Journal of Forest and Environmental Science

Institute of Forest Science, kangwon National University (강원대학교 산림과학연구소)
권호 표지
DOI QR코드

DOI QR Code

Alleviating Effects of Nitric Oxide on Cadmium Toxicity in White Poplar (Populus alba)

  • Semsettin Kulac (Department of Forest Engineering, Faculty of Forestry, Duzce University) ;
  • Yakup Cikili (Department of Soil Science and Plant Nutrition, Faculty of Agriculture, Canakkale Onsekiz Mart University) ;
  • Halil Samet (Department of Crop and Animal Production, Izmit Vocational School, Kocaeli University) ;
  • Ertugrul Filiz (Department of Crop and Animal Production, Cilimli Vocational School, Duzce University)
  • Received : 2023.08.23
  • Accepted : 2023.12.21
  • Published : 2024.03.31
Download PDF
⟨ Previous Next ⟩

Abstract

Cadmium (Cd) is non-essential heavy metal that negatively affects plant metabolism. Nitric oxide (NO) is an increasingly important molecule for plant metabolism that makes signaling. In this study, it was aimed to investigate the alleviating effect of sodium nitroprusside (SNP) application as NO donor in white poplar (Populus alba) under Cd stress conditions. SNP and without SNP treatments increased the Cd accumulation in root tissue. While photosynthetic pigments (Chl a, Chl b, Chl a+b, and carotenoid) content decreased by only Cd application, SNP+Cd application decreased the rate of photosynthetic pigments reduction. When the results of Cd and Cd+SNP applications were evaluated for mineral (Fe, Zn, Mn and Cu) uptake, it was found that the positive effect of SNP was heterogeneously affected. Depending on SNP application, it was found that malondialdehyde (MDA) amount decreased in leaf in 100 µM Cd applications while hydrogen peroxide (H2O2) amount decreased in 100 and 500 µM Cd applications. When antioxidant enzyme activities were examined, it was found that catalase (CAT) and ascorbate peroxidase (APX) enzyme activities increased with 100 µM SNP applications under all Cd applications. As a result, it was found that SNP application under Cd stress generally supports physiological processes positively in white poplar, suggesting that NO molecule plays important alleviating roles in plant metabolism.

