biologia plantarum

International journal on Plant Life established by Bohumil Němec in 1959

Biologia plantarum 67:45-53, 2023 | DOI: 10.32615/bp.2023.002

The impact of cadmium stress on the ascorbate-glutathione pathway and ascorbate regeneration in tea plants

H.B. WANG1, Y.Q. LIU1, L.L. CHEN1, X.Q. LI1, N.H. HA1, 2, T.X. HOANG2, X.H. LI1, X. CHEN1, *
1 Tea Research Institute, Nanjing Agricultural University, Nanjing 210095, P.R. China
2 Northern Mountainous Agriculture and Forestry Science Institute, Phu Tho 35909, Vietnam

Ascorbic acid (AsA) and glutathione (GSH) contribute to defense responses under abiotic stresses. The present study explored the ascorbate-glutathione cycle and ascorbate regeneration under high concentration (30 mM) of cadmium in the tea plant (Camellia sinensis L.). The tea leaves showed speckles and necrosis from the third day of Cd treatment. The content of superoxide anion (O2.-) and hydrogen peroxide (H2O2) in the leaves were significantly higher until the seventh day after Cd treatment. The content of O2.- and H2O2 were the highest on the fifth day (212.7 and 153.6 % of the control, respectively). The AsA content increased (86.9 %) on the first day after Cd treatment and decreased significantly in the subsequent days, while GSH showed a reverse trend. The enzymatic activity assays showed that dehydroascorbate reductase (DHAR) and glutathione reductase (GR) involved in AsA regeneration were downregulated considerably after Cd foliar application. In contrast, the activities of ascorbate peroxidase (APX) and monodehydroascorbate reductase (MDHAR) increased on the first day and then declined. Reverse-transcription quantitative PCR showed upregulation of glutathione synthetase (CsGSHS), γ-glutamylcysteine synthetase (Csγ-ECS), and CsMDHAR of the AsA regeneration pathway and downregulation of CsDHAR and CsGR. The expressions of GDP-L-galactose phosphorylase (CsGGP), L-galactose-1-phosphate phosphatase (CsGPP), and L-galactono- 1,4-lactone dehydrogenase (CsGaILDH) of the L-galactose pathway were also downregulated. The results indicated that AsA, which can respond to Cd stress of plants by increasing antioxidant ability, was consumed to scavenge ROS; moreover, Cd stress inhibited AsA synthesis and regeneration, which made that tea plants suffering severe damage.

Keywords: AsA-GSH cycle, cadmium stress, Camellia sinensis, gene expression.

Received: September 9, 2022; Revised: February 21, 2023; Accepted: February 27, 2023; Published online: April 10, 2023  Show citation

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WANG, H.B., LIU, Y.Q., CHEN, L.L., LI, X.Q., HA, N.H., HOANG, T.X., LI, X.H., & CHEN, X. (2023). The impact of cadmium stress on the ascorbate-glutathione pathway and ascorbate regeneration in tea plants. Biologia plantarum67, Article 45-53. https://doi.org/10.32615/bp.2023.002
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References

