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Research Article

volume 42 issue 1 (february 2019) : 72-76,   Doi: 10.18805/LR-435

The effects of plant growth promoting rhizobacteria on antioxidant activity in chickpea (Cicer arietinum L.) under salt stress
 

H
Hilal Yilmaz
H
Haluk Kulaz
1Department of Field Crops, Faculty of Agriculture, Yuzuncu Yil University, 65080 Van, Turkey.

  • Submitted05-06-2018|

  • Accepted06-10-2018|

  • First Online 07-12-2018|

  • doi 10.18805/LR-435

Cite article:- Yilmaz Hilal, Kulaz Haluk (2018). The effects of plant growth promoting rhizobacteria on antioxidant activity in chickpea (Cicer arietinum L.) under salt stress. Legume Research. 42(1): 72-76. doi: 10.18805/LR-435.

ABSTRACT

In chickpea soil salinity is one of the most important factors affecting yield, nodulation and physiological events. Salinity affects the growth of salt sensitive varieties. The inoculation of plant growth promoting rhizobacteria (PGPR) allows to reduce the harmful effects of salinity. To prevent adverse effects of chickpea salinity, the effects of four bacteria (Rhizobium ciceri, A-08, EB-80 and Isolate-30) in root rhizosphere under controlled environmental growth conditions were studied. This study has shown that PGPRs play an important role in growth regulators for the positive development of plants under salt stress. It has been observed that these isolates, common in roots, are tolerant to salinity antioxidant activity and an increase in proline, MDA, APX, SOD and CAT concentrations were found under saline conditions when unvaccinated plants were compared with grafted plants. The results also suggested that inoculated PGPR strains can reduce salinity stress by increasing salt tolerance.

