Advertisement

Plant Growth Regulation

, Volume 81, Issue 3, pp 533–542 | Cite as

β-Cyclodextrin–hemin enhances tolerance against salinity in tobacco seedlings by reestablishment of ion and redox homeostasis

  • Jing Zhang
  • Xincheng Yang
  • Yong Ren
  • Bo Yang
  • Ziwei Liu
  • Benwu You
  • Hongxiu Zhang
  • Wenbiao ShenEmail author
  • Xueping ChenEmail author
Original paper
  • 234 Downloads

Abstract

β-Cyclodextrin–hemin (β-CDH) is a complex combining hemin with β-cyclodextrin (β-CD), which could improve hemin solubility. Our previous results showed that β-CDH, was able to enhance alfalfa tolerance against cadmium stress. However, whether or how β-CDH influences salinity tolerance is still elusive. In this report, we observed that similar to the beneficial responses of hemin rather than β-CD, the addition of β-CDH not only alleviated salinity-induced seedling growth inhibition (in particular), but also arrested chlorophyll degradation in tobacco seedlings. The efficiency of β-CDH against salinity stress compared to that of hemin, was confirmed, since the maximum beneficial responses against NaCl stress was obtained with 0.1 μM β-CDH and 10 μM hemin, respectively. Subsequent work showed that the redox imbalance caused by salinity stress could be improved by β-CDH. This was suggested by the reduced lipid peroxidation and hydrogen peroxide accumulation, as well as the induction of representative antioxidant genes, encoding superoxide dismutase, guaiacol peroxidase, and ascorbate peroxidase. Meanwhile, compared to control conditions, the ratio of K+ to Na+ was relatively low in NaCl-stressed tobacco seedlings. By contrast, the administration of β-CDH not only significantly blocked the increase of Na+, but also obviously increased K+, thus resulting in a high K+ to Na+ ratio in both shoot and root parts. Ion homeostasis is therefore reestablished. Together, our results suggested that β-CDH was able to improve salinity tolerance via the reestablishment of redox and ion homeostasis.

Keywords

Nicotiana tabacum β-Cyclodextrin–hemin (β-CDH) Reactive oxygen species (ROS) Ion homeostasis Redox homeostasis 

Notes

Acknowledgements

This work was funded by the grant from China Tobacco Anhui Industrial, Co., Ltd (0920140421003), the National Natural Science Foundation of China (31170241), the Fundamental Research Funds for the Central Universities (KYTZ201402), and the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).

Author contributions

WS and XC designed the overall study and obtained funding; JZ, XY, YR, BY, ZL, BY, HZ carried out the experiments; JZ and WS analyzed and interpreted result; WS, JZ and XC wrote the first draft of the manuscript, and all authors approved the final version of the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

Supplementary material

10725_2016_230_MOESM1_ESM.doc (300 kb)
Supplementary material 1 (DOC 300 KB)

