Plant Soil Environ., 2025, 71(2):136-147 | DOI: 10.17221/309/2024-PSE

Spermidine mitigates wheat copper toxicity by modulating ascorbate and glutathione metabolism, copper accumulation and photosynthetic performanceOriginal Paper

Limin Wu1, Qiumei Zhang2, Ninghai Lu1
1 Henan Institute of Science and Technology, Xinxiang, P.R. China
2 Henan Fengyuan Seed Company Limited, Xinxiang, P.R. China

The influence of spermidine (Spd) on wheat ascorbate and glutathione metabolism, copper (Cu) accumulation and photosynthetic performance under Cu stress was studied. The findings displayed that Cu stress boosted reduced ascorbate (AsA) and reduced glutathione (GSH) contents by improving ascorbate peroxidase (APX), glutathione reductase (GR), dehydroascorbate reductase (DHAR), monodehydroascorbate reductase (MDHAR), L-galactono-1,4-lactone dehydrogenase (GalLDH) and gamma-glutamylcysteine synthetase (γ-ECS) activities. Nevertheless, Cu stress promoted malondialdehyde (MDA) accumulation and electrolyte leakage (EL) level, and lowered AsA/dehydroascorbic acid (DHA) and GSH/oxidised glutathione (GSSG). Meanwhile, Cu stress promoted Cu accumulation in plant tissues. It declined net photosynthetic rate (Pn), chlorophyll fluorescence parameter maximum photochemical efficiency of PSII (Fv/Fm), chlorophyll (Chl) and carotenoids (Car) contents, and wheat height and biomass. In this way, Cu stresses limited wheat growth. Compared with Cu stress, Spd plus Cu stress enhanced APX, GR, DHAR, MDHAR, GalLDH and γ-ECS activities to 4.75, 5.14, 3.77, 2.96, 3.24 and 2.83 U/g FW (fresh weight), respectively. This way, Spd further increased AsA and GSH contents to 4.62 and 0.78 µmol/g FW under Cu stress. Meanwhile, Spd increased AsA/DHA to 14.60 and GSH/GSSG to 15.97 and declined MDA content to 11.68 nmol/g FW and EL to 17.00% under Cu stress. Besides, Spd declined Cu content in leaves to 68.8 µg/g DW and roots to 152.9 µg/g DW and respectively increased Pn, Fv/Fm and Chl and Car contents to 15.22 µmol/m2/s, 0.74, 1.55 mg/g FW and 0.38 mg/g FW. In this way, Spd promoted wheat growth under Cu stress. Meanwhile, we found that Spd alone also improved the ascorbate and glutathione metabolism, photosynthetic performance, and wheat growth compared to the control. These results illustrated that Spd mitigated wheat Cu toxicity by reducing Cu accumulation and improving ascorbate and glutathione metabolism and photosynthetic performance. Hence, using Spd will be a good strategy to improve the Cu tolerance of wheat crops in the future.

Keywords: environmental pollutant; micronutrient; antioxidant metabolism; non-enzymatic antioxidants; Triticum aestivum L.

Received: June 10, 2024; Revised: January 17, 2025; Accepted: January 20, 2025; Prepublished online: February 7, 2025; Published: February 24, 2025  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
Wu L, Zhang Q, Lu N. Spermidine mitigates wheat copper toxicity by modulating ascorbate and glutathione metabolism, copper accumulation and photosynthetic performance. Plant Soil Environ. 2025;71(2):136-147. doi: 10.17221/309/2024-PSE.
Download citation

