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Role of xylo-oligosaccharides in protection against salinity-induced adversities in Chinese cabbage

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Abstract

Soil salinity is a stringent abiotic constraint limiting crop growth and productivity. The present study was carried out to appraise the role of xylo-oligosaccharides (XOSs) in improving the salinity tolerance of Chinese cabbage. Salinity stress (0.5 % NaCl solution) and four levels (0, 40, 80, 120 mg L−1) of XOSs were imposed on 20-day-old plants cultured under controlled conditions. Salinity stress decreased the aboveground fresh biomass, photosynthesis, transpiration rate, stomatal conductance, internal CO2 concentration, water use efficiency, and chlorophyll contents but increased the stomatal limitation value of Chinese cabbage compared with control. Such physiological interferences, disturbances in plant water relations, and visually noticeable growth reductions in Chinese cabbage were significantly alleviated by the addition of XOSs under salinity stress. Under salinity stress, application of XOSs significantly enhanced the activities of enzymatic (superoxide dismutase, peroxidase, catalase) and non-enzymatic (ascorbate, carotene) antioxidants and reduced the malondialdehyde content in the leaves of Chinese cabbage. The XOS-applied plants under salinity stress also recorded higher soluble sugars, proline, and soluble protein content in their leaves. Exposure of salinity stress increased the ratio of Na+/K+, Na+/Ca2+, and Na+/Mg2+ in shoot as well as root of Chinese cabbage, however, XOS application significantly reduced these ratios particularly in shoot. Lower levels of XOSs (40 or 80 mg L−1) were more effective for most of the studied attributes. The greater salinity tolerance and better growth in these treatments were related with enhanced antioxidative defense system, reduced lipid peroxidation, increased osmolyte accumulation, and maintenance of ionic balance.

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Abbreviations

AsA:

Ascorbate

CAT:

Catalase

CAR:

Carotene

Ci :

Internal CO2 concentration

EDTA:

Ethylenediamine tetraacetic acid

Gs :

Stomatal conductance

Ls :

Stomatal limitation value

MDA:

Malondialdehyde

NBT:

Nitroblue tetrazolium

NDOs:

Non-digestible oligosaccharides

Pn :

Photosynthesis

POD:

Peroxidase

SOD:

Superoxide dismutase

Tr :

Transpiration

WUE :

Water use efficiency

XOS:

Xylo-oligosaccharides

References

  • Amador BM, Yamada S, Yamaguchi T, Puente ER, Serrano NAV, Hernandez JLG, Aguilar RL, Dieguez ET, Garibay AN (2007) Influence of calcium silicate on growth, physiological parameters and mineral nutrition in two legume species under salt stress. J Agron Crop Sci 193:413–421

    Article  Google Scholar 

  • Anjum SA, Tanveer M, Hussain S, Bao M, Wang L, Khan I, Ehsanullah, Tung SA, Samad RA, Shahzad B (2015) Cadmium toxicity in Maize (Zea mays L.): consequences on antioxidative systems, reactive oxygen species and cadmium accumulation. Environ Sci Pollut Res doi:10.1007/s11356-015-4882-z

  • Athar HR, Khan A, Ashraf M (2008) Exogenously applied ascorbic acid alleviates salt-induced oxidative stress in wheat. Environ Exp Bot 63:224–231

    Article  CAS  Google Scholar 

  • Azevedo NA, Prisco JT, Filho JE, Lacerda CF, Silva JV, Costa PH, Filho EG (2004) Effects of salt stress on plant growth, stomatal response and solute accumulation of different maize genotypes. Braz J Plant Physiol 16:31–38

    Google Scholar 

  • Bernstein N, Silk WK, Läuchli A (1995) Growth and development of sorghum leaves under conditions of NaCl stress: possible role of some mineral elements in growth inhibition. Planta 196:699–705

    Article  CAS  Google Scholar 

  • Blumwald E (2000) Sodium transport and salt tolerance in plants. Curr Opin Cell Biol 12:431–434

    Article  CAS  Google Scholar 

  • Chow WS, Marylin CB, Anderson JM (1990) Growth and photosynthetic responses of spinach to salinity: implications of K+ nutrition for salt tolerance. Aust J Plant Physiol 17:563–578

    Article  CAS  Google Scholar 

  • Cramer GR, Lauchli A, Polito VS (1985) Displacement of Ca+ by Na+ from the plasma lemma of root cells. Plant Physiol 79:207–211