References

  1. Attuwaybi BO, Kozar RA, Moore-Olufemi SD, Sato N, Hassoun HT, Weisbrodt NW, Moore FA (2004) Heme oxygenase-1 induction by hemin protects against gut ischemia/reperfusion injury. J Surg Res 118:53–57CrossRefPubMedGoogle Scholar
  2. Badawi GH, Kawano N, Yamauchi Y, Shimada E, Sasaki R, Kubo A, Tanaka K (2004a) Over-expression of ascorbate peroxidase in tobacco chloroplasts enhances the tolerance to salt stress and water deficit. Physiol Plant 121:231–238CrossRefPubMedGoogle Scholar
  3. Badawi GH, Yamauchi Y, Shimada E, Sasaki R, Kawano N, Tanaka K, Tanaka K (2004b) Enhanced tolerance to salt stress and water deficit by overexpressing superoxide dismutase in tobacco (Nicotiana tabacum) chloroplasts. Plant Sci 166:919–928CrossRefGoogle Scholar
  4. Ben-Ari Z, Issan Y, Katz Y, Sultan M, Safran M, Michal LS, Nader GA, Kornowski R, Grief F, Pappo O, Hochhauser E (2013) Induction of heme oxygenase-1 protects mouse liver from apoptotic ischemia/reperfusion injury. Apoptosis 18:547–555CrossRefPubMedGoogle Scholar
  5. Bodine KD, Gin DY, Gin MS (2014) Synthesis of readily modifiable cyclodextrin analogues via cyclodimerization of an alkynyl-azido trisaccharide. J Am Chem Soc 126:1638–1639CrossRefGoogle Scholar
  6. Bouchenak F, Henri P, Benrebiha FZ, Rey P (2012) Differential responses to salinity of two Atriplex halimus populations in relation to organic solutes and antioxidant systems involving thiol reductases. J Plant Physiol 169:1445–1453CrossRefPubMedGoogle Scholar
  7. 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 72:248–254CrossRefPubMedGoogle Scholar
  8. Cao Z, Geng B, Xu S, Xuan W, Nie L, Shen W, Liang Y, Guan R (2011) BnHO1, a haem oxygenase-1 gene from Brassica napus, is required for salinity and osmotic stress-induced lateral root formation. J Exp Bot 62:4675–4689CrossRefPubMedPubMedCentralGoogle Scholar
  9. Chattopadhayay MK, Tiwari BS, Chattopadhyay G, Bose A, Sengupta DN, Ghosh B (2002) Protective role of exogenous polyamines on salinity-stressed rice (Oryza sativa) plants. Physiol Plant 116:192–199CrossRefPubMedGoogle Scholar
  10. Chaturvedi AK, Patel MK, Mishra A, Tiwari V, Jha B (2014) The SbMT-2 gene from a halophyte confers abiotic stress tolerance and modulates ROS scavenging in transgenic tobacco. PLoS One 9:e111379CrossRefPubMedPubMedCentralGoogle Scholar
  11. Chen H, Zhang J, Neff MM, Hong SW, Zhang H, Deng XW, Xiong L (2008) Integration of light and abscisic acid signaling during seed germination and early seedling development. Proc Natl Acad Sci USA 105:4495–4500CrossRefPubMedPubMedCentralGoogle Scholar
  12. Deinlein U, Stephan AB, Horie T, Luo W, Xu G, Schroeder JI (2014) Plant salt-tolerance mechanisms. Trends Plant Sci 19:371–379CrossRefPubMedPubMedCentralGoogle Scholar
  13. Deng YQ, Bao J, Yuan F, Liang X, Feng ZT, Wang BS (2016) Exogenous hydrogen sulfide alleviates salt stress in wheat seedlings by decreasing Na+ content. Plant Growth Regul 79:391–399CrossRefGoogle Scholar
  14. El-Shabrawi H, Kumar B, Kaul T, Reddy MK, Singla-Pareek SL, Sopory SK (2010) Redox homeostasis, antioxidant defense, and methylglyoxal detoxification as markers for salt tolerance in Pokkali rice. Protoplasma 245:85–96CrossRefPubMedGoogle Scholar
  15. Fu G, Zhang L, Cui W, Wang Y, Shen W, Ren Y, Zheng T (2011) Induction of heme oxygenase-1 with β-CD–hemin complex mitigates cadmium-induced oxidative damage in the roots of Medicago sativa. Plant Soil 345:271–285CrossRefGoogle Scholar
