S., Reinders Y., Kierszniowska S., Schulze W.X., Harms G.S., Hedrich R., Geiger D., Kreuzeret I. 2013. Arabidopsis nanodomain-delimited ABA signaling pathway regulates the anion channel SLAH3. Proceedings of the National Academy of Science USA, 110(20). 8296–8301.
  23. Domingues R.M., Domingues P., Melo T., Pérez-Sala D., Reis A., Spickett C.M. 2013. Lipoxidation adducts with peptides and proteins: deleterious modifications or signaling mechanisms? Journal of Proteomics, 92: 110– 131.
  24. Dong S., Jiang Y., Dong Y., Wang L., Wang W., Ma Z., Yan C., Ma C., Liu L. 2019. A study on soybean responses to drought stress and rehydration. Saudi Journal of Biological Sciences, 26(8): 2006–2017.
  25. Fan L., Li R., Pan J., Ding Z., Lin J. 2015. Endocytosis and its regulation in plants. Trends in Plant Science, 20(6): 388– 397.
  26. Farooq M., Wahid A., Kobayashi N., Fujita, D., Basra S.M.A. 2009. Plant drought stress: effects, mechanisms and management. Agronomy for Sustainable Development, 29(1): 185–212.
  27. Fathi A., Tari D.B. 2016. Effect of drought stress and its mechanism in plants. International Journal of Life Sciences, 10(1): 1–6.
  28. Finkel T., Holbrook N.J. 2000. Oxidants, oxidative stress and the biology of ageing. Nature, 408(6809): 239–247.
  29. Gaweł S., Wardas M., Niedworok E., Wardas P. 2004. Malondialdehyde (MDA) as a lipid peroxidation marker. Wiadomości lekarskie, 57(9–10): 453–455.
  30. Giera M., Lingeman H., Niessen W.M.A. 2012. Recent advancements in the LC- and GC-based analysis of malondialdehyde (MDA): a brief overview. Chromatographia, 75(9–10): 433–440.
  31. Guo Y.Y.,Yu H.Y.,Yang M.M., Kong D.S., Zhang Y.J. 2018. Effect of drought stress on lipid peroxidation, osmotic adjustment and antioxidant enzyme activity of leaves and roots of Lycium ruthenicum Murr. seedling. Russian Journal of Plant Physiology, 65(2): 244–250.
  32. Gutierrez-Carbonell E., Takahashi D., Lüthje S., González-Reyes J.A., Mongrand S., Contreras-Moreira B., Abadía A., Uemura M., Abadía J., López-Millán A.F. 2016. Shotgun proteomic approach reveals that Fe deficiency causes marked changes in the protein profiles of plasma membrane and detergent-resistant microdomain preparations from Beta vulgaris roots. Journal of Proteome Research, 15(8): 2510–2524.
  33. Haney C.H., Riely B.K., Tricoli D.M., Cook D.R., Ehrhardt D.W., Long S.R. 2011. Symbiotic rhizobia bacteria trigger a change in localization and dynamics of the Medicago truncatula receptor kinase LYK3. Plant Cell, 23: 2774–2787.
  34. Hohenberger P., Eing C., Straessner R., Durst S., Frey W., Nick P. 2011. Plantactin controls membrane permeability. Biochimica et Biophysica Acta, 1808(9): 2304–2312.
  35. Jarsch I.K., Ott T. 2011. Perspectives on remorin proteins, membrane rafts, and their role during plant–microbe interactions. Molecular Plant-Microbe Interactions, 24(1): 7–12.
  36. Jemo M., Sulieman S., Bekkaoui F., Oluwatosin A.K., Olomide A. H., Allah E.F.A., Alqarawi A.A., Tran L.S.P. 2017. Comparative analysis of the combined effects of different water and phosphate levels on growth and biological nitrogen fixation of nine cowpea varieties. Frontiers in Plant Science, 8(2111): 1–16.
  37. Khoubnasabjafari M., Ansarin K., Jouyban A. 2015. Reliability of malondialdehyde as a biomarker of oxidative stress in psychological disorders. Bioimpacts, 5(3): 123– 127.
  38. Kaur N., Gupta A.K. 2005. Signal transduction pathways under abiotic stresses in plant. Current Science, 88(11): 1771–1780.