References

  1. Agami R.A. (2016): Pre-soaking in indole-3-acetic acid or spermidine enhances copper tolerance in wheat seedlings. South African Journal of Botany, 104: 167-174. Go to original source...
  2. Alshegaihi R.M., Saleem M.H., Saleem A., Ali B., Aziz H., Fahad S., Alataway A., Dewidar A.Z., Elansary H.O. (2024): Silicon and titanium dioxide mitigate copper stress in wheat (Triticum aestivum L.) through regulating antioxidant defense mechanisms. Journal of Plant Growth Regulation, 43: 1519-1535. Go to original source...
  3. Aqeel U., Parwez R., Aftab T., Khan M.M.A., Naeem M. (2023): Silicon dioxide nanoparticles suppress copper toxicity in Mentha arvensis L. by adjusting ROS homeostasis and antioxidant defense system and improving essential oil production. Environmental Research, 236: 116851. Go to original source... Go to PubMed...
  4. Castro B., Citterico M., Kimura S., Stevens D.M., Wrzaczek M., Coaker G. (2021): Stress-induced reactive oxygen species compartmentalization, perception and signalling. Nature Plants, 7: 403-412. Go to original source... Go to PubMed...
  5. Fardus J., Hossain S., Rob M.M., Masayuki F. (2023): L-glutamic acid modulates antioxidant defense systems and nutrient homeostasis in lentil (Lens culinaris Medik.) under copper toxicity. Environmental Science and Pollution Research, 30: 78507-78520. Go to original source... Go to PubMed...
  6. Griffith O.W. (1980): Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Analytical Biochem-istry, 106: 207-212. Go to original source... Go to PubMed...
  7. Gaur S., Kumar J., Prasad S.M., Sharma S., Bhat J.A., Sahi S., Singh V.P., Tripathi D.K., Chauhan D.K. (2021): Silicon and nitric oxide interplay alleviates copper induced toxicity in mung bean seedlings. Plant Physiology and Biochemistry, 167: 713-722. Go to original source... Go to PubMed...
  8. Groppa M.D., Tomaro M.L., Benavides M.P. (2007): Polyamines and heavy metal stress: the antioxidant behavior of spermine in cadmium- and copper-treated wheat leaves. Biometals, 20: 185-195. Go to original source... Go to PubMed...
  9. Gong Q., Li Z., Wang L., Zhou J., Kang Q., Niu D. (2021): Gibberellic acid application on biomass, oxidative stress response, and photosynthesis in spinach (Spinacia oleracea L.) seedlings under copper stress. Environmental Science and Pollution Research, 28: 53594-53604. Go to original source... Go to PubMed...
  10. Hodges D.M., Andrews C.J., Johnson D.A., Hamilton R.I. (1996): Antioxidant compound responses to chilling stress in differentially sensitive inbred maize lines. Plant Physiology, 98: 685-692. Go to original source...
  11. Hodges M.D., DeLong J.M., Forney C.F., Prange R.K. (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. Go to original source...
  12. Khafagy M.A., Arafa A.A., EI-Banna M.F. (2009): Glycinebetaine and ascorbic acid can alleviate the harmful effects of NaCl salinity in sweet pep-per. Australian Journal of Crop Science, 3: 257-267.
  13. Li R., Wu L., Shao Y., Hu Q., Zhang H. (2022): Melatonin alleviates copper stress to promote rice seed germination and seedling growth via cross-talk among various defensive response pathways. Plant Physiology and Biochemistry, 179: 65-77. Go to original source... Go to PubMed...
  14. Ogawa K., Hatano-Iwasaki A., Yanagida M., Lwabuchi M. (2004): Level of glutathione is regulated by ATP-dependent ligation of glutamate and cysteine through photosynthesis in Arabidopsis thaliana: mechanism of strong interaction of light intensity with flowering. Plant Cell and Physi-ology, 45: 1-8. Go to original source... Go to PubMed...
  15. Pan L., Huang C., Li R., Li Y. (2024): The bHLH transcription factor PhbHLH121 regulates response to iron deficiency in Petunia hybrida. Plants, 13: 3429. Go to original source... Go to PubMed...
  16. Panfili I., Bartucca M.L., Del Buono D. (2019): The treatment of duckweed with a plant biostimulant or a safener improves the plant capacity to clean water polluted by terbuthylazine. Science of The Total Environment, 646: 832-840. Go to original source... Go to PubMed...
  17. Ramel F., Birtic S., Cuiné S., Triantaphylidès C., Ravanat J.-L., Havaux M. (2012): Chemical quenching of singlet oxygen by carotenoids in plants. Plant Physiology, 158: 1267-1278. Go to original source... Go to PubMed...
  18. Saman M., Sepehri A. (2021): Alleviating effects of Serendipita indica and nitric oxide in proso millet plants (Panicum miliaceum L.) exposed to copper toxicity. Journal of Soil Science and Plant Nutrition, 21: 3065-3075. Go to original source...
