biologia plantarum

International journal on Plant Life established by Bohumil Nìmec in 1959

Biologia plantarum 63:113-121, 2019 | DOI: 10.32615/bp.2019.014

Implication of peroxisomes and mitochondria in the halophyte Cakile maritima tolerance to salinity stress

N. Ben Amor1,*, A. Jimenez2, M. Boudabbous3, F. Sevilla2, C. Abdelly1
1 Laboratory of Plant Extremophiles, Biotechnology Center, 2050 Borj Cédria, Tunisia
2 Department of Stress Biology and Plant Pathology, CEBAS-CSIC, 30100 Murcia, Spain
3 Laboratory of Molecular Biotechnology of Eukaryotes, CBS, 3018 Sfax, Tunisia

The role of mitochondria and peroxisomes in the tolerance of the halophyte Cakile martima to salt stress was studied. The plants were subjected to 0, 100, and 200 mM NaCl for 5 weeks. The evaluation of oxidative stress according to the content of malondialdehyde (MDA), carbonyl (CO-) proteins, O2-, and H2O2, and the activities of several antioxidant enzymes, such as superoxide dismutase, peroxidase, and enzymes of the ascorbate-glutathione cycle were determined in two purified organelles, mitochondria and peroxisomes. The intact organelles were purified by centrifugation in Percoll density gradients. Results show that the content of MDA and CO- proteins was higher in mitochondria than in peroxisomes under the salt stress. The antioxidant enzymes showed higher activities in peroxisomes than in mitochondria under different NaCl concentrations. These activities were highest at 100 mM NaCl. Our results suggest that the ascorbate glutathione cycle in peroxisomes plays a key role in the tolerance of Cakile maritima to salinity.

Keywords: ascorbate-glutathione cycle, carbonyl proteins, H2O2, malondialdehyde, NaCl, O2-, peroxidase, superoxide dismutase

Accepted: November 15, 2018; Prepublished online: November 15, 2018; Published online: January 19, 2019  Show citation

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Ben Amor, N., Jimenez, A., Boudabbous, M., Sevilla, F., & Abdelly, C. (2019). Implication of peroxisomes and mitochondria in the halophyte Cakile maritima tolerance to salinity stress. Biologia plantarum, 63, Article 113-121. https://doi.org/10.32615/bp.2019.014
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    References

