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Differential responses of peroxidases in sweetpotato suspension-cultured cells to cadmium treatment

  • Ju Hwan Kim (Department of Pharmacology, College of Medicine, Dankook University) ;
  • Ki Jung Nam (Department of Biology Education, IALS, Gyeongsang National University) ;
  • Kang-Lok Lee (Department of Biology Education, IALS, Gyeongsang National University) ;
  • Yun-Hee Kim (Department of Biology Education, IALS, Gyeongsang National University)
  • Received : 2023.04.19
  • Accepted : 2023.05.08
  • Published : 2023.05.12

Abstract

As cultured plant cells can grow in high oxidative stress conditions, they form an excellent system to study antioxidant mechanisms and the mass production of antioxidants. Oxidative stress is a major cause of damage in plants exposed to various types of environmental stress, including heavy metals, such as cadmium (Cd). Heavy metal accumulation can interfere with many cell functions and plant growth. To evaluate the contribution of oxidative stress to Cd-induced toxicity, cultured sweetpotato (Ipomoea batatas) cells were treated with increasing concentrations of Cd (0, 10, 25, and 50 μM) and cultured further. Cell growth was significantly inhibited by 25 and 50 μM of Cd, and the total protein content increased with 50 μM of Cd. Additionally, the activity of peroxidase (POD) and ascorbate peroxidase (APX), antioxidant enzymes that remove hydrogen peroxide (a reactive oxygen species), increased in the cells after treatment with 50 μM of Cd. The expression analysis of POD, APX, and peroxiredoxin (PRX) isolated from sweetpotato cultured cells in a previous study revealed the differential expression of POD in response to Cd. In this study, the expression levels of several acidic POD (swpa2, swpa3, and swpa4) and basal POD (swpb1, swpb2, and swpb3) genes were increased in Cd-treated cultured cells. These results indicate that Cd-mediated oxidative stress is closely linked to improved POD-mediated antioxidant defense capacity in sweetpotato suspension-cultured cells.

Keywords

Acknowledgement

This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Science, ICT and Future Planning (NRF-2021R1A2C400188711).

