Photosynthetica 2024, 62(4):381-392 | DOI: 10.32615/ps.2024.038

Chloroplast antioxidant reactions associated with zinc-alleviating effects on iron toxicity in wheat seedlings

Y.L. XU, J.Y. GUO, Z. ZHANG, R.R. MA, H. MA, Y. ZHANG, Y.L. YANG
College of Life Science, Northwest Normal University, 730070 Lanzhou, China

This study aimed to explore the mechanism by which Zn retards Fe toxicity by analyzing the morphological, photosynthetic, and chloroplast physiological parameters of wheat seedlings treated with either single or combined Zn and Fe. Different behavior of the seedlings was observed under untreated and treated conditions. The most discriminating quantitative traits were associated with leaf area, biomass dry mass and fresh mass, net photosynthetic rate, intercellular CO2 concentration, stomatal conductance, transpiration rate of seedlings, Hill reaction, Mg2+-ATPase and Ca2+-ATPase activities, malondialdehyde and O2*- contents, and glutathione reductase, ascorbate peroxidase, peroxidase, and superoxide dismutase activities and their gene expression in the seedling chloroplast. The obtained findings suggest the important function of an appropriate Zn concentration in preventing Fe toxicity. Therefore, a thorough evaluation of the effects of Zn on Fe-stressed plant growth is beneficial for sustainable agriculture.

Additional key words: antioxidant reaction; chloroplast; Fe stress; wheat; Zn treatment.

Received: February 29, 2024; Revised: October 30, 2024; Accepted: November 4, 2024; Prepublished online: December 5, 2024; Published: December 19, 2024  Show citation

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XU, Y.L., GUO, J.Y., ZHANG, Z., MA, R.R., MA, H., ZHANG, Y., & YANG, Y.L. (2024). Chloroplast antioxidant reactions associated with zinc-alleviating effects on iron toxicity in wheat seedlings. Photosynthetica62(4), 381-392. doi: 10.32615/ps.2024.038
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References