    Article  CAS  Google Scholar 

  • Demirevska-Kepova K, Simova-Stoilova L, Stoyanova ZP, Feller U (2006) Cadmium stress in barley: growth, leaf pigment, and protein composition and detoxification of reactive oxygen species. J Plant Nutr 29:451–468

    Article  CAS  Google Scholar 

  • Empadinhas N, Da Costa MS (2008) Osmoadaptation mechanisms in prokaryotes: distribution of compatible solutes. Int Microb 11:151–161

    CAS  Google Scholar 

  • Fahad S, Hussain S, Matloob A, Khan FA, Khaliq A, Saud S et al (2014) Phytohormones and plant responses to salinity stress: a review. Plant Growth Regul 75:391–404

    Article  Google Scholar 

  • Fahad S, Hussain S, Saud S, Khan F, Hassan S, Amanullah, Nasim W et al. (2015) Exogenously applied plant growth regulators affect heat‐stressed rice pollens. J Agron Crop Sci doi: 10.1111/jac.12148

  • Gao JF (2005) Experimental guidance for plant physiology. Higher Education Press, Beijing, China, pp 74–76

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

  • Greenway H, Munns R (1980) Mechanisms of salt tolerance in nonhalophytes. Annu Rev Plant Physiol Plant Mol Biol 31:149–190

    Article  CAS  Google Scholar 

  • Han R, Lefèvre I, Albacete A, Pérez-Alfocea F, Barba-Espín G, Díaz-Vivancos P, Quinet M, Ruan C, Hernández JA, Cantero-Navarro E, Lutts S (2013) Antioxidant enzyme activities and hormonal status in response to Cd stress in the wetland halophyte. Physiol Plant 147:352–368

    Article  CAS  Google Scholar 

  • Hussain S, Khaliq A, Matloob A, Wahid MA, Afzal I (2013) Germination and growth response of three wheat cultivars to NaCl salinity. Soil Environ 32:36–43

    CAS  Google Scholar 

  • Jamil M, Ashraf M, Rha E (2012) Alleviation of salt stress using gibberellic acid in Chinese cabbage. Acta Agron Hung 60:345–355

    Article  CAS  Google Scholar 

  • Khaliq A, Aslam F, Matloob A, Hussain S, Geng M, Wahid A, Rehman H (2015a) Seed priming with selenium: consequences for emergence, seedling growth, and biochemical attributes of rice. Biol Trace Element Res 166:236–244

    Article  CAS  Google Scholar 

  • Khaliq A, Zia-ul-Haq M, Ali F, Aslam F, Matloob A, Navab A, Hussain S (2015b) Salinity tolerance in wheat cultivars is related to enhanced activities of enzymatic antioxidants and reduced lipid peroxidation. Clean Soil Air Water 43:1248–1258

    Article  CAS  Google Scholar 

  • Li HS, Sun Q, Zhao SJ (2000) Principles and techniques of plant physiological biochemical experiment. Higher Education, Beijing, pp 130–248 (In Chinese)

    Google Scholar 

  • Lichtenthaler HK (1987) Chlorophyll 416 and carotenoids: pigments of photosynthetic biomembranes. In: Packer L, Douce R (eds) Methods in enzymology. Academic, San Diego, pp 350–382

    Google Scholar 

  • Ling PX, Zhu XQ, Su YS, Zhang XY (2007) Progress in the functions and applications of xylo-oligosaccharides. Food Drug 9:015

    Google Scholar 

  • Maathuis FJ (2009) Physiological functions of mineral macronutrients. Curr Opin Plant Biol 12:250–258

    Article  CAS  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic, San Diego, California, USA

    Google Scholar 

  • Munns R, Termaat A (1986) Whole-plant responses to salinity. Aust J Plant Physiol 13:143–160

    Article  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Physiol Plant Mol Biol 59:651–681

    Article  CAS  Google Scholar 

  • Mustafa Z, Pervez MA, Ayyub CM, Matloob A, Khaliq A, Hussain S, Ihsan MZ, Butt M (2014) Morpho-physiological characterization of chilli genotypes under NaCl salinity. Soil Environ 33:133–141

    Google Scholar 

  • Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60:324–349

    Article  CAS  Google Scholar 

  • Quan RD, Shang M, Zhang H, Zhao YX, Zhang JR (2004) Engineering of enhanced glycine betaine synthesis improves drought tolerance in maize. Plant Biotechnol J 2:477–486

