Photosynthetica 2018, 56(3):811-819 | DOI: 10.1007/s11099-017-0733-0

Effects of salt stress on low molecular antioxidants and redox state of plastoquinone and P700 in Arabidopsis thaliana (glycophyte) and Eutrema salsugineum (halophyte)

M. Wiciarz1, E. Niewiadomska2,*, J. Kruk1
1 Department of Plant Physiology and Biochemistry, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Kraków, Poland
2 The Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków, Poland

The effects of NaCl treatment were analysed in two species of considerably different resistance. In glycophyte, the content of ascorbate decreased but lipophilic antioxidants (α-tocopherol, plastochromanol, and hydroxy-plastochromanol) increased due to 150 mM NaCl. In halophyte, 300 mM NaCl caused a significant increase in hydrophilic antioxidants (ascorbate, total glutathione) but not in the lipophilic antioxidants. The redox states of plastoquinone (PQ) and P700 were also differently modulated by salinity in both species, as illustrated by an increased oxidation of these components in glycophyte. The presented data suggest that E. salsugineum was able to avoid a harmful singlet oxygen production at PSII, which might be, at least in part, attributed to the induction of the ascorbate-glutathione cycle. Another important cue of a high salinity resistance of this species might be the ability to sustain a highly reduced states of PQ pool and P700 under stress, which however, drastically affect the NADPH yield.

Additional key words: chloroplast; oxidative stress; photosystems; salinity

Received: December 28, 2016; Accepted: April 10, 2017; Prepublished online: September 1, 2018; Published: August 1, 2018  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
Wiciarz, M., Niewiadomska, E., & Kruk, J. (2018). Effects of salt stress on low molecular antioxidants and redox state of plastoquinone and P700 in Arabidopsis thaliana (glycophyte) and Eutrema salsugineum (halophyte). Photosynthetica, 56(3), 811-819. doi: 10.1007/s11099-017-0733-0
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    Supplementary files

