Journal of Plant Growth Regulation

, Volume 38, Issue 2, pp 701–712 | Cite as

Application of Brassinosteroid Mimetics Improves Growth and Tolerance of Maize to Nicosulfuron Toxicity

  • Shaojin Liu
  • Yan He
  • Hao Tian
  • Chunxin Yu
  • Weiming Tan
  • Zhaohu Li
  • Liusheng DuanEmail author


Pesticide residues, especially for herbicides, often damage crops, except for weeds, which results in reduced production or even death in agriculture. Brassinosteroids (BRs) can alleviate the injury from pesticide stress and enhance the growth of plants. However, the roles of low-cost BR mimetics in alleviation and protection from herbicide (nicosulfuron, NSF) stress in maize remain unclear. To investigate the effects of brassinosteroid mimetics on the growth of NSF-stressed plants, we treated maize seedlings with bikinin and brazide at 10 µM prior to NSF treatment, and epibrassinolide (EBL) as a positive control. The NSF treatment dramatically reduced the height, root length, and biomass of maize, and significantly influenced photosynthetic activity and pigments. Accumulation of reactive oxygen species (ROS) and membrane lipid peroxidation, enhanced activity of antioxidant, and detoxification-related enzymes were also observed under NSF stress. As compared to NSF-induced plants, foliar application of bikinin and brazide significantly increased biomass, photosynthesis, and antioxidant enzymes activities and decreased the ROS levels by more than 32.3%, the similar effects as EBL. The glutathione content genes (GST1, ABC-2, ALS1) involved in detoxification in the BR mimetics + NSF-treated plants were higher than those of NSF alone. Reduced levels of NSF residues by more than 55% after 3 days were observed as a result of BR mimetics pretreatment. In summary, our results present a new pattern of roles of BR mimetics, which display the potential protection of plants under pesticide stress.


Bikinin Brazide Herbicide stress Maize Nicosulfuron detoxification 



We are very thankful to Prof. Lizhen Zhang for helpful comments on the manuscript. The study was funded by the China National Science Fund for Distinguished Young Scholars (Grant 31425017 to L.D.).

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no competing interests.