  1. Adil M.F., Sehar S., Han Z.G. et al.: Zinc alleviates cadmium toxicity by modulating photosynthesis, ROS homeostasis, and cation flux kinetics in rice. - Environ. Pollut. 265: 114979, 2020. Go to original source...
  2. Anjum S.A., Tanveer M., Hussain S. et al.: Osmoregulation and antioxidant production in maize under combined cadmium and arsenic stress. - Environ. Sci. Pollut. Res. 23: 11864-11875, 2016. Go to original source...
  3. Bejaoui F., Salas J.J., Nouairi I. et al.: Changes in chloroplast lipid contents and chloroplast ultrastructure in Sulla carnosa and Sulla coronaria leaves under salt stress. - J. Plant Physiol. 198: 32-38, 2016. Go to original source...
  4. Briat J.-F., Dubos C., Gaymard F.: Iron nutrition, biomass production, and plant product quality. - Trends Plant Sci. 20: 33-40, 2015. Go to original source...
  5. Calgaroto N.S., Cargnelutti D., Rossato L.V. et al.: Zinc alleviates mercury-induced oxidative stress in Pfaffia glomerata (Spreng.) Pedersen. - BioMetals 24: 959-971, 2011. Go to original source...
  6. Cao B.L., Ma Q., Zhao Q. et al.: Effects of silicon on absorbed light allocation, antioxidant enzymes and ultrastructure of chloroplasts in tomato leaves under simulated drought stress. - Sci. Hortic.-Amsterdam 194: 53-62, 2015. Go to original source...
  7. Chatterjee A.K., Mandal B., Mandal L.N.: Interaction of nitrogen and potassium with zinc in submerged soil and lowland rice. - J. Indian Soc. Soil Sci. 44: 792-794, 1996.
  8. Chen H.-C., Zhang S.-L., Wu K.-J. et al.: The effects of exogenous organic acids on the growth, photosynthesis and cellular ultrastructure of Salix variegata Franch. under Cd stress. - Ecotox. Environ. Safe. 187: 109790, 2020. Go to original source...
  9. Ciarkowska A., Ostrowski M., Jakubowska A.: Abiotic stress and phytohormones affect enzymic activity of 1-O-(indole-3-acetyl)-β-D-glucose: myo-inositol indoleacetyl transferase from rice (Oryza sativa). - J. Plant Physiol. 205: 93-96, 2016. Go to original source...
  10. Dai H., Shan C.: Effects of lanthanum on the antioxidant capacity of chloroplasts and chlorophyll fluorescence parameters of maize seedlings under chromium stress. - Photosynthetica 57: 27-31, 2019. Go to original source...
  11. Das S., Biswas A.K.: Comparative study of silicon and selenium to modulate chloroplast pigments levels, Hill activity, photosynthetic parameters and carbohydrate metabolism under arsenic stress in rice seedlings. - Environ Sci. Pollut. Res. 29: 19508-19529, 2022. Go to original source...
  12. Delias D.S., Da-Silva C.J., Martins A.C. et al.: Iron toxicity increases oxidative stress and impairs mineral accumulation and leaf gas exchange in soybean plants during hypoxia. - Environ. Sci. Pollut. Res. 29: 22427-22438, 2022. Go to original source...
  13. Ding F., Wang M., Zhang S.: Overexpression of a Calvin cycle enzyme SBPase improves tolerance to chilling-induced oxidative stress in tomato plants. - Sci. Hortic.-Amsterdam 214: 27-33, 2017. Go to original source...
  14. Du J., Shu S., Shao Q.S. et al.: Mitigative effects of spermidine on photosynthesis and carbon-nitrogen balance of cucumber seedlings under Ca(NO3)2 stress. - J. Plant Res. 129: 79-91, 2016. Go to original source...
  15. Du J., Zeng J., Ming X.Y. et al.: The presence of zinc reduced cadmium uptake and translocation in Cosmos bipinnatus seedlings under cadmium/zinc combined stress. - Plant Physiol. Biochem. 151: 223-232, 2020. Go to original source...
  16. Du W., Yang J.Y., Peng Q.Q. et al.: Comparison study of Zn nanoparticles and Zn sulphate on wheat growth: from toxicity and Zn biofortification. - Chemosphere 227: 109-116, 2019. Go to original source...
  17. Duan Y.P., Zhang Y., Zhao B.: Lead, zinc tolerance mechanism and phytoremediation potential of Alcea rosea (Linn.) Cavan. and Hydrangea macrophylla (Thunb.) Ser. and ethylenediaminetetraacetic acid effect. - Environ. Sci. Pollut. Res. 29: 41329-41343, 2022. Go to original source...
  18. Elbasan F., Arikan B., Ozfidan-Konakci C. et al.: Hesperidin and chlorogenic acid mitigate arsenic-induced oxidative stress via redox regulation, photosystems-related gene expression, and antioxidant efficiency in the chloroplasts of Zea mays. - Plant Physiol. Biochem. 208: 108445, 2024. Go to original source...
  19. Erinle O.K., Jiang Z., Ma B.B. et al.: Exogenous calcium induces tolerance to atrazine stress in Pennisetum seedlings and promotes photosynthetic activity, antioxidant enzymes and psbA gene transcripts. - Ecotox. Environ. Safe. 132: 403-412, 2016. Go to original source...