    Download filephs-201803-0006_S1.pdf

    File size: 117.15 kB

    References

    1. Amor N., Jiménez A., Megdiche W. et al.: Response of antioxidant systems to NaCl stress in the halophyte Cakile maritima.-Physiol. Plantarum 126: 446-457, 2006. Go to original source...
    2. Amtmann A.: Learning from evolution: Thellungiella generates new knowledge on essential and critical components of abiotic stress tolerance in plants.-Mol. Plant. 2: 3-12, 2009. Go to original source...
    3. 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...
    4. Baier M., Dietz K.-J.: Chloroplasts as source and target of cellular redox regulation: a discussion on chloroplast redox signals in the context of plant physiology.-J. Exp. Bot. 56: 1449-1462, 2005. Go to original source...
    5. Baker N.R.: Chlorophyll fluorescence: A probe of photosynthesis in vivo.-Annu. Rev. Plant Biol. 59: 89-113, 2008. Go to original source...
    6. Bilger W., Björkman O.: Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbency changes, fluorescence and photosynthesis in leaves of Hedera canariensis.-Photosynth. Res. 25: 173-185 1990. Go to original source...
    7. Bose J., Rodrigo-Moreno A., Shabala S.: ROS homeostasis in halophytes in the context of salinity stress tolerance.-J. Exp. Bot. 65: 1241-1257, 2014. Go to original source...
    8. Chang C.C., Ball L., Fryer M.J. et al.: Induction of ascorbate peroxidase 2 expression in wounded Arabidopsis leaves does not involve known wound-signalling pathways but is associated with changes in photosynthesis.-Plant J. 38: 499-511, 2004. Go to original source...
    9. Chen H.-X., Gao H.-Y., An S.-Z., Li W.-J.: Dissipation of excess energy in Mehler-peroxidase reaction in Rumex leaves during salt shock.-Photosynthetica 42: 117-122, 2004. Go to original source...
    10. Dassanayake M., Oh D., Hong H. et al.: Transcription strength and halophytic lifestyle.-Trend. Plant Sci. 16: 1-3, 2011. Go to original source...
    11. Degl'Innocenti E., Hafsi C., Guidi L. et al.: The effect of salinity on photosynthetic activity in potassium-deficient barley species.-J. Plant Physiol. 166: 1968-1981, 2009. Go to original source...
    12. Dietzel L., Bräutigam K., Pfannschmidt T.: Photosynthetic acclimation: state transitions and adjustment of photosystem stoichiometry-functional relationships between short-term and long-term light quality acclimation in plants.-FEBS J. 275: 1080-1088, 2008. Go to original source...
    13. Ellouzi H., Hamed K.B., Cela J. et al.: Early effects of salt stress on the physiological and oxidative status of Cakile maritima (halophyte) and Arabidopsis thaliana (glycophyte).-Physiol. Plantarum 142: 128-143, 2011. Go to original source...
    14. Foyer C.H., Noctor G.: Ascorbate and glutathione: the heart of the redox hub.-Plant Physiol. 155: 2-18, 2011. Go to original source...
    15. Foyer C.H., Noctor G.: Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications.-Antioxid. Redox Sign. 11: 861-905, 2009. Go to original source...
    16. Gao F., Zhou Y., Zhu W.: Proteomic analysis of cold stressresponsive proteins in Thellungiella rosette leaves.-Planta 230: 1033-1046, 2009. Go to original source...
    17. Ghars M.A., Richard L., Lefebvre-De Vos D.: Phospholipases C and D modulate proline accumulation in Thellungiella halophila/salsuginea differently according to the severity of salt or hyperosmotic stress.-Plant Cell Physiol. 53: 183-192, 2012. Go to original source...
    18. Gong Q., Li P., Ma S.: Salinity stress adaptation competence in the extremophile Thellungiella halophila in comparison with its relative Arabidopsis thaliana: Salinity stress adaptation in T. halophila.-Plant J. 44: 826-839, 2005. Go to original source...
    19. Gossett D., Millhollon E., Lucas M.: Antioxidant response to NaCl stress in salt-tolerant and salt-sensitive cultivars of cotton.-Plant Cell Rep. 13: 706-714, 1994. Go to original source...
    20. Gruszka J., Pawlak A., Kruk J.: Tocochromanols, plastoquinol and other biological prenyllipids as singlet oxygen quenchers-determination of singlet oxygen quenching rate constants and oxidation products.-Free Radical Biol. Med. 45: 920-928, 2008. Go to original source...
    21. Hebbelmann I., Selinski J., Wehmeyer C. et al.: Multiple strategies to prevent oxidative stress in Arabidopsis plants lacking the malate valve enzyme NADP-malate dehydrogenase.-J. Exp. Bot. 63: 1445-1459, 2012. Go to original source...
    22. Hernández J., Olmos E., Corpas F. et al.: Salt-induced oxidative stress in chloroplasts of pea plants.-Plant Sci. 105: 151-167, 1995. Go to original source...
    23. Johnson G.N.: Physiology of PSI cyclic electron transport in higher plants.-Biochim. Biophys. Acta. 1807: 384-389, 2011. Go to original source...
    24. Khorobrykh S.A., Karonen M., Tyystjärvi E.: Experimental evidence suggesting that H2O2 is produced within the thylakoid membrane in a reaction between plastoquinol and singlet oxygen.-FEBS Lett. 589: 779-786, 2015. Go to original source...