References

  1. Asada K (1992) Ascorbate peroxidase - A hydrogen peroxide-scavenging enzyme in plants. Physiol Plant 85:235-241
  2. Asgari Lajayer B, Ghorbanpour M, Nikabadi S (2017) Heavy metals in contaminated environment: destiny of secondary metabolite biosynthesis, oxidative status and phytoextraction in medicinal plants. Ecotoxicol Environ Saf 145:377-390
  3. Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276-287
  4. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254
  5. Cetin ES, Babalik Z, Hallac-Turk F, Gokturk-Baydar N (2014) The effects of cadmium chloride on secondary metabolite production in Vitis vinifera cv. cell suspension cultures. Biological Res 47:47
  6. Chiao WT, Chen BC, Syu CH, Juang KW (2020) Aspects of cultivar variation in physiological traits related to Cd distribution in rice plants with a short-term stress. Bot Stud 61:27
  7. Cosio C, Dunand C (2009) Specific functions of individual class III peroxidase genes. J Exp Bot 60:391-408
  8. Farooq M, Hussain M, Usman M, Farooq S, Alghamdi SS, Siddique HM (2018) Impact of abiotic stresses on grain composition and quality in food legumes. J Agric Food Chem 66:8887-8897
  9. Huh GH, Lee SJ, Bae YS, Liu JR, Kwak SS (1997) Molecular cloning and characterization of cDNAs for anionic and neutral peroxidases from suspension cultured cells of sweetpotato and their differential expression in response to stress. Mol Gen Genet 255:382-391
  10. Jan AT, Azam M, Siddiqui K, Ali A, Choi I, Haq QM (2015) Heavy metals and human health: mechanistic insight into toxicity and counter defense system of antioxidants. Int J Mol Sci 16:29592-29630
  11. Jang IC, Park SY, Kim KY, Kwon SY, Kim GK, Kwak SS (2004). Differential expression of 10 sweetpotato peroxidase genes in response to bacterial pathogen, Pectobacterium chrysanthem. Plant Physiol Biochem 42:451-455
  12. Jung HI, Chae MJ, Kong MS, Kang SS, Kim YH (2016) Effect of rice straw compost on cadmium transfer and metal-ions distribution at different growth stages of soybean. Kor J Soil Sci Fert 49:644-650
  13. Jung HI, Kong MS, Lee EJ, Jung GB, Kim YH (2018) Growth inhibition patterns and bioconcentration profiles in cadmium-stressed oilseed rape (Brassica napus L.). Kor J Soil Sci Fert 51:159-168
  14. Khan A, Khan S, Khan MA, Qamar Z, Waqas M (2015) The uptake and bioaccumulation of heavy metals by food plants, their effects on plants nutrients, and associated health risk: a review. Environ Sci Pollut Res Int 22:13772-13799
  15. Kim KY, Huh GH, Lee HS, Kwon SY, Hur Y, Kwak SS (1999) Molecular characterization of two anionic peroxidase cDNAs isolated from suspension cultures of sweetpotato. Mol Gen Genet 261:941-947
  16. Kim SK, Kwak SS, Jung KH, Min SR, Park IH, Liu JR (1994) Selection of plant cell lines for high yields of peroxidase. Kor Biochem J 27:132-137
  17. Kim YH, Kim Y, Cho E, Kwak S, Kwon S, Bae J, Lee B, Meen B, Huh GH (2004) Alterations in intracellular and extracellular activities of antioxidant enzymes during suspension culture of sweetpotato. Phytochemistry 65:2471-2476
  18. Kim YH, Lee HS, Kwak SS (2010) Differential responses of sweetpotato peroxidases to heavy metals. Chemosphere 81:79-85
  19. Kim YH, Lim S, Han SH, Lee JC, Song WK, Bang JW, Kwon SY, Lee HS, Kwak SS (2007) Differential expression of 10 sweetpotato peroxidases in response to sulfur dioxide, ozone, and ultraviolet radiation. Plant Physiol Biochem 45:908-914
  20. Kwak SS, Kim SK, Lee MS, Jung KH, Park IH, Liu JR (1995) Acidic peroxidase from suspension-cultures of sweet potato. Phytochemistry 39:981-984
  21. Loix C, Huybrechts M, Vangronsveld J, Gielen M, Keunen E, Cuypers A (2017) Reciprocal interactions between cadmium-induced cell wall responses and oxidative stress in plants. Front Plant Sci 8:1867
  22. MacFarlane GR, Burchett MD (2001) Photosynthetic pigments and peroxidase activity as indicators of heavy metal stress in the grey mangrove, Avicennia marina (Forsk.) Vierh. Mar Pollut Bull 42:233-240
  23. Meuwly P, Rauser WE (1992). Alteration of thiol pools in roots and shoots of maize seedlings exposed to cadmium: adaptation and developmental cost. Plant Physiol 99:8-15
  24. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490-498
  25. Mittler R, Zilinskas BA (1994) Regulation of pea cytosolic ascorbate peroxidase and other antioxidant enzymes during the progression of drought stress and following recovery from drought. Plant J 5:397-405
  26. Murashige T, Skoog F (1962) A revised medium for rapid growth and bio-assay with tobacco tissue cultures. Physiol Plant 15:473-497
  27. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867-880
  28. Noctor G, Foyer CH (1998) Ascorbate glutathione: Keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249-279
  29. Park SY, Ryu SH, Kwon SY, Lee HS, Kim GK, Kwak SS (2003) Differential expression of six novel peroxidase cDNAs from cell cultures of sweetpotato on response to stress. Mol Gen Genom 269:542-552
  30. Passardi F, Cosio C, Penel C, Dunand C (2005) Peroxidases have more functions than a swiss army knife. Plant Cell Rep 24:255-265
  31. Peroza EA, Kaabi AA, Meyer-Klaucke W, Wellenreuther G, Freisinger E (2009) The two distinctive metal ion binding domains of the wheat metallothionein Ec-1. J Inorg Biochem 103:342-353
  32. Schutzendubel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351-1365
  33. Shi Z, Cao J, Pang H, Jia L, Sun K, Feng H (2020) Cell viability in the cadmium-stressed cell suspension cultures of tobacco is regulated by extracellular ATP, possibly by a reactive oxygen species-associated mechanism. Biocell 44:89-99
  34. Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, Takeda T, Yabuta Y, Yoshimura K (2002) Regulation and function of ascorbate peroxidase isoenzymes. J Exp Bot 53:1305-1319
  35. Singh S, Parihar P, Singh R, Singh VP, Prasad M (2016). Heavy metal tolerance in plants: role of transcriptomics, proteomics, metabolomics, and ionomics. Front Plant Sci 6:1143
  36. Srivastava RK, Pandey P, Rajpoot R, Rani A, Dubey RS (2014). Cadmium and lead interactive effects on oxidative stress and antioxidative responses in rice. Protoplasma 251:1047-1065
  37. Van Assche F, Clijsters H (1990) Effects of metals on enzyme activity in plants. Plant Cell Environ 13:195-206
  38. You SH, Kim SW, Kim SH, Liu JR, Kwak SS (1996) Selection and isozymes analysis of plant cell lines for high yields of superoxide dismutase. Kor J Plant Tissue Cult 23:103-125