An Investigation into the Effects of Cadmium and Nitric Oxide on Induced Secondary Metabolism and Antioxidant System in Pimpinella anisum L. Through Transcriptional Upregulations in AIS1, PAL, SOD, R2R3-MYB, and bZIP Genes

Document Type : Research Paper

Authors

1 Department of Biology, Damghan Branch, Islamic Azad University, Damghan, Iran

2 Department of Biology, North Tehran Branch, Islamic Azad University, Tehran, Iran

3 Department of Biology, Payame Noor University, Tehran, Iran

4 Department of Biology, Science and Research Branch, Islamic Azad University, Tehran, Iran

Abstract

This study was aimed to evaluate the cytoprotective role of nitric oxide (NO) against cadmium (Cd) through the potential transcriptional modifications in the expression of genes. Pimpinella anisum seedlings were treated with Cd (0 and 1 mM) and/or NO (0 and 25 µM). The Cd-associated decreases in shoot and root biomass were mitigated by the exogenously applied NO. Proline concentrations were increased in response to NO and/or Cd. Cd and NO treatments caused a considerable increase in peroxidase activities in comparison to the control. The individual Cd treatment led to the slight significant (p≤0.001) up-regulation in expression of R2R3-MYB transcription factor by 2.5 folds, while the simultaneous exposure to NO and Cd stimulated this gene by 7.2 folds (p≤0.0001). With a similar trend, NO significantly (p≤0.0001) upregulated bZIP transcription factor by 5.9 folds in Cd-treated seedlings.  Likewise, upregulation (5.2 folds) in the significant (p≤0.0001) increase in expression of the phenylalanine ammonia-lyase (PAL) gene resulted from the NO+Cd application. Moreover, t-anol/isoeugenol synthase 1 (AIS1) gene was slightly stimulated (p≤0.05) in response to individual NO treatment. However, the Cd treatment resulted in a drastic significant (p≤0.0001) increase in AIS1 expression by 42 folds which was partly declined in the Cd+NO group and reached 22 folds (p≤0.0001). Moreover, the NO+Cd treatment caused significant (p≤0.0001) induction in the transcription of the superoxide dismutase (SOD) gene by 11.3 folds.  The correlation observed among expression patterns of mentioned genes, therefore, highlights the close interplay between the transcription factors, secondary metabolism, and antioxidant system.    