  39. Kinnunen P.K.J., Kaarniranta K., Mahalka A.K. 2012. Proteinoxidized phospholipid interactions in cellular signaling for cell death: from biophysics to clinical correlations. Biochimica et Biophysica Acta, 1818(10): 2446–2455.
  40. Kolupaev Yu.Ye., Karpets Yu.V. 2007. Ukrainian Botanical Journal, 64(5): 713–719.
  41. Kolupaev Yu.Ie., Kosakivska I.V. 2008. Ukrainian Botanical Journal, 65(3): 418–430.
  42. Kraft M. L. 2013. Plasma membrane organization and function: moving past lipid rafts. Molecular Biology of the Cell, 24(18): 2765–2768.
  43. Kunert K.J., Vorster B.J., Fenta B. A., Kibido T., Dionisio G., Foyer C.H. 2016. Drought stress responses in soybean roots and nodules. Frontiers in Plant Science, 7(442): 1–7.
  44. Laxa M., Liebthal M., Telman W., Chibani K., Dietz K.-J. 2019. The role of the plant antioxidant system in drought tolerance. Antioxidants (Basel), 8(4): 1–31.
  45. Li R., Liu P., Wan Y., Chen T., Wang Q., Mettbach U., Baluska F., Samaj J., Fang X., Lucas W.J., Lin J. 2012. A membrane microdomain-associated protein, Arabidopsis Flot1, is involved in a clathrin-independent endocytic pathway and is required for seedling development. Plant Cell, 24(5): 2105–2122.
  46. Lingwood D., Simons K. 2010. Lipid rafts as a membraneorganizing principle. Science, 327(5961): 46–50.
  47. Massey K.A., Nicolaou A. 2011. Lipidomics of polyunsaturated-fatty-acid-derived oxygenated metabolites. Biochemical Society Transactions, 39(5): 1240–1246.
  48. Mhamdi A., Van Breusegem F. 2018. Reactive oxygen species in plant development. Development, 145(15): 1–12.
  49. Minibaeva F.V., Hordon L.Kh. 2003. Fiziologiya rasteniy, 50(3): 459–464.
  50. Mittler R. 2002. Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science, 7(9): 405–409.
  51. Mittler R., Vanderauwera S., Gollery M., Van Breusegem F. 2004. Reactive oxygen gene network of plants. Trends in Plant Science, 9: 490–498.
  52. Mittler R., Vanderauwera S., Suzuki N., Miller G., Tognetti V. B., Vandepoele K., Gollery M., Shulaev V., Breusegem F.V. 2011. ROS signaling: the new wave? Trends in Plant Science, 16(6): 300–309.
  53. Mittler R. 2017. ROS are good. Trends in Plant Science, 22(1): 11–19.
  54. Mohammadi M., Karr A.L. 2001. Membrane lipid peroxidation, nitrogen fixation and leghemoglobin content in soybean root nodules. Journal of Plant Physiology, 158(1): 9–19.
  55. Muller B., Pantin F., Génard M., Turc O., Freixes S., Piques M. 2011. Water deficits uncouple growth from photosynthesis, increase C content, and modify the relationships between C and growth in sink organs. Journal of Experimental Botany, 62(6): 1715–29.
  56. Nadeem M., Li J., Yahya M., Sher A., Ma C., Wang X., Qiu L. 2019. Research progress and perspective on drought stress in legumes: A Review. International Journal of Molecular Sciences, 20(10): 2–32.
  57. Nakashima K., Suenaga K. 2017. Toward the genetic improvement of drought tolerance in crops. Japan Agricultural Research Quarterly, 51(1): 1–10.
  58. Negre-Salvayre A., Coatrieux C., Ingueneau C., Salvayre R. 2008. Advanced lipid peroxidation end products in oxidative damage to proteins. Potential role in diseases and therapeutic prospects for the inhibitors. British Journal of Pharmacology, 153(1): 6–20.
  59. Niki E. 2014. Biomarkers of lipid peroxidation in clinical material. Biochimica et Biophysica Acta, 1840(2): 809–817.
  60. Niki E., YoshidaY., Saito Y. 2005. Lipid peroxidation: mechanisms, inhibition, and biological effects. Biochemical and Biophysical Research Communications, 338(1): 668–676.