  20. Fan W.-J., Feng Y.-X., Li Y.-H. et al.: Unraveling genes promoting ROS metabolism in subcellular organelles of Oryza sativa in response to trivalent and hexavalent chromium. - Sci. Total Environ. 744: 140951, 2020. Go to original source...
  21. Feng K., Lu J., Chen Y. et al.: The coordinated alterations in antioxidative enzymes, PeCu/ZnSOD and PeAPX2 expression facilitated in vitro Populus euphratica resistance to salinity stress. - Plant Cell Tiss. Org. Cult. 150: 399-416, 2022. Go to original source...
  22. Fu J., Wang Y.-F., Liu Z.-H. et al.: Trichoderma asperellum alleviates the effects of saline-alkaline stress on maize seedlings via the regulation of photosynthesis and nitrogen metabolism. - Plant Growth Regul. 85: 363-374, 2018. Go to original source...
  23. Gindri R.G., Navarro B.B., da Cruz Dias P.V. et al.: Physiological responses of rice (Oryza sativa L.) oszip7 loss-of-function plants exposed to varying Zn concentrations. - Physiol. Mol. Biol. Pla. 26: 1349-1359, 2020. Go to original source...
  24. Hasanuzzaman M., Hossain M.A., Fujita M. et al.: Exogenous selenium pretreatment protects rapeseed seedlings from cadmium-induced oxidative stress by upregulating antioxidant defense and methylglyoxal detoxification systems. - Biol. Trace Elem. Res. 149: 248-261, 2012. Go to original source...
  25. Hu C.-H., Zheng Y., Tong C.-L., Zhang D.-J.: Effects of exogenous melatonin on plant growth, root hormones and photosynthetic characteristics of trifoliate orange subjected to salt stress. - Plant Growth Regul. 97: 551-558, 2022. Go to original source...
  26. Hu H., Wang L., Li Y. et al.: Insight into mechanism of lanthanum (III) induced damage to plant photosynthesis. - Ecotox. Environ. Safe. 127: 43-50, 2016. Go to original source...
  27. Huang H., Liu X.Q., Qu C.H. et al.: Influences of calcium deficiency and cerium on the conversion efficiency of light energy of spinach. - BioMetals 21: 553-561, 2008. Go to original source...
  28. Kang J.J., Zhao W.Z., Zheng Y. et al.: Calcium chloride improves photosynthesis and water status in the C4 succulent xerophyte Haloxylon ammodendron under water deficit. - Plant Growth Regul. 82: 467-478, 2017. Go to original source...
  29. Kaur N., Sharma I., Kirat K., Pati P.K.: Detection of reactive oxygen species in Oryza sativa L. (rice). - Bio-protocol 6: e2061, 2016. Go to original source...
  30. Kroh G.E., Pilon M.: Regulation of iron homeostasis and use in chloroplasts. - Int. J. Mol. Sci. 21: 3395, 2020. Go to original source...
  31. Krohling C.A., Eutrópio F.J., Bertolazi A.A. et al.: Ecophysiology of iron homeostasis in plants. - Soil Sci. Plant Nutr. 62: 39-47, 2016. Go to original source...
  32. Li M.P., Kim C.H.: Chloroplast ROS and stress signaling. - Plant Commun. 3: 100264, 2022. Go to original source...
  33. Li S.-P., Zeng L.-S., Su Z.-L.: Wheat growth, photosynthesis and physiological characteristics under different soil Zn levels. - J. Integr. Agr. 21: 1927-1940, 2022. Go to original source...
  34. Li X., Ma H., Jia P. et al.: Responses of seedling growth and antioxidant activity to excess iron and copper in Triticum aestivum L. - Ecotox. Environ. Safe. 86: 47-53, 2012. Go to original source...
  35. Ma T., Duan X.H., Yang Y.Y. et al.: Zn-alleviating effects on Fe-induced phytotoxicity in roots of Triticum aestivum. - Biol. Plantarum 61: 733-740, 2017. Go to original source...
  36. Marschner P.: Marschner's Mineral Nutrition of Higher Plants. 3rd Edition. Pp. 672. Academic Press, Amsterdam 2012.
  37. Mateos-Naranjo E., Andrades-Moreno L., Cambrollé J., Perez-Martin A.: Assessing the effect of copper on growth, copper accumulation and physiological responses of grazing species Atriplex halimus: ecotoxicological implications. - Ecotox. Environ. Safe. 90: 136-142, 2013. Go to original source...
  38. Mira M.M., Asmundson B., Renault S. et al.: Suppression of the soybean (Glycine max) Phytoglobin GmPgb1 improves tolerance to iron stress. - Acta Physiol. Plant. 43: 147, 2021. Go to original source...
  39. Müller B.: Iron transport mechanisms and their evolution focusing on chloroplasts. - J. Plant Physiol. 288: 154059, 2023. Go to original source...
  40. Omoto E., Nagao H., Taniguchi M., Miyake H.: Localization of reactive oxygen species and change of antioxidant capacities in mesophyll and bundle sheath chloroplasts of maize under salinity. - Physiol. Plantarum 149: 1-12, 2013. Go to original source...