    1. Aebi, H.: Catalase in vitro. - Methods Enzymol. 105: 121-126, 1984. Go to original source...
    2. Apel, K., Hirt, H.: Reactive oxygen species: metabolism, oxidative stress, and signal transduction. - Annu. Rev. Plant Biol. 55: 373-399, 2004. Go to original source...
    3. Arrigoni, O., Dipierro, S., Borraccino, G.: Ascorbate free radical reductase: a key enzyme of the ascorbic acid system. - FEBS Lett. 125: 242-244, 1981. Go to original source...
    4. Asada, K.: The water-water cycle in chloroplasts: scavenging of active oxygen and dissipation of excess photons. - Annu. Rev. Plant Physiol. Plant mol. Biol. 50: 601-639, 1999. Go to original source...
    5. Asada, K.: The water-water cycle as alternative photon and electron sinks. Philosophical Transactions of the Royal Society of London, Series B. Biological Sciences. 355: 1419-1431, 2000. Go to original source...
    6. Ashraf, M.: Biotechnological approach of improving plant salt tolerance using antioxidants as markers. - Biotech. Adv. 27: 84-93, 2009. Go to original source...
    7. Ben Amor, N., Ben Hamed, K., Debez, A., Grignon, G., Abdelly, C.: Physiological and antioxidant responses of the perennial halophyte Crithmum maritimum to salinity.- Plant Sci. 168: 889-899, 2005. Go to original source...
    8. Ben Amor, N., Jiménez, A., Megdiche, W., Lundqvist, M., Sevilla, F., Abdelly, C.: Response of antioxidant systems to NaCl stress in the halophyte Cakile maritima. - Physiol. Plant. 126: 446-457, 2006. Go to original source...
    9. Ben Amor, N., Megdiche, W., Jiménez, A., Sevilla, F., Abdelly, C.: The effect of calcium on the antioxidant systems in the halophyte Cakile maritima under salt stress. - Acta Physiol. Plant. 32: 453-461, 2010. Go to original source...
    10. Bergmeyer, H.U., Gawwehn, K., Grassl, M.: Enzymes as biochemical reagents. - In Bergmeyer, H.U. (ed.): Methods of Enzymatic Analysis. Pp. 425-556. Academic Press, New York 1974.
    11. Boveris, A.: Determination of the production of superoxide radicals and hydrogen peroxide in mitochondria. -Methods Enzymol. 105: 429-435, 1984. Go to original source...
    12. Bradford, M.M.: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. - Anal. Biochem. 72: 248-254, 1976. Go to original source...
    13. Buege, A.J., Aust, S.D.: Microsomal lipid peroxidation. - Method Enzymol. 52: 302-310, 1972. Go to original source...
    14. Corpas, F.J.: What is the role of hydrogen peroxide in plant peroxisomes?. - Plant Biol. 17: 1099-1103, 2015. Go to original source...
    15. Corpas, F.J., Gomez, M., Hernández, J.A., Del Río, L.A.: Metabolism of activated oxygen in peroxisomes from two Pisum sativum L. cultivars with different sensitivity to sodium chloride. - J. Plant Physiol. 89: 103-110, 1993b. Go to original source...
    16. Corpas, F.J., Palma, J.M., Del Río, L.A.: Evidence for the presence of proteolytic activity in peroxisomes. - Eur. J. cell. Biol. 61: 81-85, 1993a.
    17. Dalton, D.A., Baird, L.M., Langeberg, L., Taugher, C.Y., Anyan, W.R., Vance, C.P., Sarath, G.: Subcellular localization of oxygen defense enzymes in soybean (Glycine max [L.] Merr.) root nodules. - Plant Physiol. 102: 481-489, 1993. Go to original source...
    18. Debez, A., Ben Hamed, K., Grignon, C., Abdelly, C.: Salinity effects on germination, growth, and seed production of the halophyte Cakile maritima. - Plant Soil 262: 179-189, 2004. Go to original source...
    19. Debez, A., Braun, H., Pich, A, Taamalli, W., Koyro, H., Abdelly, C., Huchzermeyer, B.: Proteomic and physiological responses of the halophyte Cakile maritima to moderate salinity at the germinative and vegetative stages. - J. Proteomics 75: 5667-5694, 2012. Go to original source...
    20. Del Río, L.A., Corpas, F.J., Sandalio, L.M., Palma, J.M., Gómez, M., Barroso, J.B.: Reactive oxygen species, antioxidant systems and nitric oxide in peroxisomes - J. exp. Bot. 53: 1255-1272, 2002. Go to original source...
