Pre-breeding: the role of antioxidant enzymes on maize in salt stress tolerance

  • Zigen Cai
  • Kai Feng
  • Xin Li
  • Hai Yan
  • Zhongbao ZhangEmail author
  • Xiaolu LiuEmail author
Original Article


Maize is a crop that is moderately sensitive to salt stress. Salinization of soil is a severe threat to maize production worldwide. Understanding the response and tolerance mechanism of maize to salt stress may be conducive to formulate strategies to improve maize performance under saline environments. In this study, salt-tolerant, salt-sensitive and moderate salt-tolerant maize plants were investigated, respectively, under salt stress conditions in three aspects: growth status, enzyme activity and gene expression level. After 30 days of planting and salt stress treatment, the plant height of USTB-297 (salt-tolerant maize) was 49.40% higher than that of USTB-265 (salt-sensitive maize) and 25.10% higher than that of USTB-109 (moderate salt-tolerant maize). Analysis of antioxidant enzymes superoxide dismutase (EC1.15.1.1), ascorbate peroxidase (EC1.11.1.11) and catalase (EC1.11.1.6) revealed that there are distinctions between these different breeds. Salt-tolerant breed with a higher plant height also had higher antioxidant enzyme activity and related genes expression compared to salt-sensitive or moderate salt-tolerant breed. The detection of gene expression in superoxide dismutase, catalase and ascorbate peroxidase using real-time PCR and the data of enzyme activity indicate that we can build a method of breeding for maize.


Salinity Maize Tolerance Real-time PCR Antioxidant enzymes 



Superoxide dismutase




Ascorbate peroxidase



This work was supported partly by Beijing Natural Science Foundation (No.6,172,007) and Beijing Academy of Agriculture and Forestry Sciences (No. KJCX 20170404, 20170203 and 20160301).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399CrossRefGoogle Scholar
  2. Beers, Sizer RF (1952) A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem 195:133–140PubMedPubMedCentralGoogle Scholar
  3. Chinnusamy V, Zhu JK (2003) Plant salt tolerance. Top Curr Genet 4:241–270CrossRefGoogle Scholar
  4. Chinnusamy V, Jagendorf A, Zhu JK (2005) Understanding and improving salt tolerance in plants. Crop Sci 45:437–448CrossRefGoogle Scholar
  5. Di H, Yu T, Deng Y, Dong X, Li R, Zhou Y, Wang ZH (2017) Complementary dna (cdna) cloning and functional verification of resistance to head smut disease (Sphacelotheca reiliana) of an nbs–lrr gene zmnl in maize (Zea mays). Euphytica 213(12):288CrossRefGoogle Scholar
  6. Fraga D, Meulia T, Fenster S (2008) Real-time PCR. Wiley, Hoboken, pp 10.3.1–10.3.34Google Scholar
  7. Giannopolitis CN, Ries SK (1977) Superoxide dismutases. I. Occurrence in higher plants. Plant Physiol. 59:309–314CrossRefGoogle Scholar
  8. Hasanuzzaman M, Nahar K, Alam MM, Roychowdhury R, Fujita M (2013) Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int J Mol Sci 14:9643–9684CrossRefGoogle Scholar
  9. Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51(51):463–499CrossRefGoogle Scholar
  10. Heffner EF, Lorenz AJ, Jannink JL, Sorrells ME (2010) Plant breeding with genomic selection: gain per unit time and cost. Crop Sci 50:1681–1690CrossRefGoogle Scholar
  11. Liang W, Ma X, Wan P, Liu L (2018) Plant salt-tolerance mechanism: a review. Biochem Bioph Res Co. 495:286–291CrossRefGoogle Scholar
  12. Mckersie BD, Leshem YY (1994) Stress and stress coping in cultivated plants. Springer, Dordrecht, pp 194–217CrossRefGoogle Scholar
  13. Miller G, Suzuki N, Ciftci-yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant, Cell Environ 33:453–467CrossRefGoogle Scholar
  14. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410CrossRefGoogle Scholar
  15. Muhammad F, Mubshar H, Abdul W, Kadambot H (2015) Salt stress in maize: effect, resistance mechanisms, and management. A review. Agron Sustain Dev 35:461–481CrossRefGoogle Scholar
  16. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681CrossRefGoogle Scholar
  17. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880Google Scholar
  18. Neto ADDA, Prisco JT, Enéas-Filho J, Abreu CEBD, Gomes-Filho E (2006) Effect of salt stress on antioxidative enzymes and lipid peroxidation in leaves and roots of salt-tolerant and salt-sensitive maize genotypes. Environ Exp Bot 56(1):87–94CrossRefGoogle Scholar
  19. Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279CrossRefGoogle Scholar
  20. Parida AK, Das AB, Mohanty P (2004) Defense potentials to NaCl in mangrove, Bruguiera parviflora: differential changes of isoforms of some antioxidative enzymes. J Plant Physiol 161:531–542CrossRefGoogle Scholar
  21. Scandalios JG (2002) The rise of ROS. Trends Biochem Sci 27:483–486CrossRefGoogle Scholar
  22. Vaidyanathan H, Sivakumar P, Chakrabarty R, Thomas G (2003) Scavenging of reactive oxygen species in NaCl-stressed rice (Oryza sativa L.) e differential response in salt-tolerant and sensitive varieties. Plant Sci 165:1411–1418CrossRefGoogle Scholar
  23. Wahid A, Perveen M, Gelani S, Basra SMA (2007) Pretreatment of seed with H2O2 improves salt tolerance of wheat seedlings by alleviation of oxidative damage and expression of stress proteins. J Plant Physiol 164:283–294CrossRefGoogle Scholar
  24. Xiang PK, Pan JW, Zhang MY, Xin X, Yan Z, Yang L, Li DP, Li DQ (2011) ZmMKK4, a novel group C mitogen-activated protein kinase in maize (Zea mays), confers salt and cold tolerance in transgenic Arabidopsis. Plant, Cell Environ 34:1291–1303CrossRefGoogle Scholar
  25. Xu FJ, Jin CH, Liu WJ, Zhang YS, Lin XY (2011) Pretreatment with H2O2 alleviates aluminum-induced oxidative stress in wheat seedlings. J Integr Plant Biol 53:44–53CrossRefGoogle Scholar
  26. Yoshida T, Fujita Y, Sayama H, Kidokoro S, Maruyama K, Mizoi J, Yamaguchi-Shinozaki K (2010) AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation. Plant J 61:672–685CrossRefGoogle Scholar
  27. Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71CrossRefGoogle Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2019

Authors and Affiliations

  1. 1.Department of Biological Technology, Institute of Chemistry and Biological EngineeringUniversity of Science and Technology, BeijingBeijingPeople’s Republic of China
  2. 2.Beijing Agro-Biotechnology Research Center, Beijing Academy of Agriculture and Forestry SciencesBeijingPeople’s Republic of China

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