  1. Adamczyk-Szabela D., Lisowska K., Romanowska-Duda Z., Wolf W.M.: Associated effects of cadmium and copper alter the heavy metals uptake by Melissa officinalis. - Molecules 24: 2458, 2019. Go to original source...
  2. Ahammed G.J., Li C.-X., Li X., Liu A., Chen S., Zhou J.: Overexpression of tomato RING E3 ubiquitin ligase gene SlRING1 confers cadmium tolerance by attenuating cadmium accumulation and oxidative stress. - Physiol. Plantarum 173: 449-459, 2021.
  3. Ahmad P., Tripathi D.K., Deshmukh R., Singh V.P., Corpas F.J.: Revisiting the role of ROS and RNS in plants under changing environment. - Environ. Exp. Bot. 161: 1-3, 2019. Go to original source...
  4. Al-Harthi M.M., Bafeel S.O., El-Zohri M.: Gibberellic acid and jasmonic acid improve salt tolerance in summer squash by modulating some physiological parameters symptomatic for oxidative stress and mineral nutrition. - Plants-Basel 10: 2768, 2021. Go to original source...
  5. Bashri G., Prasad S.M.: Exogenous IAA differentially affects growth, oxidative stress and antioxidants system in Cd stressed Trigonella foenum-graecum L. seedlings: toxicity alleviation by up-regulation of ascorbate-glutathione cycle. - Ecotox. Environ. Safe. 132: 329-338, 2016. Go to original source...
  6. Chen Z.X., Lan Q.Y., Zheng L., Bao Y.X., Luo Y.L.: Effects of dehydration and temperature on seed viability and antioxidative enzymes activities on three kinds of cultivars of Camellia sinensis. - Braz. J. Bot. 38: 497-504, 2015. Go to original source...
  7. Dobrikova A., Apostolova E., Adamakis I.-D.S., Hanć A., Sperdouli I., Moustakas M.: Combined impact of excess zinc and cadmium on elemental uptake, leaf anatomy and pigments, antioxidant capacity, and function of photosynthetic apparatus in clary sage (Salvia sclarea L.). - Plants-Basel 11: 2407, 2022. Go to original source...
  8. Elliott H.A., Liberati M.R., Huang C.P.: Competitive adsorption of heavy metals by soils. - J. Environ. Qual. 15: 214-219, 1986. Go to original source...
  9. Emamverdian A., Ding Y.L., Barker J., Mokhberdoran F., Ramakrishnan M., Liu G.H., Li Y.: Nitric oxide ameliorates plant metal toxicity by increasing antioxidant capacity and reducing Pb and Cd translocation. - Antioxidants 10: 1981, 2021. Go to original source...
  10. Eskling M., Arvidsson P.O., Åkerlund H.-E.: The xanthophyll cycle, its regulation and components. - Physiol. Plantarum 100: 806-816, 1997. Go to original source...
  11. Fung K.F., Wong M.H.: Effects of soil pH on the uptake of Al, F and other elements by tea plants. - J. Sci. Food. Agr. 82: 146-152, 2002. Go to original source...
  12. Gajewska E., Owacki R., Mazur J., Skłodowska M.: Differential response of wheat roots to Cu, Ni and Cd treatment, oxidative stress and defense reactions. - Plant Growth Regul. 71: 13-20, 2013. Go to original source...
  13. Genchi G., Sinicropi M.S., Lauria G., Carocci A., Catalano A.: The effects of cadmium toxicity. - Int. J. Environ. Res. Public Health 17: 3782, 2020. Go to original source...
  14. Hartmann T.N., Fricker M.D., Rennenberg H., Meyer A.J.: Cell-specific measurement of cytosolic glutathione in poplar leaves. - Plant Cell Environ. 26: 965-975, 2003. Go to original source...
  15. Hasanuzzaman M., Nahar K., Anee T.I., Fujita M.: Exogenous silicon attenuates cadmium-induced oxidative stress in Brassica napus L. by modulating AsA-GSH pathway and glyoxalase system. - Front. Plant Sci. 8: 1061, 2017. Go to original source...
  16. He Q., Zhou T., Sun J., Wang P., Yang C., Bai L., Liu Z.: Transcriptome profiles of leaves and roots of goldenrain tree (Koelreuteria paniculata Laxm.) in response to cadmium stress. - Int. J. Environ. Res. Public Health 18: 12046, 2021. Go to original source...