    21. Del Río, L.A., Sandalio, L.M., Corpas, F.J., Palma, J.M., Barroso, J.B.: Reactive oxygen species and reactive nitrogen species in peroxisomes. Production, scavenging, and role in cell signaling. - Plant Physiol. 141: 330-335, 2006. Go to original source...
    22. Del Río, L.A., Sandalio, L.M., Palma, J.M., Bueno, P., Corpas, F.J.: Metabolism of oxygen radicals in peroxisomes and cellular implications. - Free Radical Biol. Med. 13: 557-580, 1992. Go to original source...
    23. Demidchik, V.: Mechanisms of oxidative stress in plants: from classical chemistry to cell biology. - Environ. exp. Bot. 109: 212-228, 2015. Go to original source...
    24. Doehlert, D.C., Kuo, T.M., Felker, F.C.: Enzymes of sucrose and hexose metabolism in developing kernels of two inbreeds of maize. - Plant Physiol. 81: 511-515, 1988. Go to original source...
    25. Edwards, E.A., Rawsthorne, S., Mullineaux, P.M.: Subcellular distribution of multiple forms of glutathione reductase in leaves of pea (Pisum sativum L.). - Planta. 180: 278-284, 1990. Go to original source...
    26. Foyer, C.H., Lopez-Delgado, H., Dat, J.E., Scott, I.M.: Hydrogen peroxide- and glutathione-associated mechanisms of acclamatory stress tolerance and signalling. - Physiol. Plant. 100: 241-254, 1997. Go to original source...
    27. Foyer, C.H., Noctor, G.: Redox sensing and signaling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. - Physiol. Plant. 119: 355-364, 2003. Go to original source...
    28. Frew, J., Jones, P., Scholes, G.: Spectrophotometric determination of hydrogen peroxide and organic hydroperoxides at low concentrations in aqueous solution. - Anal. chim. Acta 155: 130-150, 1983. Go to original source...
    29. Gill, S.S., Tuteja, N.: Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. - Plant Physiol. Biochem. 48: 909-930, 2010. Go to original source...
    30. Gomez, J.M., Hernández, J.A., Jimènez, A., Del Río, L.A., Sevilla, F.: Differential response of antioxidative enzymes of chloroplasts and mitochnodria to long-term NaCl stress of Pea plants. - Free Rad. Res. 31: 11-18, 1999. Go to original source...
    31. Gomez, S.M., Kalamani, A.: Butterfly Pea (Clitoria ternatea): A nutritive multipurpose forage legume for the tropics - An overview. - Pakistan J. Nutrition. 2: 374-379. 2003. Go to original source...
    32. Hernández, J.A., Corpas, F.J., Gómez, M., Del Río L.A., Sevilla, F.: Salt induced oxidative stress mediated by activated oxygen species in pea leaf mitochondria. - Physiol. Plant. 89: 103-108, 1993. Go to original source...
    33. Hewitt, E.J.: Sand and Water Culture Methods Used in the Study of Plant Nutrition. - Commonwealth Bureau of Horticulture, East Malling 1966.
    34. Igamberdiev, A.U., Lea, P.J.: The role of peroxisomes in the integration of metabolism and evolutionary diversity of photosynthetic organisms. - Biochemistry 60: 651-674, 2002. Go to original source...
    35. Hu, J., Baker, A., Bartel, B., Linka, N., Mullen, R.T., Reumann, S., Zolman, B.K.: Plant Peroxisomes: Biogenesis and Function. - Plant Cell. 24: 2279-2303, 2012. Go to original source...
    36. Jimènez, A., Hernandez, J.A., Del Rio, L., Sevilla, F.: Role of the ascorbate-glutathione cycle of mitochondria and peroxisomes in the senescence of pea leaves. - Plant Physiol. 118: 1327-1335, 1998. Go to original source...
    37. Jimènez, A., Hernandez, J.A., Del Río, L.A., Sevilla, F.: Evidence for the presence of the ascorbate-glutathione cycle in mitochondria and peroxisomes of pea leaves. - Plant Physiol. 114: 275-284, 1997. Go to original source...
    38. Jithesh, M.N., Prashanth, S.R., Sivaprakash, K.R., Ajay, K., Parida, A.K.: Antioxidative response mechanisms in halophytes: their role in stress defence. - J. Genet. 85: 237-254. 2006. Go to original source...
    39. Karkonen, A., Kuchitsu, K.: Reactive oxygen species in cell wall metabolism and development in plants. - Phytochemistry 112: 22-32. 2015. Go to original source...
    40. Kleczkowski, A., Edwards, E.: Identification of hydroxypyruvate and glyoxylate reductases in maize leaves. - Plant Physiol. 91: 278-286. 1989. Go to original source...