  19. Shan C., Liang Z. (2010): Jasmonic acid regulates ascorbate and glutathione metabolism in Agropyron cristatum leaves under water stress. Plant Science, 178: 130-139. Go to original source...
  20. Song Y., Xiang F., Zhang G., Miao Y., Miao C., Song C. (2016): Abscisic acid as an internal integrator of multiple physiological processes modulates leaf senescence onset in Arabidopsis thaliana. Frontiers in Plant Science, 7: 181. Go to original source... Go to PubMed...
  21. Sun M., Li S., Gong Q., Xiao Y., Peng F. (2022): Leucine contributes to copper stress tolerance in peach (Prunus persica) seedlings by enhancing photosynthesis and the antioxidant defense system. Antioxidants, 11: 2455. Go to original source... Go to PubMed...
  22. Sun X., Lv A., Chen D., Zhang Z., Wang X., Zhou A., Xu X., Shao Q., Zheng Y. (2023): Exogenous spermidine enhanced the water deficit tolerance of Anoectochilus roxburghii by modulating plant antioxidant enzymes and polyamine metabolism. Agricultural Water Management, 289: 108538. Go to original source...
  23. Tabata K., Oba K., Suzuki K., Esaka M. (2001): Generation and properties of ascorbic acid-deficient transgenic tobacco cells expressing antisense RNA of L-galactono-1,4-lactone dehydrogenase. Plant Journal, 27: 139-148. Go to original source... Go to PubMed...
  24. Valentovicova K., Haluskova L., Huttova J., Mistrik I., Tamas L. (2010): Effect of cadmium on diaphorase activity and nitric oxide production in barley root tips. Journal of Plant Physiology, 167: 10-14. Go to original source... Go to PubMed...
  25. Wang S.H., Zhang H., He Q.Y. (2011): Effects of copper stress on Medicago sativa seedlings leaf antioxidative system. Chinese Journal of Applied Ecology, 22: 2285-2290.
  26. Wu Z., Wang J., Yan D., Yuan H., Wang Y., He Y., Wang X., Li Z., Mei J., Hu M., Zhou T., Chong S., Zheng B. (2020): Exogenous spermidine improves salt tolerance of pecan-grafted seedlings via activating antioxidant system and inhibiting the enhancement of Na+/K+ ratio. Acta Physi-ologiae Plantarum, 42: 83. Go to original source...
  27. Xu J., Sui C., Ge J., Ren R., Pang Y., Gan H., Du Y., Cao H., Sun Q. (2024): Exogenous spermidine improved the salinity-alkalinity stress tolerance of grapevine (Vitis vinifera) by regulating antioxidant system, Na+/K+ homeostasis and endogenous polyamine contents. Scientia Horticulturae, 326: 112725. Go to original source...
  28. Xu X., Shi G., Ding C., Wu W. (2011): Regulation of exogenous spermidine on the reactive oxygen species level and polyamine metabolism in Alternanthera philoxeroides (Mart.) Griseb under copper stress. Plant Growth Regulation, 63: 251-258. Go to original source...
  29. Yang H.Y., Shi G.X., Li W.L., Wu W.L. (2013): Exogenous spermidine enhances Hydrocharis dubia cadmium tolerance. Russian Journal of Plant Physiology, 60: 770-775. Go to original source...
  30. Yin Z.P., Li S., Ren J., Song X.S. (2014): Role of spermidine and spermine in alleviation of drought-induced oxidative stress and photosynthetic inhibition in Chinese dwarf cherry (Cerasus humilis) seedlings. Plant Growth Regulation, 74: 209-218. Go to original source...
  31. Zai X.M., Fan J.J., Hao Z.P., Liu X.M., Zhang W.X. (2021): Effect of co-inoculation with arbuscular mycorrhizal fungi and phosphate solubilizing fungi on nutrient uptake and photosynthesis of beach palm under salt stress environment. Scientific Reports, 11: 5761. Go to original source... Go to PubMed...
  32. Zeng J., Tang J., Zhang F., Wang Y., Kang H., Chen G., Zhang Z., Yuan S., Zhou Y. (2021): Ammonium regulates redox homeostasis and photosyn-thetic ability to mitigate copper toxicity in wheat seedlings. Ecotoxicology and Environmental Safety, 226: 112825. Go to original source... Go to PubMed...
  33. Zhao X.L., Zhang Y.B., Zhang X.Q., Shan C.J. (2023): Putrescine improves salt tolerance of wheat seedlings by enhancing ascorbate and glutathione metabolism, photosynthetic performance, and ion homeostasis. Plant, Soil and Environment, 69: 512-521. Go to original source...
  34. Zhou Y., Huo S., Wang L., Meng J., Zhang Z., Xi Z. (2018): Exogenous 24-Epibrassinolide alleviates oxidative damage from copper stress in grape (Vitis vinifera L.) cuttings. Plant Physiology and Biochemistry, 130: 555-565. Go to original source... Go to PubMed...

This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International (CC BY NC 4.0), which permits non-comercial use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.