  16. Garg N, Bhandari P (2016) Silicon nutrition and mycorrhizal inoculations improve growth, nutrient status, K+/Na+ ratio and yield of Cicer arietinum L. genotypes under salinity stress. Plant Growth Regul 78:371–387CrossRefGoogle Scholar
  17. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930CrossRefPubMedGoogle Scholar
  18. Groß F, Durner J, Gaupels F (2013) Nitric oxide, antioxidants and prooxidants in plant defence responses. Front Plant Sci 4:419CrossRefPubMedPubMedCentralGoogle Scholar
  19. He M, Pan H, Chang RCC, So KF, Brecha NC, Pu M (2014) Activation of the Nrf2/HO-1 antioxidant pathway contributes to the protective effects of Lycium barbarum polysaccharides in the rodent retina after ischemia-reperfusion-induced damage. PLoS One 9:e84800CrossRefPubMedPubMedCentralGoogle Scholar
  20. Horváth E, Szalai G, Janda T (2007) Induction of abiotic stress tolerance by salicylic acid signaling. J Plant Growth Regul 26:290–300CrossRefGoogle Scholar
  21. Huang Y, Cai R, Mao L, Liu Z, Huang H (1999) Spectrophotometric determination of hydrogen peroxide using β-CD–hemin as a mimetic enzyme of peroxidase. Anal Sci 15:889–894CrossRefGoogle Scholar
  22. Huang J, Han B, Xu S, Zhou M, Shen W (2011a) Heme oxygenase-1 is involved in the cytokinin-induced alleviation of senescence in detached wheat leaves during dark incubation. J Plant Physiol 168:768–775CrossRefPubMedGoogle Scholar
  23. Huang XS, Luo T, Fu XZ, Fan QJ, Liu JH (2011b) Cloning and molecular characterization of a mitogen-activated protein kinase gene from Poncirus trifoliata whose ectopic expression confers dehydration/drought tolerance in transgenic tobacco. J Exp Bot 62:5191–5206CrossRefPubMedPubMedCentralGoogle Scholar
  24. Lee DH, Kim YS, Lee CB (2001) The inductive responses of the antioxidant enzymes by salt stress in the rice (Oryza sativa L.) J Plant Physiol 158:737–745CrossRefGoogle Scholar
  25. Leshem Y, Seri L, Levine A (2007) Induction of phosphatidylinositol 3-kinase-mediated endocytosis by salt stress leads to intracellular production of reactive oxygen species and salt tolerance. Plant J 51:185–197CrossRefPubMedGoogle Scholar
  26. Li J, Zhu D, Wang R, Shen W, Guo Y, Ren Y, Shen W, Huang L (2015) β-Cyclodextrin–hemin complex-induced lateral root formation in tomato: involvement of nitric oxide and heme oxygenase 1. Plant Cell Rep 34:381–393CrossRefPubMedGoogle Scholar
  27. Lin Y, Li M, Huang L, Shen W, Ren Y (2012) Involvement of heme oxygenase-1 in β-cyclodextrin–hemin complex-induced cucumber adventitious rooting process. Plant Cell Rep 31:1563–1572CrossRefPubMedGoogle Scholar
  28. Liu Z, Cai R, Mao L, Huang H, Ma W (1999) Highly sensitive spectrofluorimetric determination of hydrogen peroxide with β-cyclodextrin–hemin as catalyst. Analyst 124:173–176CrossRefGoogle Scholar
  29. Lv WT, Lin B, Zhang M, Hua XJ (2011) Proline accumulation is inhibitory to Arabidopsis seedlings during heat stress. Plant Physiol 156:1921–1933CrossRefPubMedPubMedCentralGoogle Scholar
  30. Mazel A, Leshem Y, Tiwari BS, Levine A (2004) Induction of salt and osmotic stress tolerance by overexpression of an intracellular vesicle trafficking protein AtRab7 (AtRabG3e). Plant Physiol 134:118–128CrossRefPubMedPubMedCentralGoogle Scholar
  31. Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467CrossRefPubMedGoogle Scholar
  32. Ndisang JF, Jadhav A (2014) Hemin therapy improves kidney function in male streptozotocin-induced diabetic rats: role of the heme oxygenase/atrial natriuretic peptide/adiponectin axis. Endocrinology 155:215–229CrossRefPubMedGoogle Scholar