  17. Hossain M.A., Nakano Y., Asada K.: Monodehydroascorbate reductase in spinach chloroplasts and its participation in regeneration of ascorbate for scavenging hydrogen peroxide. - Plant Cell Physiol. 25: 385-395, 1984.
  18. Hossain M.N., Sarker U., Raihan M.S., Al-Huqail A.A., Siddiqui M.H., Oba S.: Influence of salinity stress on color parameters, leaf pigmentation, polyphenol and flavonoid contents, and antioxidant activity of Amaranthus lividus leafy vegetables. - Molecules 27: 1821, 2022. Go to original source...
  19. Hou W.H., Xiao C., Song G.L., Wang Q.H., Chang C.C.: Effects of copper and cadmium on heavy metal polluted waterbody restoration by duckweed (Lemna minor). - Plant Physiol. Biochem. 45: 62-69, 2007. Go to original source...
  20. Jakubowska D., Janicka-Russak M., Kabała K., Migocka M., Reda M.: Modification of plasma membrane NADPH oxidase activity in cucumber seedling roots in response to cadmium stress. - Plant Sci. 234: 50-59, 2015. Go to original source...
  21. Kaya C., Akram N.A., Ashraf M., Alyemeni M.N., Ahmad P.: Exogenously supplied silicon (Si) improves cadmium tolerance in pepper (Capsicum annuum L.) by up-regulating the synthesis of nitric oxide and hydrogen sulfide. - J. Biotechnol. 316: 35-45, 2020. Go to original source...
  22. Kohli S.K., Khanna K., Bhardwaj R., Abd Allah E.F., Ahmad P., Corpas F.J.: Assessment of subcellular ROS and NO metabolism in higher plants: multifunctional signaling molecules. - Antioxidants 8: 641, 2019. Go to original source...
  23. Li H., Huang W., Wang G.L., Wang W.L., Cui X., Zhuang J.: Transcriptomic analysis of the biosynthesis, recycling, and distribution of ascorbic acid during leaf development in tea plant (Camellia sinensis (L.) O. Kuntze). - Sci. Rep.-UK 7: 46212, 2017. Go to original source...
  24. Li H., Huang W., Wang G.L., Wu Z.J., Zhuang J.: Expression profile analysis of ascorbic acid-related genes in response to temperature stress in the tea plant, Camellia sinensis (L.) O. Kuntze. - Genet. Mol. Res. 15: 15048756, 2016. Go to original source...
  25. Li X., Wei J.P., Scott E.R., Liu J.W., Guo S., Li Y., Zhang L., Han W.Y.: Exogenous melatonin alleviates cold stress by promoting antioxidant defense and redox homeostasis in Camellia sinensis L. - Molecules 23: 165, 2018. Go to original source...
  26. Manara A., Fasani E., Molesini B., DalCorso G., Pennisi F., Pandolfini T., Furini A.: The tomato metallocarboxypeptidase inhibitor I, which interacts with a heavy metal-associated isoprenylated protein, is implicated in plant response to cadmium. - Molecules 25: 700, 2020. Go to original source...
  27. Morkunas I., Woźniak A., Mai V.C., Rucińska-Sobkowiak R., Jeandet P.: The role of heavy metals in plant response to biotic stress. - Molecules 23: 2320, 2018. Go to original source...
  28. Murtaza G., Javed W., Hussain A., Qadir M., Aslam M.: Soil-applied zinc and copper suppress cadmium uptake and improve the performance of cereals and legumes. - Int. J. Phytoremediat. 19: 199-206, 2017. Go to original source...
  29. Nejatolahi M., Mortazavi S., Ildoromi A.: Levels of Cu, Zn, Pb, and Cd in the leaves of the tea plant (Camellia sinensis) and in the soil of Gilan and Mazandaran farms of Iran. - J. Food Meas. Charact. 8: 277-282, 2014. Go to original source...
  30. Noctor G., Foyer C.H.: Ascorbate and glutathione: keeping active oxygen under control. - Annu. Rev. Plant Physiol. Plant Mol. Biol. 49: 249-279, 1998. Go to original source...