Keywords

References

  1. Arasimowicz-Jelonek M, Floryszak-Wieczorek J. 2011. Understanding the fate of peroxynitrite in plant cells--from physiology to pathophysiology. Phytochemistry 72: 681-688. https://doi.org/10.1016/j.phytochem.2011.02.025
  2. Barba-Espin G, Diaz-Vivancos P, Job D, Belghazi M, Job C, Hernandez JA. 2011. Understanding the role of H2O2 during pea seed germination: a combined proteomic and hormone profiling approach. Plant Cell Environ 34: 1907-1919. https://doi.org/10.1111/j.1365-3040.2011.02386.x
  3. Beligni MV, Lamattina L. 2001. Nitric oxide: a non-traditional regulator of plant growth. Trends Plant Sci 6: 508-509. https://doi.org/10.1016/S1360-1385(01)02156-2
  4. Bernard A. 2008. Cadmium & its adverse effects on human health. Indian J Med Res 128: 557-564.
  5. Cakmak I, Strbac D, Marschner H. 1993. Activities of hydrogen peroxide-scavenging enzymes in germinating wheat seeds. J Exp Bot 44: 127-132.
  6. Chmielowska-Bak J, Gzyl J, Rucinska-Sobkowiak R, ArasimowiczJelonek M, Deckert J. 2014. The new insights into cadmium sensing. Front Plant Sci 5: 245.
  7. Choudhury FK, Rivero RM, Blumwald E, Mittler R. 2017. Reactive oxygen species, abiotic stress and stress combination. Plant J 90: 856-867. https://doi.org/10.1111/tpj.13299
  8. Cikili Y, Kulac S, Samet H, Filiz E. 2019. Effects of exogenous nitric oxide on cadmium toxicity in black poplar (Populus nigra): physiological approaches. Acta Bot Croat 78: 116-124. https://doi.org/10.2478/botcro-2019-0018
  9. Clemens S. 2006. Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88: 1707-1719. https://doi.org/10.1016/j.biochi.2006.07.003
  10. Dai H, Shan C, Jia G, Lu C, Yang T, Wei A. 2013. Cadmium detoxification in Populus×canescens. Turk J Bot 37: 950-955. https://doi.org/10.3906/bot-1110-9
  11. Das K, Roychoudhury A. 2014. Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Environ Sci 2: 53.
  12. Durand TC, Baillif P, Alberic P, Carpin S, Label P, Hausman JF, Morabito D. 2011. Cadmium and Zinc are differentially distributed in Populus tremula×P. alba exposed to metal excess. Plant Biosyst 145: 397-405. https://doi.org/10.1080/11263504.2011.567787
  13. Emamverdian A, Ding Y, Barker J, Mokhberdoran F, Ramakrishnan M, Liu G, Li Y. 2021. Nitric oxide ameliorates plant metal toxicity by increasing antioxidant capacity and reducing Pb and Cd translocation. Antioxidants (Basel) 10: 1981.
  14. Gallego SM, Pena LB, Barcia RA, Azpilicueta CE, Iannone MF, Rosales EP, Zawoznik MS, Groppa MD, Benavides MP. 2012. Unravelling cadmium toxicity and tolerance in plants: Insight into regulatory mechanisms. Environ Exp Bot 83: 33-46. https://doi.org/10.1016/j.envexpbot.2012.04.006
  15. Gill SS, Hasanuzzaman M, Nahar K, Macovei A, Tuteja N. 2013. Importance of nitric oxide in cadmium stress tolerance in crop plants. Plant Physiol Biochem 63: 254-261. https://doi.org/10.1016/j.plaphy.2012.12.001
  16. Gill SS, Tuteja N. 2010. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48: 909-930.
  17. Gill SS, Tuteja N. 2011. Cadmium stress tolerance in crop plants: probing the role of sulfur. Plant Signal Behav 6: 215-222. https://doi.org/10.4161/psb.6.2.14880
  18. Gross F, Durner J, Gaupels F. 2013. Nitric oxide, antioxidants and prooxidants in plant defence responses. Front Plant Sci 4: 419.
  19. He J, Ma C, Ma Y, Li H, Kang J, Liu T, Polle A, Peng C, Luo ZB. 2013. Cadmium tolerance in six poplar species. Environ Sci Pollut Res Int 20: 163-174. https://doi.org/10.1007/s11356-012-1008-8
  20. Hodges D, DeLong J, Forney C, Prange RK. 1999. Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207: 604-611. https://doi.org/10.1007/s004250050524
  21. Hu Y, Nan Z, Jin C, Wang N, Luo H. 2014. Phytoextraction potential of poplar (Populus alba L. var. pyramidalis Bunge) from calcareous agricultural soils contaminated by cadmium. Int J Phytoremediation 16: 482-495. https://doi.org/10.1080/15226514.2013.798616
  22. Kumar Rai P, Kumar G. 2010. The genotoxic potential of two heavy metals in inbred lines of maize (Zea mays L.). Turk J Bot 34: 39-46.
  23. Leitner M, Vandelle E, Gaupels F, Bellin D, Delledonne M. 2009. NO signals in the haze: nitric oxide signalling in plant defence. Curr Opin Plant Biol 12: 451-458. https://doi.org/10.1016/j.pbi.2009.05.012
  24. Lichtenthaler HK. 1987. Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148: 350-382. https://doi.org/10.1016/0076-6879(87)48036-1
  25. Lux A, Martinka M, Vaculik M, White PJ. 2011. Root responses to cadmium in the rhizosphere: a review. J Exp Bot 62: 21-37. https://doi.org/10.1093/jxb/erq281
  26. Madejon P, Maranon T, Murillo JM, Robinson B. 2004. White poplar (Populus alba) as a biomonitor of trace elements in contaminated riparian forests. Environ Pollut 132: 145-155. https://doi.org/10.1016/j.envpol.2004.03.015
  27. Meng Y, Jing H, Huang J, Shen R, Zhu X. 2022. The role of nitric oxide signaling in plant responses to cadmium stress. Int J Mol Sci 23: 6901.
  28. Miller RO. 1998. High-temperature oxidation: dry ashing. In: Handbook of Reference Methods for Plant Analysis (Kalra YP, ed). CRC Press, Boca Raton, pp 53-56.
  29. Mittler R. 2017. ROS are good. Trends Plant Sci 22: 11-19. https://doi.org/10.1016/j.tplants.2016.08.002
  30. Mukherjee SP, Choudhuri MA. 1983. Implications of water stress-induced changes in the levels of endogenous ascorbic acid and hydrogen peroxide in Vigna seedlings. Physiol Plant 58: 166-170. https://doi.org/10.1111/j.1399-3054.1983.tb04162.x
  31. Nakano Y, Asada K. 1981. Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22: 867-880.
  32. Ovecka M, Takac T. 2014. Managing heavy metal toxicity stress in plants: biological and biotechnological tools. Biotechnol Adv 32: 73-86. https://doi.org/10.1016/j.biotechadv.2013.11.011
  33. Parmar P, Kumari N, Sharma V. 2013. Structural and functional alterations in photosynthetic apparatus of plants under cadmium stress. Bot Stud 54: 45.
  34. Romero-Puertas MC, Corpas FJ, Sandalio LM, Leterrier M, Rodriguez-Serrano M, Del Rio LA, Palma JM. 2006. Glutathione reductase from pea leaves: response to abiotic stress and characterization of the peroxisomal isozyme. New Phytol 170: 43-52. https://doi.org/10.1111/j.1469-8137.2006.01643.x
  35. Siddiqui MH, Al-Whaibi MH, Basalah MO. 2011. Role of nitric oxide in tolerance of plants to abiotic stress. Protoplasma 248: 447-455. https://doi.org/10.1007/s00709-010-0206-9
  36. Terron-Camero LC, Pelaez-Vico MA, Del-Val C, Sandalio LM, Romero-Puertas MC. 2019. Role of nitric oxide in plant responses to heavy metal stress: exogenous application versus endogenous production. J Exp Bot 70: 4477-4488. https://doi.org/10.1093/jxb/erz184
  37. Xiong J, An L, Lu H, Zhu C. 2009. Exogenous nitric oxide enhances cadmium tolerance of rice by increasing pectin and hemicellulose contents in root cell wall. Planta 230: 755-765. https://doi.org/10.1007/s00425-009-0984-5
  38. Xu J, Wang W, Sun J, Zhang Y, Ge Q, Du L, Yin H, Liu X. 2011. Involvement of auxin and nitric oxide in plant Cd-stress responses. Plant Soil 346: 107-119. https://doi.org/10.1007/s11104-011-0800-4
  39. Yang Y, Li X, Yang S, Zhou Y, Dong C, Ren J, Sun X, Yang Y. 2015. Comparative physiological and proteomic analysis reveals the leaf response to cadmium-induced stress in poplar (Populus yunnanensis). PLoS One 10: e0137396.