REFERENCES

  1. Akgül, D. S. and Mirik, M. (2008). Biocontrol of Phytophthora Capsici on pepper plants by Bacillus megnaterium strains. Journal of Plant Patholology, 90 (1): 29-34.
  2. Ashraf, M., Berge S.H., and Mahmood O.T. (2004). Inoculation wheat seedlings with exopolysaccharide-producing bacteria restricts sodium uptake and stimulates plant growth under salt stree. Biol. Fer. Soils.40:157-162.
  3. Aslantas, R., Cakmakcý, R., Sahin, F. (2007). Effect of plant growth promoting rhizobacteria on young apple tree growth and fruit yield under orchard conditions. Science Horticulture,111: 371–377.
  4. Cakmakci, R. (2006). Bitki geliþme promotörü rizobakteri kullanýmýndaki son geliþmeler: organik tarým perspektif ve uygulamalarý. Organik Tarým Kongresi. Yalova.
  5. Cakmakci, R., Dönmez, M. F., Erdoðan, Ü. (2007 a). The effect of plant growth promoting rhizobacteria on barley seedling growth, nutrient uptake, some soil properties, and bacterial counts. Turkish J. Agric. For,31: 189-199.
  6. Cakmakci, R., Erat, M., Erdoðan, Ü., Dönmez, F. (2007b). The influence of plant growth-promoting rhizobacteria on growth and enzyme activities in wheat and spinach plants. J. Plant Nutr. Soil Science,170: 288-295.
  7. del Rio, L. A., Corpas F. J., Sandalio L. M., Palma J. M., Barroso J. B. (2003). Plant peroxisomes, reactive oxygen metabolism and nitric oxide. IUBMB Life, 55:71-81. 
  8. Farooq, M., Gogoi, N., Hussain, M., Barthakur, S., Paul, S., Bharadwaj, N., Migdadi, M.H., Alghamdi, S.S., Siddique, K. H. (2017). Effects, tolerance mechanisms and management of salt stress in grain legumes. Plant Physiology and Biochemistry, 118: 199-217.
  9. Gururani, M. A., Upadhyaya, C. P., Baskar, V., Venkatesh, J., Nookaraju, A., Park, S. W. (2013). Plant growth-promoting rhizobacteria enhance abiotic stress tolerance in Solanum tuberosum through inducing changes in the expression of ROS-scavenging enzymes and improved photosynthetic performance. Journal of Plant Growth Regulation, 32(2): 245-258.
  10. Hang, H.S. and Lee, K.D. (2005). Physiological responses of soybean –inoculation of Bradyrhizobium japonicum with PGPR in saline soil conditions. Research Journal of Agricultural and Biological Sciences, 1(3):216-221.
  11. Heidari, M. (2010). Nucleic acid metabolism, proline concentration and antioxidants enzyme activity in canola (Brassica nupus L.) under salinity stress. Agricultural Sciences in China, 9(4): 504-511. 
  12. Horie T., Kaneko T., Sugimoto G., Sasano S., Panda S.K., Shibasaka M., Katsuhara M. (2011). Mechanisms of water transport mediated by PIP aquaporins and their regulation via phosphorylation events under salinity stress in barley roots, Plant Cell Physiol,52: 663-675.
  13. Hussein, T.M., Chandrasekhar, T., Hazara, M., Sultan, Z., Saleh, B.K., Gopal, G.R. (2008). Recent advances in salt stress biology – a review. Biotechnology and Molecular Biology, 3 (1): 8-13. 
  14. Jamei, R., Heidari, R., Khara, J., Zare, S. (2009). Hypoxia Induced changes in the lipid peroxidation, membrane permeability, reactive oxygen species generation, and antioxidative response systems in Zea mays leaves. Turk. J. Biol, 33: 45-52. 
  15. Jebara, S., Jebara, M., Liman, F., Aouani, E. (2005). Changes in ascorbate peroxidase, catalase, guaicol peroxidase and superoxide dismutase activities in common bean nodules under salt stres. J. of Plant Physiol,162: 929-936.
  16. Khan, A., Zhao, X. Q., Javed, M. T., Khan, K. S., Bano, A., Shen, R. F., Masood, S. (2016). Bacillus pumilus enhances tolerance in rice (Oryza sativa L.) to combined stresses of NaCl and high boron due to limited uptake of Na+. Environmental and Experimental Botany, 124: 120-129.
  17. Kim, K., Jang, Y.J., Lee, S.M., Oh, B.T., Chae, J.C., Lee, K.J. (2014). Alleviation of salt stress by Enterobacter sp. EJ01 in tomato and Arabidopsis is accompanied by upregulation of conserved salinity responsive factors in plants. Mol. Cells,37: 109-117.