    25. Klughammer C., Schreiber U.: An improved method, using saturating light pulses, for the determination of photosystem I quantum yield via P700+-absorbance changes at 830 nm.-Planta 192: 261-268, 1994. Go to original source...
    26. Kruk J., Karpinski S.: An HPLC-based method of estimation of the total redox state of plastoquinone in chloroplasts, the size of the photochemically active plastoquinone-pool and its redox state in thylakoids of Arabidopsis.-Biochim. Biophys. Acta 1757: 1669-1675, 2006. Go to original source...
    27. Kruk J., Trebst A.: Plastoquinol as a singlet oxygen scavenger in photosystem II.-Biochim. Biophys. Acta 1777: 154-162, 2008. Go to original source...
    28. Kruk J., Szymanska R.: Singlet oxygen and non-photochemical quenching contribute to oxidation of the plastoquinone-pool under high light stress in Arabidopsis.-BBA-Bioenergetics 1817: 705-710, 2012. Go to original source...
    29. Kruk J., Szymanska R., Nowicka B. et al.: Function of isoprenoid quinones and chromanols during oxidative stress in plants.-New Biotechnol. 33: 636-643, 2016. Go to original source...
    30. Lichtenthaler H.K.: Chlorophylls and carotenoids: pigments of photosynthetic biomembranes.-Methods Enzymol. 148: 350-382, 1987. Go to original source...
    31. Lokhande V.H., Srivastava A.K., Srivastava S. et al.: Regulated alterations in redox and energetic status are the key mediators of salinity tolerance in the halophyte Sesuvium portulacastrum (L.) L.-Plant Growth Regul. 65: 287-298, 2011. Go to original source...
    32. Luwe M.W.F., Takahama U., Heber U.: Role of ascorbate in detoxifying ozone in the apoplast of spinach (Spinacia oleracea L.) leaves.-Plant Physiol. 101: 969-976, 1993. Go to original source...
    33. Mittova V., Theodoulou F.L., Kiddle G. et al.: Coordinate induction of glutathione biosynthesis and glutathionemetabolizing enzymes is correlated with salt tolerance in tomato.-FEBS Lett. 554: 417-421, 2003. Go to original source...
    34. M'rah S., Ouerghi Z., Eymery F.: Efficiency of biochemical protection against toxic effects of accumulated salt differentiates Thellungiella halophila from Arabidopsis thaliana.-J. Plant Physiol. 164: 375-384, 2007. Go to original source...
    35. Müller P., Li X.P., Niyogi K.K.: Non-photochemical quenching. A response to excess light energy.-Plant Physiol. 125: 1558-1566, 2001. Go to original source...
    36. Munné-Bosch S.: The role of alpha-tocopherol in plant stress tolerance.-J. Plant Physio. 162: 743-748, 2005. Go to original source...
    37. Munné-Bosch S., Alegre L.: The function of tocopherols and tocotrienols in plants.-Crit. Rev. Plant Sci. 21: 31-57, 2002. Go to original source...
    38. Munns R., Tester M.: Mechanisms of salinity tolerance.-Annu. Rev. Plant Biol. 59: 651-681, 2008. Go to original source...
    39. Murata N., Takahashi S., Nishiyama Y. et al.: Photoinhibition of photosystem II under environmental stress.-BBABioenergetics 1767: 414-421, 2007. Go to original source...
    40. Niewiadomska E., Bilger W., Gruca M. et al.: CAM-related changes in chloroplastic metabolism of Mesembryanthemum crystallinum L.-Planta 233: 275-285, 2011. Go to original source...
    41. Niewiadomska E., Wiciarz M.: Adaptations of chloroplastic metabolism in halophytic plants.-In: Lüttge U., Beyschlag W. (ed.): Progress in Botany. Pp. 177-193. Springer International Publishing Switzerland 2015. Go to original source...
    42. Noctor G.: Metabolic signalling in defence and stress: the central roles of soluble redox couples.-Plant Cell Environ. 29: 409-425, 2006. Go to original source...
    43. Noctor G., Foyer C.H.: Ascorbate and glutathione: keeping active oxygen under control.-Annu. Rev. Plant Phys. 49: 249-279, 1998. Go to original source...
    44. Nowicka B., Kruk J.: Occurrence, biosynthesis and function of isoprenoid quinones.-BBA-Bioenergetics 1797: 1587-1605, 2010. Go to original source...
    45. Ozgur R., Uzilday B., Sekmen A.H. et al.: Reactive oxygen species regulation and antioxidant defence in halophytes.-Funct. Plant Biol. 40: 832-847, 2013. Go to original source...
    46. Pang C.H., Zhang S.J., Gong Z.Z. et al.: NaCl treatment markedly enhances H2O2-scavenging system in leaves of halophyte Suaeda salsa.-Physiol. Plantarum 125: 490-499, 2005. Go to original source...
    47. Peeva V.N., Tóth S.Z., Cornic G., Ducruet J.-M.: Thermoluminescence and P700 redox kinetics as complementary tools to investigate the cyclic/chlororespiratory electron pathways in stress conditions in barley leaves-Physiol. Plantarum 144: 83-97, 2012. Go to original source...
    48. Pfalz J., Liebers M., Hirth M. et al.: Environmental control of plant nuclear gene expression by chloroplast redox signals.-Front. Plant Sci. 3: 257, 2012. Go to original source...