Keywords

References

  1. Safari M, Ardebili Z.O, Iranbakhsh A. Selenium nano-particle induced alterations in expression patterns of heat shock factor A4A, HSFA4A., and high molecular weight glutenin subunit 1Bx, Glu-1Bx. and enhanced nitrate reductase activity in wheat (Triticum aestivumL). Acta Physiol Plant. 2018;40:117.
  2. Ali S, Rizwan M, Noureen S, Anwar S, Ali B, Naveed M, Abd_Allah EF, Alqarawi AA, Ahmad P. Combined use of biochar and zinc oxide nanoparticle foliar spray improved the plant growth and decreased the cadmium accumulation in rice, Oryza sativa L. Plant Environ Sci Pollut R. 2019;26:11288-11299.
  3. Babajani A, Iranbakhsh A, Ardebili Z.O, Eslami B. Seed priming with non-thermal plasma modified plant reactions to selenium or zinc oxide nanoparticles, cold plasma as a novel emerging tool for plant science. Plasma Chem. Plasma Process. 2019;39:21-34. 
  4. Bali A, Sidhu GPS, Kumar V, Bhardwaj R. Mitigating cadmium toxicity in plants by phytohormones. In cadmium toxicity and tolerance in plants. Academic Press. 2019;375-396.
  5. Shanmugaraj BM, Malla A, Ramalingam S. Cadmium stress and toxicity in plants, an overview. In Cadmium Toxicity and Tolerance in Plants. Academic Press. 2019;1-17.
  6. Singh S, Prasad SM, Sharma S, Dubey NK, Ramawat N, Prasad R, Singh VP, Tripathi DK, Chauhan DK. Silicon and nitric oxide‐mediated mechanisms of cadmium toxicity alleviation in wheat seedlings. Physiol Plant. 2020.
  7. Corpas FJ. Nitric Oxide and Hydrogen Sulfide in Higher Plants under Physiological and Stress Conditions. Antioxidants. 2019;8;457.
  8. Groß F, Durner J, Gaupels F. Nitric oxide, antioxidants and prooxidants in plant defence responses. Front Plant Sci. 2013;4:419.
  9. Nazerieh H, Aredebili ZO, Iranbakhsh A. Potential benefits and toxicity of nanoselenium and nitric oxide in peppermint. Acta Agric Slov. 2018;111:357-368.
  10. Iranbakhsh A, Ardebili ZO, Molaei H, Ardebili O, Amini M. Cold Plasma Up-Regulated Expressions of WRKY1 Transcription Factor and Genes Involved in Biosynthesis of Cannabinoids in Hemp, Cannabis sativa L. Plasma Chem. Plasma Process. 2020. https,//doi.org/10.1007/s11090-020-10058-2
  11. Majeed S, Nawaz F, Naeem M, Ashraf M.Y. Effect of exogenous nitric oxide on sulfur and nitrate assimilation pathway enzymes in maize. Zea mays L. under drought stress. Acta physiol plant. 2018;40:206.
  12. Shams M, Ekinci M, Ors S, Turan M, Agar G, Kul R, Yildirim E. Nitric oxide mitigates salt stress effects of pepper seedlings by altering nutrient uptake, enzyme activity and osmolyte accumulation. Physiol Mol Biol Plant. 2019;25:1149-1161.
  13. Kaya C, Okant M, Ugurlar F, Alyemeni M.N, Ashraf M, Ahmad P. Melatonin-mediated nitric oxide improves tolerance to cadmium toxicity by reducing oxidative stress in wheat plants. Chemosphere. 2019; 225:627-638
  14. Tripathi K, Mishra, RK, Singh S, Singh S, Singh VP, Singh PK, Chauhan DK, Prasad SM, Dubey NK, Pandey AC. Nitric oxide ameliorates zinc oxide nanoparticles phytotoxicity in wheat seedlings, implication of the ascorbate-glutathione cycle. Front plant sci. 2017;8:1.
  15. Santisree P, Bhatnagar-Mathur P, Sharma K.K. Molecular insights into the functional role of nitric oxide, NO. as a signal for plant responses in chickpea. Func Plant Biol. 2018;45:267-283.
  16. Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L. M.Y.B transcription factors in Arabidopsis. Trend Plant Sci. 2010;15:573-581.
  17. Inne R. The positives and negatives of NPR, a unifying model for salicylic acid signaling in plants. Cell. 2018;173:1314-1315.
  18. Khan M.N, Siddiqui M.H, Mohammad F, Naeem M. Interactive role of nitric oxide and calcium chloride in enhancing tolerance to salt stress. Nitric Oxide. 2012;27:210-8.
  19. Sun W, Shahrajabian MH, Cheng Q. Anise (Pimpinella anisum L.), a dominant spice and traditional medicinal herb for both food and medicinal purposes. Cogent Biol. 2019;5:1673688.