  41. Romanowska E., Dro¿ak A., Pokorska B. et al.: Organization and activity of photosystems in the mesophyll and bundle sheath chloroplasts of maize. - J. Plant Physiol. 163: 607-618, 2006. Go to original source...
  42. Sarwar N., Ishaq W., Farid G. et al.: Zinc-cadmium interactions: Impact on wheat physiology and mineral acquisition. - Ecotox. Environ. Safe. 122: 528-536, 2015. Go to original source...
  43. Sharma P., Chouhan R., Bakshi P. et al.: Amelioration of chromium-induced oxidative stress by combined treatment of selected plant-growth-promoting rhizobacteria and earthworms via modulating the expression of genes related to reactive oxygen species metabolism in Brassica juncea. - Front. Microbiol. 13: 802512, 2022. Go to original source...
  44. Shu S., Yuan L.-Y., Guo S.-R. et al.: Effects of exogenous spermine on chlorophyll fluorescence, antioxidant system and ultrastructure of chloroplasts in Cucumis sativus L. under salt stress. - Plant Physiol. Biochem. 63: 209-216, 2013. Go to original source...
  45. Tisarum R., Rika R., Pipatsitee P. et al.: Iron (Fe) toxicity, uptake, translocation, and physio-morphological responses in Catharanthus roseus. - Physiol. Mol. Biol. Pla. 29: 1289-1299, 2023. Go to original source...
  46. van Oort P.A.J.: Mapping abiotic stresses for rice in Africa: Drought, cold, iron toxicity, salinity and sodicity. - Field Crop. Res. 219: 55-75, 2018. Go to original source...
  47. Wang G.P., Zhang X.Y., Li F. et al.: Overaccumulation of glycine betaine enhances tolerance to drought and heat stress in wheat leaves in the protection of photosynthesis. - Photosynthetica 48: 117-126, 2010. Go to original source...
  48. Wang J., Zhong X., Zhu K. et al.: Reactive oxygen species, antioxidant enzyme activity, and gene expression patterns in a pair of nearly isogenic lines of nicosulfuron-exposed waxy maize (Zea mays L.). - Environ. Sci. Pollut. Res. 25: 19012-19027, 2018. Go to original source...
  49. Wang J.H., Moeen-ud-din M., Yang S.H.: Dose-dependent responses of Arabidopsis thaliana to Zn are mediated by auxin homeostasis and transport. - Environ. Exp. Bot. 189: 104554, 2021. Go to original source...
  50. Wu C., Dun Y., Zhang Z.J. et al.: Foliar application of selenium and zinc to alleviate wheat (Triticum aestivum L.) cadmium toxicity and uptake from cadmium-contaminated soil. - Ecotox. Environ. Safe. 190: 110091, 2019. Go to original source...
  51. Wu J., Shu S., Li C. et al.: Spermidine-mediated hydrogen peroxide signaling enhances the antioxidant capacity of salt-stressed cucumber roots. - Plant Physiol. Biochem. 128: 152-162, 2018. Go to original source...
  52. Wu X., Liu C., Qu C.X. et al.: Effects of lead on activities of photochemical reaction and key enzymes of carbon assimilation in spinach chloroplast. - Biol. Trace Elem. Res. 126: 269-279, 2008. Go to original source...
  53. Yang H.Y., Shi G.X., Xu Q.S., Wang H.X.: Cadmium effects on mineral nutrition and stress related indices in Potamogeton crispus. - Russ. J. Plant Physiol. 58: 253-260, 2011. Go to original source...
  54. Yang Y.L., Xu Y.L., Li J.M. et al.: [Comparison of photosynthetic characteristics of wheat seedlings under Zn and Fe treatments alone or in combination.] - J. Lanzhou Univ. (Nat. Sci.) 57: 344-352, 2021. [In Chinese]
  55. Zhang C.Y., He Q., Wang M.H. et al.: Exogenous indole acetic acid alleviates Cd toxicity in tea (Camellia sinensis). - Ecotox. Environ. Safe. 190: 110090, 2020a. Go to original source...
  56. Zhang G.-H., Xu Q., Zhu X.-D. et al.: SHALLOT-LIKE1 is a KANADI transcription factor that modulates rice leaf rolling by regulating leaf abaxial cell development. - Plant Cell 21: 719-735, 2009. Go to original source...
  57. Zhang H.H., Li X., Xu Z.S. et al.: Toxic effects of heavy metals Pb and Cd on mulberry (Morus alba L.) seedling leaves: Photosynthetic function and reactive oxygen species (ROS) metabolism responses. - Ecotox. Environ. Safe. 195: 110469, 2020b. Go to original source...
  58. Zhang Z., Chang X.X., Zhang L. et al.: Spermidine application enhances tomato seedling tolerance to salinity-alkalinity stress by modifying chloroplast antioxidant systems. - Russ. J. Plant Physiol. 63: 461-468, 2016. Go to original source...
  59. Zhou Y., Diao M., Cui J.-X. et al.: Exogenous GSH protects tomatoes against salt stress by modulating photosystem II efficiency, absorbed light allocation and H2O2-scavenging system in chloroplasts. - J. Integr. Agr. 17: 2257-2272, 2018. Go to original source...