    49. Pfannschmidt T.: Chloroplast redox signals: how photosynthesis controls its own genes.-Trends Plant Sci. 8: 33-41, 2003. Go to original source...
    50. Pfannschmidt T., Bräutigam K., Wagner R. et al.: Potential regulation of gene expression in photosynthetic cells by redox and energy state: approaches towards better understanding.-Ann. Bot.-London 103: 599-607, 2009. Go to original source...
    51. Pilarska M., Wiciarz M., Jajic I. et al.: A different pattern of production and scavenging of reactive oxygen species in halopythic Eutrema salsugineum (Thellungiella salsuginea) plants in comparison to Arabidopsis thaliana and its relation to salt stress signaling.-Front. Plant. Sci. 7: 1179, 2016. Go to original source...
    52. Pospíąil P.: Production of reactive oxygen species by photosystem II.-BBA-Bioenergetics 1787: 1151-1160, 2009. Go to original source...
    53. Puthiyaveetil S., Ibrahim I.M., Allen J.F.: Oxidation-reduction signalling components in regulatory pathways of state transitions and photosystem stoichiometry adjustment in chloroplasts.-Plant Cell Environ. 35: 347-359, 2012. Go to original source...
    54. Sacksteder C.A., Kramer D.M.: Dark-interval relaxation kinetics (DIRK) of absorbance changes as a quantitative probe of steadystate electron transfer.-Photosynth. Res. 66: 145-158, 2000. Go to original source...
    55. Scheibe R., Stitt M.: Comparison of NADP-malate dehydrogenase activation, QA reduction and O2 evolution in spinach leaves.-Plant Physiol. Bioch. 26: 473-481, 1988.
    56. Scheibe R.: Malate valves to balance cellular energy supply.-Physiol. Plantarum 120: 21-26, 2004. Go to original source...
    57. Scheibe R., Backhausen J.E., Emmerlich V. et al.: Strategies to maintain redox homeostasis during photosynthesis under changing conditions.-J. Exp. Bot. 56: 1481-1489, 2005. Go to original source...
    58. Slesak I., Karpinska B., Surówka E. et al.: Redox changes in the chloroplast and hydrogen peroxide are essential for regulation of C(3)-CAM transition and photooxidative stress responses in the facultative CAM plant Mesembryanthemum crystallinum L.-Plant Cell Physiol. 44: 573-581, 2003. Go to original source...
    59. Stepien P., Johnson G.N.: Contrasting responses of photosynthesis to salt stress in the glycophyte Arabidopsis and the halophyte Thellungiella: role of the plastid terminal oxidase as an alternative electron sink.-Plant Physiol. 149: 1154-1165, 2009. Go to original source...
    60. Suzuki N., Koussevitzky S., Mittler R., Miller G.: ROS and redox signalling in the response of plants to abiotic stress.-Plant Cell Environ. 35: 259-270, 2012. Go to original source...
    61. Szymanska R., Kruk J.: Plastoquinol is the main prenyllipid synthesized during acclimation to high light conditions in Arabidopsis and is converted to plastochromanol by tocopherol cyclase.-Plant Cell Physiol. 51: 537-545, 2010. Go to original source...
    62. Szymanska R., Nowicka B., Kruk J.: Hydroxy-plastochromanol and plastoquinone-C as singlet oxygen products during photooxidative stress in Arabidopsis.-Plant Cell Environ. 37: 1464-1473, 2014. Go to original source...
    63. Taji T., Seki M., Satou M. et al.: Comparative genomics in salt tolerance between Arabidopsis and Arabidopsis-related halophyte salt cress using Arabidopsis microarray.-Plant Physiol. 135: 1697-1709, 2004. Go to original source...
    64. Takahama U., Oniki T.: Regulation of peroxidase-dependent oxidation of phenolics in the apoplast of spinach leaves by ascorbate.-Plant Cell Physiol. 33: 379-387, 1992.
    65. Takahashi S., Murata N.: How do environmental stresses accelerate photoinhibition?-Trends Plant Sci. 13: 178-182, 2008. Go to original source...
    66. Takahashi S., Murata N.: Glycerate-3-phosphate, produced by CO2 fixation in the Calvin cycle, is critical for the synthesis of the D1 protein of photosystem II.-Biochim. Biophys. Acta 1757: 198-205, 2006. Go to original source...
    67. Uzilday B., Ozgur R., Sekmen A.H.: Changes in the alternative electron sinks and antioxidant defence in chloroplasts of the extreme halophyte Eutrema parvulum (Thellungiella parvula) under salinity.-Ann. Bot.-London 115: 449-463, 2015. Go to original source...
    68. Vaidyanathan H., Sivakumar P., Chakrabarty R. et al. Scavenging of reactive oxygen species in NaCl-stressed rice (Oryza sativa L.).-differential response in salt-tolerant and sensitive varieties.-Plant Sci. 165: 1411-1418, 2003. Go to original source...
    69. Vinocur B., Altman A.: Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations.-Curr. Opin. Biotech. 16: 123-132, 2005. Go to original source...
    70. Wiciarz M., Gubernator B., Kruk J. et al.: Enhanced chloroplastic generation of H2O2 in stress-resistant Thellungiella salsuginea in comparison to Arabidopsis thaliana.-Physiol. Plantarum 153: 467-476, 2015. Go to original source...

    Return to the content