  20. Ahmad P, Ahanger M.A, Alyemeni M.N, Wijaya L, Alam P. Exogenous application of nitric oxide modulates osmolyte metabolism, antioxidants, enzymes of ascorbate-glutathione cycle and promotes growth under cadmium stress in tomato. Protoplasma. 2018;255:79-93.
  21. Dong Y.J, Chen W.F, Liu F.Z, Wan Y.S. Physiological responses of peanut seedlings to exposure to low or high cadmium concentration and the alleviating effect of exogenous nitric oxide to high cadmium concentration stress. Plant Biosystems-An International Journal Dealing with all Aspects of Plant Biology. 2020;154:405-12.
  22. Mostofa MG, Seraj Z.I, Fujita M. Exogenous sodium nitroprusside and glutathione alleviate copper toxicity by reducing copper uptake and oxidative damage in rice (Oryza sativa L.) seedlings. Protoplasma. 2014;251:1373-86.
  23. Basalah M.O, Ali H.M, Al-Whaibi M.H, Siddiqu M.H, Sakran A.M, Al Sahli A. Nitric oxide and salicylic acid mitigate cadmium stress in wheat seedlings. J Pure Appl Microbiol. 2013;7:139-148.
  24. Zha H, Jin Q, Wang Y, Chu L, L X, Xu,Y. Effects of nitric oxide on alleviating cadmium stress in Typha angustifolia. Plant Growth Regul. 2016;78:243-251.
  25. Laspina NV, Groppa MD, Tomaro L, Benavides MP. Nitric oxide protects sunflower leaves against Cd-induced oxidative stress. Plant Science. 2005;169: 323-330.
  26. Xu J, Wang W, Yin H, Liu X, Sun H, Mi Q. Exogenous nitric oxide improves antioxidative capacity and reduces auxin degradation in roots of Medicago truncatula seedlings under cadmium stress. Plant Soil. 2010;326:321.
  27. John R, Ahmad P, Gadgil K, Sharm S. Cadmium and leadinduced changes in lipid peroxidation, antioxidative enzymes and metal accumulation inBrassica junceaL. at three different growth stages. Arch Agron Soil Sci. 2009;55:395-405.
  28. Melo L.C, Alleoni L.R, Carvalho G, Azevedo RA. Cadmium‐and barium‐toxicity effects on growth and antioxidant capacity of soybean (Glycine max L.) plants, grown in two soil types with different physicochemical properties. J Plant Nutr Soil Sci. 2011;174:847-59.
  29. Shan S, Liu F, Li C. Effects of cadmium on growth, oxidative stress and antioxidant enzyme activities in peanut, Arachis hypogaea L. seedlings. J Agric Sci. 2012;4:142-151.
  30. Singh A, Prasad S.M. Effect of agro-industrial waste amendment on Cd uptake inAmaranthus caudatusgrown under contaminated soil, an oxidative biomarker response. Ecotoxicol Environ Saf. 2014;100:105-113.
  31. He J, Ren Y, Chen X, Che H. Protective roles of nitric oxide on seed germination and seedling growth of rice, Oryza sativa L. under cadmium stress. Ecotoxic Environ Safety. 2013;108:114-9.
  32. Wang Q, Liang X, Dong Y, Xu L, Zhang X, Hou J, Fan Z. Effects of exogenous nitric oxide on cadmium toxicity, element contents and antioxidative system in perennial ryegrass. Plant Growth Regul. 2013;69:11-20.
  33. Stracke R, Werber M, Weisshaar B. The R2R3-MYB gene family in Arabidopsis thaliana. Cur Opinion Plant Biol. 2001;4:447-56.
  34. Cao Y, Han Y, Li D, Lin Y, Cai Y. MYB transcription factors in chinese pear (Pyrus bretschneideri Rehd.): genome-wide identification, classification, and expression profiling during fruit development. Front Plant Sci. 2016;7:577.
  35. Chen C, Zhang K, Khurshid M, Li J, He M, Georgiev MI, Zhang X, Zhou M. MYB Transcription Repressors Regulate Plant Secondary Metabolism. Crit Rev Plant Sci. 2019;38:159-70.
  36. Lv Z, Guo Z, Zhang L, Zhang F, Jiang W, Shen Q, Fu X, Yan T, Shi P, Hao X, Ma Y. Interaction of bZIP transcription factor TGA6 with salicylic acid signaling modulates artemisinin biosynthesis in Artemisia annua. J Exp Bot. 2019;70:3969-79.
  37. Han J, Liu H.T, Wang S.C, Wang C.R, Miao G.P. A class I TGA transcription factor from Tripterygium wilfordii Hook. f. modulates the biosynthesis of secondary metabolites in both native and heterologous hosts. Plant Sci. 2020;290:110293.
Journal of Medicinal plants and By-product
Volume 11, Issue 1
April 2022
Pages 129-134

Files

Share

How to cite

Statistics