  61. Niu C.F., Wei W., Zhou Q.Y., Tian A.G., Hao Y.J., Zhang W.K., Ma B., Lin Q., Zhang Z.B., Zhang J.S., Chen S.Y. 2012. Wheat WRKY genes TaWRKY2 and TaWRKY19 regulate abiotic stress tolerance in transgenic Arabidopsis plants. Plant Cell Environ, 35(6): 1156–1170.
  62. Onyango A.N., Baba N. 2010. New hypotheses on the pathways of formation of malondialdehyde and isofurans. Free Radical Biology and Medicine, 49(10): 1594–1600.
  63. Ostapchenko L.I., Synelnyk T.B., Kompanets I.V. 2016. Biolohichni membrany ta osnovy vnutrishnoklitynnoi syhnalizatsii. Teoretychni aspekty: navch. posib. Kyiv: Vyd-vo Kyivskoho universytetu, 639 pp.
  64. Ott T. 2017. Membrane nanodomains and microdomains in plant– microbe interactions. Current Opinion in Plant Biology, 40: 82–88.
  65. Perraki A., Binaghi M., Mecchia M.A., Gronnier J., German-Retana S., Mongrand S., Bayer E., Zelada A.M., Germain V. 2014. StRemorin1.3 hampers Potato virus X TGBp1 ability to increase plasmodesmata permeability, but does not interfere with its silencing suppressor activity. FEBS Letters, 588(9): 1699–1705.
  66. Reis A., Spickett C.M. 2012. Chemistry of phospholipid oxidation. Biochimica et Biophysica Acta, 1818(10): 2374–2387.
  67. Rossard S., Luini E., Pérault J.-M., Bonmort J., Roblin G. 2006. Early changes in membrane permeability, production of oxidative burst and modification of PAL activity induced by ergosterol in cotyledons of Mimosa pudica. Journal of Experimental Botany, 57(6): 1245–1252.
  68. Rucińska R., Gwozdz E.A. 2005. Influence of lead on membrane permeability and lipoxygenase activity in lupine roots. Biologia Plantarum, 49: 617–619.
  69. Sagi M., Fluhr R. 2006. Production of reactive oxygen species by plant NADPH oxidases. Plant Physiology, 141(2): 336–340.
  70. Savicka M., Škute N. 2010. Effects of high temperature on malondialdehyde content, superoxide production and growth changes in wheat seedlings (Triticum aestivum L.). Ekologija, 56(1–2): 26–33.
  71. Schaur R.J. 2003. Basic aspects of the biochemical reactivity of 4-hydroxynonenal. Molecular Aspects of Medicine, 24(4-5): 149–159.
  72. Seifert G.J., Xue H., Acet T. 2014. The Arabidopsis thaliana FASCICLIN LIKE ARABINOGALACTAN PROTEIN 4 gene acts synergistically with abscisic acid signalling to control root growth. Annals of Botany, 114(6): 1125–1133.
  73. Segal L.M., Wilson R.A. 2018. Reactive oxygen species metabolism and plant-fungal interactions. Fungal Genetics and Biology, 110: 1–9.
  74. Sies H. 2017. Hydrogen peroxide as a central redox signaling molecule in physiological oxidative stress: oxidative stress. Redox Biology, 11: 613–619.
  75. Srivastava V., Malm E., Sundqvist G., Bulone V. 2013. Quantitative proteomics reveals that plasma membrane microdomains from poplar cell suspension cultures are enriched in markers of signal transduction, molecular transport, and callose biosynthesis. Molecular and Cellular Proteomics, 12(12): 3874–3885.
  76. Sweeney D.C., Reberšek M., Dermol J., Rems L., Miklavčič D., Davalos R.V. 2016. Quantification of cell membrane permeability induced by monopolar and high-frequency bipolar bursts of electrical pulses. Biochimica et Biophysica Acta (BBA) – Biomembranes, 1858(8): 2689–2698.
  77. Sweeney D.C., Weaver J.C., Davalos R.V. 2018a. Characterization of cell membrane permeability in vitro part I: transport behavior induced by single-pulse electric fields. Technology in Cancer Research & Treatment, 17: 1–15.