  18. Kim, S.Y., Lim, J.H., Park, M. R., Kim, Y.J., Park, T.I.I., Seo, Y.W., Choi, K.G., Yun, S.J., (2005). Enhanced antioxidant enzymes are associated with reduced hydrogen peroxide in barley roots under salt stress. J. Biochem. Mol. Biol, 38: 218–224.
  19. Kloepper, J. W., Reddy, M. S., Rodriguez K, R., Kenney, D. S., Kokalis B. N., Martinez O. N., Vavrina, C. S. (2004). Application for rhizobacteria in transplant production and yield enhancement. Acta Hort,631: 217-229.
  20. Koca, H., Bor, M., Ozdemir, F., Türkan, G. (2007). The effect of salt stress on lipid peroxidation, antioxidative enzymes and proline content of sesame cultivars. Environmental and Experimental Botany, 60: 344-351. 
  21. Kotan, R. and Sahin, F. (2002). First record of bacterial cancer by Pseudomonas syringae pv. syringae, on apricot trees in Turkey. Plant Pathology, 51: 798.
  22. Lata, C. and Prasad, M. (2011). Role of DREBs in regulation of abiotic stress responses in plants. J. Exp. Bot,62: 4731-4748.
  23. Li, H., Lei, P., Pang, X., Li, S., Xu, H., Xu, Z., Feng, X. (2017). Enhanced tolerance to salt stress in canola (Brassica napus L.) seedlings inoculated with the halotolerant Enterobacter cloacae HSNJ4. Applied Soil Ecology, 119: 26-34.
  24. Liang, W., Ma, X., Wan, P., Liu, L. (2014). Plant salt-tolerance mechanism: A review. Biochemical and Biophysical Research Communi- cations, 495(1): 286-291.
  25. Melchiorre, M., Quero, G.E., Parola, R., Racca, R., Trippi, V.S., Lascano, R. (2009). Physiological characterization of four model Lotus diploid genotypes: L. japonicus (MG20 and Gifu), L. filicaulis, and L. burttii under salt stress. Plant Science, 177: 618-628.
  26. Mittler, R. (2002). Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci.,7: 405-410.
  27. Noel, T. C., C. Sheng, C. K. Yost, R. P. Pharis., M. F. Hynes. (1996). Rhizobium leguminosarum as a plant growth-promoting rhizobacterium: direct growth promotion of canola and lettuce. Can J. Microbiol., 42:279-283.
  28. Rahnama, H. and Ebrahimzadeh, H. (2005). The effect of NaCl on antioxidant enzyme activities in potato seedlings. Biol. Planta, 49: 93-97.
  29. Reddy. M. S., Ryu, C. M., Zhang, S., Yan, Z., Kenney, D. S., Rodriguez K. R., Kloepper, J. W. (2000). Approaches for enhancing Pgpr-    mediated ýsr on varýous vegetable transplant plugs. Proc.5th Int. Conf. Plant Growth Promoting Rhizobacteria, Brasil.
  30. Sahin, F., Cakmakci, R., Kantar, F. (2004). Sugar beet and barley yields in relation to inoculation with N2-fixing and phosphate solubilizing bacteria. Plant Soil, 265: 123-129.
  31. Sairam, R. K., Srivastava, G. C., Agarwal, S., Meena, R. C. (2005). Differences in antioxidant activity in response to salinity stres in tolerant and susceptible wheat genotypes. Biol. Planta,49: 85-91.
  32. Sairam, R.K. and Saxena, D.C,. (2000). Oxidative stres and antioksidants in wheat genotypes: possible mechanism of water stres tolerance. J. Agron. and Crop Science,184: 55-61.
  33. Sevengor, S., Yasar, F., Kusvuran, S., Ellialtioglu, S. (2011). The effect of salt stress on growth, chlorophyll content, lipid peroxidation and antioxidative enzymes of pumpkin seedling. African Journal of Agricultural Research, 6(21): 4920-4924.
  34. Smirhoff, N. (1993). The role of active oxygen in the response of plants to water deficit and desiccation. New Phytol., 186:69-74.
  35. Turhan, O. and Emekci, Y. (2008). Soðuk stresinin bitkiler üzerine etkileri ve tolerans mekanizmalarý. Anadolu Üniversitesi Bilim Ve Teknoloji Dergisi,2: 177-198.
  36. Velikova, P., Yordanov, I., Edreva, A. (2000). Oxidative stress and some antioxidant systems in acid rain-treated bean plants: Protective role of exogenous polyamines. Plant Science, 15: 59–66.
  37. Younesi, O. and Moradi A. (2014). Effects of plant growth promoting rhizobacterium (PGPR) and arbuscular mycorrhizal fungus (AM) on antioxidant enzyme activities in salt stressed bean (Phaseolus vulgaris L.). Agriculture, 60: 10-21. 
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    Research Article