  1. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126. CrossRefGoogle Scholar
  2. Ahammed GJ, Choudhary SP, Chen S, Xia X, Shi K, Zhou Y, Yu J (2013) Role of brassinosteroids in alleviation of phenanthrene-cadmium co-contamination-induced photosynthetic inhibition and oxidative stress in tomato. J Exp Bot 64:199–213. CrossRefPubMedGoogle Scholar
  3. AOAC Official Method 2007.01 (2007) Pesticide residues in foods by acetonitrile extraction and partitioning with magnesium sulfate, gas chromatography/mass spectrometry and liquid chromatography/ tandem mass spectrometry. AOAC IntGoogle Scholar
  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. 1976.9999CrossRefGoogle Scholar
  5. Brennan T, Frenkel C (1977) Involvement of hydrogen peroxide in the regulation of senescence in pear. Plant Physiol 59:411–416CrossRefPubMedPubMedCentralGoogle Scholar
  6. Carey JB, Penner D, Kells JJ (1997) Physiological basis for nicosulfuron and primisulfuron selectivity in five plant species. Weed Sci 45:22–30CrossRefGoogle Scholar
  7. Chew O, Whelan J, Millar AH (2003) Molecular definition of the ascorbate-glutathione cycle in Arabidopsis mitochondria reveals dual targeting of antioxidant defenses in plants. J Biol Chem 278:46869–46877. CrossRefPubMedGoogle Scholar
  8. Clouse SD, Sasse JM (1998) Brassinosteroids: Essential regulators of plant growth and development. Annu Rev Plant Physiol Plant Mol Biol 49:427–451. CrossRefPubMedGoogle Scholar
  9. Cui J et al (2011) Role of nitric oxide in hydrogen peroxide-dependent induction of abiotic stress tolerance by brassinosteroids in cucumber. Plant Cell Environ 34:347–358CrossRefPubMedGoogle Scholar
  10. Cutler HG (1991) Brassinosteroids through the looking glass: an appraisal. In: Cutler HG, Yokota T, Adam G (eds) Brassinosteroids: chemistry, bioactivity, and application. ACS Symposium Series, 474, pp 334–345Google Scholar
  11. De Rybel B et al (2009) Chemical inhibition of a subset of Arabidopsis thaliana GSK3-like kinases activates brassinosteroid signaling. Chem Biol 16:594–604. 04.008CrossRefPubMedPubMedCentralGoogle Scholar
  12. Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21–25CrossRefPubMedGoogle Scholar
  13. Giannopolitis N, Ries SK (1977) Superoxide dismutase. I. Occurrence in higher plants. Plant Physiol 59:309–314CrossRefPubMedPubMedCentralGoogle Scholar
  14. Gruszka D (2013) The brassinosteroid signaling pathway-new key players and interconnections with other signaling networks crucial for plant development and stress tolerance. Int J Mol Sci 14:8740–8774. CrossRefPubMedPubMedCentralGoogle Scholar
  15. Habig WH, Jakoby WB (1981) Glutathione S-transferases (rat and human). Methods Enzymol 77:218–231. CrossRefPubMedGoogle Scholar
  16. Hatzios KK, Burgos N (2004) Metabolism-based herbicide resistance: regulation by safeners. Weed Sci 52:454–467. CrossRefGoogle Scholar
  17. Hayat S, Ali B, Aiman Hasan S, Ahmad A (2007) Brassinosteroid enhanced the level of antioxidants under cadmium stress in Brassica juncea. Environ Exp Bot 60:33–41. CrossRefGoogle Scholar
  18. Hodges DM, DeLong JM, Forney CF, Prange RK (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. CrossRefGoogle Scholar
  19. Honnerova J, Rothova O, Hola D, Kocova M, Kohout L, Kvasnica M (2010) The exogenous application of brassinosteroids to Zea mays L. stressed by long-term chilling does not affect the activities of photosystem 1 or 2. J Plant Growth Regul 29:500–505. CrossRefGoogle Scholar
  20. Ishida H, Makino A, Mae T (1999) Fragmentation of the large subunit of ribulose-1,5-bisphosphate carboxylase by reactive oxygen species occurs near Gly-329. J Biol Chem 274:5222–5226. CrossRefPubMedGoogle Scholar
  21. Kim YM, Park K, Joo GJ, Jeong EM, Kim JE, Rhee IK (2004) Glutathione-dependent biotransformation of the fungicide chlorothalonil. J Agric Food Chem 52:4192–4196. CrossRefPubMedGoogle Scholar
  22. Lichtenthaler H, Wellbum A (1982) Determination of total carotenoids and chlorophylls a and b of leaf in different solvents. Biochem Soc Trans 11:591–592. CrossRefGoogle Scholar
  23. Liu H, Weisman D, Ye YB, Cui B, Huang YH, Colon-Carmona A, Wang ZH (2009) An oxidative stress response to polycyclic aromatic hydrocarbon exposure is rapid and complex in Arabidopsis thaliana. Plant Sci 176:375–382. CrossRefGoogle Scholar
  24. Liu XM, Xu X, Li BH, Wang XQ, Wang GQ, Li MR (2015) RNA-Seq transcriptome analysis of maize inbred carrying nicosulfuron-tolerant and nicosulfuron-susceptible alleles. Int J Mol Sci 16:5975–5989. CrossRefPubMedPubMedCentralGoogle Scholar
  25. Liu S et al (2018) A novel bikinin analogue for Arabidopsis and rice with superior plant growth-promoting activity. J Plant Growth Regul 37:166–173. CrossRefGoogle Scholar
  26. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−∆∆Ct. Methods 25:402–408. CrossRefGoogle Scholar