  78. Sweeney D.C., Douglas T.A., Davalos R.V. 2018b. Characterization of cell membrane permeability in vitro part II: computational model of electroporationmediated membrane transport. Technology in Cancer Research & Treatment, 17: 1–13.
  79. Takahashi D., Imai H., Kawamura Y., Uemura M. 2016. Lipid profiles of detergent resistant fractions of the plasma membrane in oat and rye in association with cold acclimation and freezing tolerance. Cryobiology, 72(2): 123–134.
  80. Tarchevskyi Y.A. 2002. Plant cell signaling systems. Moscow: Nauka, 294 pp.
  81. Tatari M., Ghazvini R.F., Etemadi N., Ahadi A.M., Mousavi A. 2012. Analysis of antioxidant enzymes activity, lipid peroxidation and proline content of Agropyron desertorum under drought stress. South-Western Journal of Horticulture Biology and Environment, 3(1): 9–24.
  82. Terek O., Reshetylo S., Velychko O., Yavorska N. 2004. Visnyk of Lviv University. Biological series, 37: 218–220.
  83. Tuteja N., Sopory S.K. 2008. Chemical signaling under abiotic stress environment in plants. Plant Signaling & Behavior, 3(8): 525–536.
  84. Venero J.L., Revuelta M., Atiki L. Santiago M., Toms-Camardiel M.C., Cano J., Machado A. 2003. Evidence for dopamine-derived hydroxyl radical formation in the nigrostriatal system in response to axotomy. Free Radical Biology and Medicine, 34(1): 111–123.
  85. Veselov A.P. 2001. Fiziologiya rastenyi, 48(3): 124–131.
  86. Veselov A.P., Kurhanova L.N., Lykhacheva A.V., Sushkova U.A. 2002. Fyzyolohyia rastenyi, 49(3): 385–390.
  87. Vladymyrov Yu.A. 2000. Sorosovskiy obrazovatelnyi zhurnal, 12: 13–19.
  88. Voothuluru P., Anderson J.C., Sharp R.E., Peck S.C. 2016. Plasma membrane proteomics in the maize primary root growth zone: novel insights into root growth adaptation to water stress. Plant Cell and Environment, 39(9): 2043–2054.
  89. Wijewardana C., Alsajri F.A., Irby J.T., Krutz L.J., Golden B., Henry W.B., Gao W., Reddy K.R. 2011. Physiological assessment of water deficit in soybean using midday leaf water potential and spectral features. Functional Plant Biology, 38(6): 523–533.
  90. Xue Q., Zhu Z., Musick J.T., Stevart B.A., Dusek, D.A. 2006. Physiological mechanisms contributing to the increased water-use efficiency in winter wheat under deficit irrigation. Plant Physiology, 162(2): 154–164.
  91. Yin H., Xu L., Porter N.A. 2011. Free radical lipid peroxidation: mechanisms and analysis. Chemical Reviews, 111(10): 5944–5972.
  92. Zamzami N., Maisse C., Métivier D., Kroemer G. 2007. Measurement of membrane permeability and the permeability transition of mitochondria. Methods in Cell Biology, 80: 327–340.
  93. Zhang L., Peng J., Chen T.T., Zhao X.H., Zhang S.P., Liu S.D., Dong H.L., Feng L., Yu S.X. 2014. Effect of drought stress on lipid peroxidation and proline content in cotton roots. Journal of Animal and Plant Sciences, 24(6): 1729–1736 .
  94. Zheng J., Fu J., Gou M., Huai J., Liu Y., Jian M., Huang Q., Guo X., Dong Z., Wang H., Wang G. 2010. Genome-wide transcriptome analysis of two maize inbred lines under drought stress. Plant Molecular Biology, 72(4–5): 407–423.
  95. Zhu J.-K. 2016. Abiotic stress signaling and responses in plants. Cell, 167(2): 313–324.
  96. Zhu S.Y., Zhuang J.S., Wu Q., Liu Z.Y., Liao C.R., Luo S.G., Chen J.T., Zhong Z.M. 2018. Advanced oxidation protein products induce pre-osteoblast apoptosis through a nicotinamide adenine dinucleotide phosphate oxidasedependent, mitogen-activated protein kinases-mediated intrinsic apoptosis pathway. Aging Cell, 17(4): e12764.