  33. Oh DH, Leidi E, Zhang Q, Hwang SM, Li Y, Quintero FJ, Jiang X, D’Urzo MP, Lee SY, Zhao Y, Bahk JD, Bressan RA, Yun DJ, Pardo JM, Bohnert HJ (2009) Loss of halophytism by interference with SOS1 expression. Plant Physiol 151:210–222CrossRefPubMedPubMedCentralGoogle Scholar
  34. Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60:324–349CrossRefPubMedGoogle Scholar
  35. Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB (1997) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J 11:1187–1194CrossRefGoogle Scholar
  36. Wintermans JFGM, De Mots A (1965) Spectrophotometric characteristics of chlorophylls a and b and their phenophytins in ethanol. Biochim Biophys Acta 109:448–453CrossRefPubMedGoogle Scholar
  37. Wu L, Zhang Z, Zhang H, Wang XC, Huang R (2008) Transcriptional modulation of ethylene response factor protein JERF3 in the oxidative stress response enhances tolerance of tobacco seedlings to salt, drought, and freezing. Plant Physiol 148:1953–1963CrossRefPubMedPubMedCentralGoogle Scholar
  38. Xie YJ, Xu S, Han B, Wu MZ, Yuan XX, Han Y, Gu Q, Xu DK, Yang Q, Shen WB (2011) Evidence of Arabidopsis salt acclimation induced by up-regulation of HY1 and the regulatory role of RbohD-derived reactive oxygen species synthesis. Plant J 66:280–292CrossRefPubMedGoogle Scholar
  39. Xu S, Lou T, Zhao N, Gao Y, Dong L, Jiang D, Shen W, Huang L, Wang R (2011) Presoaking with hemin improves salinity tolerance during wheat seed germination. Acta Physiol Plant 33:1173–1183CrossRefGoogle Scholar
  40. Yue Y, Zhang M, Zhang J, Duan L, Li Z (2012) SOS1 gene overexpression increased salt tolerance in transgenic tobacco by maintaining a higher K+/Na+ ratio. J Plant Physiol 169:255–261CrossRefPubMedGoogle Scholar
  41. Zhao MG, Tian QY, Zhang WH (2007) Nitric oxide synthase-dependent nitric oxide production is associated with salt tolerance in Arabidopsis. Plant Physiol 144:206–217CrossRefPubMedPubMedCentralGoogle Scholar
  42. Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71CrossRefPubMedGoogle Scholar
  43. Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441–445CrossRefPubMedGoogle Scholar
  44. Zhu J, Lee BH, Dellinger M, Cui X, Zhang C, Wu S, Nothnagel EA, Zhu JK (2010) A cellulose synthase-like protein is required for osmotic stress tolerance in Arabidopsis. Plant J 63:128–140PubMedPubMedCentralGoogle Scholar
  45. Zhu K, Zhang J, Cui W, Jin Q, Samma MK, Shen W (2014) Role of heme oxygenase-1 in spermidine-induced alleviation of salt toxicity during alfalfa seed germination. Plant Soil 375:275–287CrossRefGoogle Scholar
  46. Zhu K, Cui W, Dai C, Wu M, Zhang J, Zhang Y, Xie Y, Shen W (2016) Methane-rich water alleviates NaCl toxicity during alfalfa seed germination. Environ Exp Bot 129:37–47CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Jing Zhang
    • 1
    • 2
  • Xincheng Yang
    • 3
  • Yong Ren
    • 4
  • Bo Yang
    • 5
  • Ziwei Liu
    • 2
  • Benwu You
    • 2
  • Hongxiu Zhang
    • 6
  • Wenbiao Shen
    • 1
    Email author
  • Xueping Chen
    • 2
    Email author
  1. 1.College of Life Sciences, Laboratory Center of Life SciencesNanjing Agricultural UniversityNanjingChina
  2. 2.Tobacco and Health Research CenterUniversity of Science and Technology of ChinaHefeiChina
  3. 3.College of HorticultureNanjing Agricultural UniversityNanjingChina
  4. 4.College of Life ScienceNanjing Normal UniversityNanjingChina
  5. 5.China Tobacco Anhui Industrial, Co., LtdHefeiChina
  6. 6.Nantong Feitian Chemical Industrial Co., LtdNantongChina

Personalised recommendations