    Article  CAS  Google Scholar 

  • Shabala S, Cuin TA (2008) Potassium transport and plant salt tolerance. Physiol Plant 133:651–669

    Article  CAS  Google Scholar 

  • Vanrensburg L, Kruger GHJ, Kruger RH (1993) Proline accumulation as drought tolerance selection criterion: its relationship to membrane integrity and chloroplast ultra-structure in Nicotiana tabacum L. J Plant Physiol 141:188–194

    Article  CAS  Google Scholar 

  • Wang J, Sun B, Cao Y, Tian Y, Wang C (2009) Enzymatic preparation of wheat bran xylo-oligosaccharides and their stability during pasteurization and autoclave sterilization at low pH. Carbohydr Polym 77:816–821

    Article  CAS  Google Scholar 

  • Yamaguchi T, Blumwald E (2005) Developing salt-tolerant crop plants: challenges and opportunities. Trends Plant Sci 10:615–620

    Article  CAS  Google Scholar 

  • Yoshino K, Higashi N, Koga K (2006) Inhibitory effects of acidic xylo-oligosaccharide on stress-induced gastric inflammation in mice. J Food Hygienic Soc Japan 47:284–287

    Article  CAS  Google Scholar 

  • Zhang FQ, Shi WY, Jin ZX, Shen ZG (2003) Response of antioxidative enzymes in cucumber chloroplast to cadmium toxicity. J Plant Nutr 26:1779–1788

    Article  CAS  Google Scholar 

  • Zhang S, Hu J, Zhang Y, Xie XJ, Knapp A (2007) Seed priming with brassinolide improves lucerne (Medicago sativa L.) seed germination and seedling growth in relation to physiological changes under salinity stress. Aust J Agric Res 58:811–815

    Article  CAS  Google Scholar 

  • Zhang YH, Wu LS, Geng MJ, Hu HQ, Zhang SX (2009) Effects of several oligosaccharides on the yield and quality of flowering Chinese cabbage. J Huazhong Agric Univ (Nat Sci Edition) 28:164–168

    CAS  Google Scholar 

  • Zhang YH, Geng MJ, Liu LY, Zhao K, Wu LS, Hu CX, Di HJ (2011) The role of calcium in regulating alginate-derived oligosaccharides in nitrogen metabolism of Brassica campestris L. var. utilis Tsen et Lee. Plant Growth Regul 64:193–202

    Article  CAS  Google Scholar 

  • Zhang M, Hu C, Zhao X, Tan Q, Sun X, Cao A, Cui M, Zhang Y (2012) Molybdenum improves antioxidant and osmotic-adjustment ability against salt stress in Chinese cabbage (Brassica campestris L. ssp. Pekinensis). Plant Soil 355:375–383

    Article  CAS  Google Scholar 

  • Zheng M, Tao Y, Hussain S, Jiang Q, Peng S, Huang J, Cui K, Nie L (2015) Seed priming in dry direct-seeded rice: consequences for emergence, seedling growth and associated metabolic events under drought stress. Plant Growth Regul doi: 10.1007/s10725-015-0083-5

  • Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71

    Article  CAS  Google Scholar 

  • Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Physiol Plant Mol Biol 53:247–273

    Article  CAS  Google Scholar 

  • Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441–445

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Science and technology support program (2010BAD01B05) and the Hubei Provincial Engineering Laboratory for New-Type Fertilizer, College of Resources and Environment, Huazhong Agricultural University.

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Authors and Affiliations

  1. Microelement Research Center, College of Resources and Environment, Huazhong Agricultural University, Wuhan, 430070, China

    Weiwei Chen, Chen Guo, Saddam Hussain, Bingxin Zhu, Fang Deng, Yan Xue, Mingjian Geng & Lishu Wu

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  1. Weiwei Chen
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  2. Chen Guo
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  3. Saddam Hussain
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  4. Bingxin Zhu
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  5. Fang Deng
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  6. Yan Xue
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  8. Lishu Wu
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Correspondence to Saddam Hussain or Lishu Wu.

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Chen, W., Guo, C., Hussain, S. et al. Role of xylo-oligosaccharides in protection against salinity-induced adversities in Chinese cabbage. Environ Sci Pollut Res 23, 1254–1264 (2016). https://doi.org/10.1007/s11356-015-5361-2

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