    41. Kuzniak, E., Sk³odowska, M.: Fungal pathogen-induced changes in the antioxidant systems of leaf peroxisomes from infected tomato plants. - Planta. 222: 192-200, 2005. Go to original source...
    42. Levine, R.L., Garland, D., Oliver, C.N., Amici, A., Climent, I., Lens, A.G., Ahn, B.W., Shaltiel, S., Stadtman, E.R.: Determination of carbonyl content in oxidatively modified proteins. - Methods Enzymol. 186: 464-478, 1990. Go to original source...
    43. Lokhande, V.H., Suprasanna, P.: Prospects of halophytes in understanding and managing abiotic stress tolerance. - In: Ahmad, P. (ed.: Environal Adaptations and Stress Tolerance of Plants in the Era of Climate Change. Pp. 29-56. Springer, Berlin 2012. Go to original source...
    44. McCord, J.M., Fridovich, I.: Superoxide dismutase: an enzymatic function for erythrocuprein. - Int. J. Biochem. cell. Biol. 244: 6049-6055, 1969. Go to original source...
    45. Mittler, R.: Oxidative stress, antioxidants and stress tolerance. - Trends Plant Sci. 7: 405-410, 2002. Go to original source...
    46. Mittova, V., Tal, M., Volokita, M., Guy, M.: Up-regulation 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. 26: 845-856, 2003. Go to original source...
    47. Mittova, V., Volokita, M., Guy, M., Tal, M.: Activities of SOD and the ascorbate-glutathione cycle enzymes in subcellular compartments in leaves and roots of the cultivated tomato and its wild salt tolerant relative Lycopersicon pennellii. - Physiol. Plant. 110: 42-51, 2000. Go to original source...
    48. Mittova, V., Volokita, M., Guy, M., Tal, M., Volokita, M.: Salinity up-regulates the antioxidative system in root mitochondria and peroxisomes of the wild salt-tolerant tomato species Lycopersicon pennellii. - J. exp. Bot. 55: 1105-1113, 2004. Go to original source...
    49. Moller, I.M.: 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, 2001. Go to original source...
    50. Ranieri, A., Petacco, F., Castagna, A., Soldatini, G.F.: Redox state and peroxidase system in sunflower plants exposed to ozone. - Plant Sci. 159: 159-168, 2000. Go to original source...
    51. Rodriguez-Serrano, M., Romero-Puertas, M.C., Pazmino, D.M., Testillano, P.S., Risueno, M.C., Del Río L.A., Sandalio, L.M.: Cellular response of pea plants to cadmium toxicity: cross talk between reactive oxygen species, nitric oxide, and calcium. - Plant Physiol. 150: 229-243, 2009. Go to original source...
    52. Sairam, R.K., Srivastava, G.C.: Changes in antioxidant activity in sub-cellular fractions of tolerant and susceptible wheat genotypes in response to long-term salt stress. - Plant Sci. 162: 897-904, 2002. Go to original source...
    53. Serrano, R., Mulet, J.M., Rios, G., Marquez, J.A., De Larrinoa, I.F., Leube, M.P., Iratxe, M., Amparo, P.A., Markus, P., Roc, R., Consuelo, M.: A glimpse of the mechanisms of ion homeostasis during salt stress. - J. exp. Bot. 50: 1023-1036, 1999. Go to original source...
    54. Sevilla, F., Jimènez, A., Lazaro, J.J.: What do the plant mitochondrial antioxidant and redox systems have to say under salinity, drought, and extreme temperature? - In: Gupta, D.K., Palma, J.M., Corpos, F.J. (ed.): Reactive Oxygen Species and Oxidative Damage in Plants Under Stress. Pp. 23-55. Springer, Dordrecht 2015. Go to original source...
    55. Smirnoff, N.: The role of active oxygen in the response of plants to water deficit and desiccation. - New Phytol. 125: 27-58, 1993. Go to original source...
    56. Torrecillas, A., Léon, A., Del Amor, F., Martinez-Mompean, M.C.: Rapid determination of chlorophyll. - Fruits 39: 617-622, 1984.
    57. Zarrouk, M., El Almi, H., Ben Youssef, N., Sleimi, N., Smaoui, A., Ben Miled, D.: Lipid composition of local halophytes seeds: Cakile maritima, Zygophyllum album and Crithmum maritimum. - In: Lieth, H, (ed.): Cash Crop Halophytes: Recent Studies. Pp. 121-126. Kluwer Academic Publishers, Dordrecht 2003. Go to original source...

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