  27. Meyer MD, Pataky JK, Williams MM II (2010) Genetic factors influencing adverse effects of mesotrione and nicosulfuron on sweet corn yield. Agron J 102:1138–1144. CrossRefGoogle Scholar
  28. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410. CrossRefGoogle Scholar
  29. Pang S, Duan L, Liu Z, Song X, Li X, Wang C (2012) Co-induction of a glutathione-S-transferase, a glutathione transporter and an ABC transporter in maize by xenobiotics. PLoS ONE 7:e40712. CrossRefPubMedPubMedCentralGoogle Scholar
  30. Puja O, Renu B, Shagun B, Ravinderjit K, Shivam J, Anjali K, Ripu DP (2015) The common molecular players in plant hormone crosstalk and signaling. Curr Protein Pept Sci 16:369–388. CrossRefGoogle Scholar
  31. Rahman I, Kode A, Biswas KS (2006) Assay for quantitative determination of glutathione and glutathione disulfide levels using enzymatic recycling method. Nat Protoc 1:3159–3165. CrossRefPubMedGoogle Scholar
  32. Shahzad B, Tanveer M, Zhao C, Rehman A, Cheema SA, Sharma A, Song H, Rehman SU, Dong ZR (2018) Role of 24-epibrassinolide (EBL) in mediating heavy metal and pesticide induced oxidative stress in plants: a review. Ecotox Environ Safety 147:935–944. CrossRefGoogle Scholar
  33. Sharma I, Bhardwaj R, Pati PK (2012) Mitigation of adverse effects of chlorpyrifos by 24-epibrassinolide and analysis of stress markers in a rice variety Pusa Basmati-1. Ecotoxicol Environ Saf 85:72–81. CrossRefPubMedGoogle Scholar
  34. Sharma I, Bhardwaj R, Pati PK (2013) Stress modulation response of 24-epibrassinolide against imidacloprid in an elite indica rice variety Pusa Basmati-1. Pestic Biochem Physiol 105:144–153. CrossRefGoogle Scholar
  35. Sharma I, Bhardwaj R, Pati PK (2015) Exogenous application of 28-homobrassinolide modulates the dynamics of salt and pesticides induced stress responses in an elite rice variety Pusa Basmati-1. J Plant Growth Regul 34:509–518. CrossRefGoogle Scholar
  36. Sharma A, Kumar V, Singh R, Thukral AK, Bhardwaj R (2016a) Effect of seed pre-soaking with 24-epibrassinolide on growth and photosynthetic parameters of Brassica juncea L. in imidacloprid soil. Ecotoxicol Environ Saf 133:195–201. CrossRefPubMedGoogle Scholar
  37. Sharma A, Thakur S, Kumar V, Kanwar MK, Kesavan AK, Thukral AK, Bhardwaj R, Alam P, Ahmad P (2016b) Pre-sowing seed treatment with 24-epibrassinolide ameliorates pesticide stress in Brassica juncea L. through the modulation of stress markers. Front Plant Sci 7:1569. CrossRefPubMedPubMedCentralGoogle Scholar
  38. Sharma A, Bhardwaj R, Kumar V, Thukral AK  (2016c) GC-MS studies reveal stimulated pesticide detoxification by brassinolide application in Brassica juncea L. plants. Environ Sci Pollut Res 23:14518–14525. CrossRefGoogle Scholar
  39. Sharma A, Thakur S, Kumar V, Kesavan AK, Thukral AK, Bhardwaj R (2017) 24-Epibrassinolide stimulates imidacloprid detoxification by modulating the gene expression of Brassica juncea L. BMC Plant Biol 17:56. CrossRefPubMedPubMedCentralGoogle Scholar
  40. Shiferaw B, Prasanna BM, Hellin J, Baenziger M (2011) Crops that feed the world 6. Past successes and future challenges to the role played by maize in global food security. Food Secur 3:307–327. CrossRefGoogle Scholar
  41. Sun L, Wu R, Su W, Gao Z, Lu C (2017) Physiological basis for isoxadifen-ethyl induction of nicosulfuron detoxification in maize hybrids. PLoS ONE 12.
  42. Thomas RL, Jen JJ, Morrr CV (1982) Changes in soluble and bound peroxidase-IAA oxidase during tomato fruit development. J Food Sci 47:158–161. CrossRefGoogle Scholar
  43. Van Eerd LL, Hoagland RE, Zablotowicz RM, Hall JC (2003) Pesticide metabolism in plants and microorganisms. Weed Sci 51:472–495.;2 CrossRefGoogle Scholar
  44. Vriet C, Russinova E, Reuzeau C (2012) Boosting crop yields with plant steroids. Plant Cell 24:842–857. CrossRefPubMedPubMedCentralGoogle Scholar
  45. Xia XJ, Huang YY, Wang L, Huang LF, Yu YL, Zhou YH, Yu JQ (2006) Pesticides-induced depression of photosynthesis was alleviated by 24-epibrassinolide pretreatment in Cucumis sativus L. Pestic Biochem Physiol 86:42–48. CrossRefGoogle Scholar
  46. Xia XJ et al (2009) Brassinosteroids promote metabolism of pesticides in cucumber. J Agric Food Chem 57:8406–8413. CrossRefPubMedGoogle Scholar
  47. Zhang ZP (2003) Development of chemical weed control and integrated weed management in China. Weed Biol Manage 3:197–203. CrossRefGoogle Scholar
  48. Zhou Y et al (2015) Brassinosteroids play a critical role in the regulation of pesticide metabolism in crop plants. Sci Rep 5:9018. CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Shaojin Liu
    • 1
  • Yan He
    • 1
  • Hao Tian
    • 1
  • Chunxin Yu
    • 1
  • Weiming Tan
    • 1
  • Zhaohu Li
    • 1
  • Liusheng Duan
    • 1
    Email author
  1. 1.State Key Laboratory of Plant Physiology and Biochemistry/Engineering Research Center of Plant Growth Regulators, Ministry of Education, College of Agronomy and BiotechnologyChina Agricultural UniversityBeijingPeople’s Republic of China

Personalised recommendations