  31. Pető A., Lehotai N., Feigl G., Tugyi N., Ördög A., Gémes K., Tari I., Erdei L., Kolbert Z.: Nitric oxide contributes to copper tolerance by influencing ROS metabolism in Arabidopsis. - Plant Cell Rep. 32: 1913-1923, 2013.
  32. Podwika W., Kleszcz K., Krośniak M., Zagrodzki P.: Copper, manganese, zinc, and cadmium in tea leaves of different types and origin. - Biol. Trace Elem. Res. 183: 389-395, 2018. Go to original source...
  33. Printz B., Lutts S., Hausman J.-F., Sergeant K.: Copper trafficking in plants and its implication on cell wall dynamics. - Front. Plant Sci. 7: 601, 2016. Go to original source...
  34. Qin S.Y., Liu H.G., Nie Z.J., Gao W., Li C., Lin Y.H., Zhao P.: AsA-GSH cycle and antioxidant enzymes play important roles in Cd tolerance of wheat. - Bull. Environ. Contam. Tox. 101: 684-690, 2018. Go to original source...
  35. Sabella E., Luvisi A., Genga A., De Bellis L., Aprile A.: Molecular responses to cadmium exposure in two contrasting durum wheat genotypes. - Int. J. Mol. Sci. 22: 7343, 2021. Go to original source...
  36. Sarker U., Oba S.: Catalase, superoxide dismutase and ascorbate-glutathione cycle enzymes confer drought tolerance of Amaranthus tricolor. - Sci. Rep.-UK 8: 16496, 2018a. Go to original source...
  37. Sarker U., Oba S.: Drought stress effects on growth, ROS markers, compatible solutes, phenolics, flavonoids, and antioxidant activity in Amaranthus tricolor. - Appl. Biochem. Biotech. 186: 999-1016, 2018b. Go to original source...
  38. Sarker U., Oba S.: The response of salinity stress-induced A. tricolor to growth, anatomy, physiology, non-enzymatic and enzymatic antioxidants. - Front. Plant Sci. 11: 559876, 2020. Go to original source...
  39. Shan C., Zhang S., Ou X.: The roles of H2S and H2O2 in regulating AsA-GSH cycle in the leaves of wheat seedlings under drought stress. - Protoplasma 255: 1257-1262, 2018. Go to original source...
  40. Subba P., Mukhopadhyay M., Mahato S.K., Bhutia K.D., Mondal K.M., Ghosh S.K.: Zinc stress induces physiological, ultra-structural, and biochemical changes in mandarin orange (Citrus reticulata Blanco) seedlings. - Physiol. Mol. Biol. Pla. 20: 461-473, 2014. Go to original source...
  41. Tao J.J., Wu H., Li Z.Y., Huang C.H., Xu X.B.: Molecular evolution of GDP-D-mannose epimerase (GME), a key gene in plant ascorbic acid biosynthesis. - Front. Plant Sci. 9: 1293, 2018. Go to original source...
  42. Thounaojam T.C., Panda P., Mazumdar P., Kumar D., Sharma G.D., Sahoo L., Panda S.: Excess copper induced oxidative stress and response of antioxidants in rice. - Plant Physiol. Biochem. 53: 33-39, 2012. Go to original source...
  43. Tian S., Lu L., Zhang J., Wang K., Brown P., He Z., Liang J., Yang X.: Calcium protects roots of Sedum alfredii H. against cadmium-induced oxidative stress. - Chemosphere 84: 63-69, 2011. Go to original source...
  44. Wingate V.P.M., Lawton M.A., Lamb C.J.: Glutathione causes a massive and selective induction of plant defense genes. - Plant Physiol. 87: 206-210, 1988. Go to original source...
  45. Yan Y.-Y., Wang J.-J., Lan X.-Y., Wang Q.-M., Xu F.-L.: Comparisons of cadmium bioaccumulation potentials and resistance physiology of Microsorum pteropus and Echinodorus grisebachii. - Environ. Sci. Pollut. Res. 25: 12507-12514, 2018. Go to original source...
  46. Zengin F.K., Munzuroglu O.: Effects of some heavy metals on content of chlorophyll, proline and some antioxidant chemicals in bean (Phaseolus vulgaris L.) seedlings. - Acta Biol. Cracov. Bot. 47: 157-164, 2005.
  47. Zhang P., Liu L., Wang X., Wang Z., Zhang H., Chen J., Liu X., Wang Y., Li C.: Beneficial effects of exogenous melatonin on overcoming salt stress in sugar beets (Beta vulgaris L.). - sPlants-Basel 10: 886, 2021. Go to original source...