    volume 42 issue 1 (february 2019) : 72-76,   Doi: 10.18805/LR-435

    The effects of plant growth promoting rhizobacteria on antioxidant activity in chickpea (Cicer arietinum L.) under salt stress
     

    H
    Hilal Yilmaz
    H
    Haluk Kulaz
    1Department of Field Crops, Faculty of Agriculture, Yuzuncu Yil University, 65080 Van, Turkey.

    • Submitted05-06-2018|

    • Accepted06-10-2018|

    • First Online 07-12-2018|

    • doi 10.18805/LR-435

    Cite article:- Yilmaz Hilal, Kulaz Haluk (2018). The effects of plant growth promoting rhizobacteria on antioxidant activity in chickpea (Cicer arietinum L.) under salt stress. Legume Research. 42(1): 72-76. doi: 10.18805/LR-435.

    ABSTRACT

    In chickpea soil salinity is one of the most important factors affecting yield, nodulation and physiological events. Salinity affects the growth of salt sensitive varieties. The inoculation of plant growth promoting rhizobacteria (PGPR) allows to reduce the harmful effects of salinity. To prevent adverse effects of chickpea salinity, the effects of four bacteria (Rhizobium ciceri, A-08, EB-80 and Isolate-30) in root rhizosphere under controlled environmental growth conditions were studied. This study has shown that PGPRs play an important role in growth regulators for the positive development of plants under salt stress. It has been observed that these isolates, common in roots, are tolerant to salinity antioxidant activity and an increase in proline, MDA, APX, SOD and CAT concentrations were found under saline conditions when unvaccinated plants were compared with grafted plants. The results also suggested that inoculated PGPR strains can reduce salinity stress by increasing salt tolerance.

    REFERENCES

    1. Akgül, D. S. and Mirik, M. (2008). Biocontrol of Phytophthora Capsici on pepper plants by Bacillus megnaterium strains. Journal of Plant Patholology, 90 (1): 29-34.
    2. Ashraf, M., Berge S.H., and Mahmood O.T. (2004). Inoculation wheat seedlings with exopolysaccharide-producing bacteria restricts sodium uptake and stimulates plant growth under salt stree. Biol. Fer. Soils.40:157-162.
    3. Aslantas, R., Cakmakcý, R., Sahin, F. (2007). Effect of plant growth promoting rhizobacteria on young apple tree growth and fruit yield under orchard conditions. Science Horticulture,111: 371–377.
    4. Cakmakci, R. (2006). Bitki geliþme promotörü rizobakteri kullanýmýndaki son geliþmeler: organik tarým perspektif ve uygulamalarý. Organik Tarým Kongresi. Yalova.
    5. Cakmakci, R., Dönmez, M. F., Erdoðan, Ü. (2007 a). The effect of plant growth promoting rhizobacteria on barley seedling growth, nutrient uptake, some soil properties, and bacterial counts. Turkish J. Agric. For,31: 189-199.
    6. Cakmakci, R., Erat, M., Erdoðan, Ü., Dönmez, F. (2007b). The influence of plant growth-promoting rhizobacteria on growth and enzyme activities in wheat and spinach plants. J. Plant Nutr. Soil Science,170: 288-295.
    7. del Rio, L. A., Corpas F. J., Sandalio L. M., Palma J. M., Barroso J. B. (2003). Plant peroxisomes, reactive oxygen metabolism and nitric oxide. IUBMB Life, 55:71-81. 
    8. Farooq, M., Gogoi, N., Hussain, M., Barthakur, S., Paul, S., Bharadwaj, N., Migdadi, M.H., Alghamdi, S.S., Siddique, K. H. (2017). Effects, tolerance mechanisms and management of salt stress in grain legumes. Plant Physiology and Biochemistry, 118: 199-217.
    9. Gururani, M. A., Upadhyaya, C. P., Baskar, V., Venkatesh, J., Nookaraju, A., Park, S. W. (2013). Plant growth-promoting rhizobacteria enhance abiotic stress tolerance in Solanum tuberosum through inducing changes in the expression of ROS-scavenging enzymes and improved photosynthetic performance. Journal of Plant Growth Regulation, 32(2): 245-258.
    10. Hang, H.S. and Lee, K.D. (2005). Physiological responses of soybean –inoculation of Bradyrhizobium japonicum with PGPR in saline soil conditions. Research Journal of Agricultural and Biological Sciences, 1(3):216-221.
    11. Heidari, M. (2010). Nucleic acid metabolism, proline concentration and antioxidants enzyme activity in canola (Brassica nupus L.) under salinity stress. Agricultural Sciences in China, 9(4): 504-511. 
    12. Horie T., Kaneko T., Sugimoto G., Sasano S., Panda S.K., Shibasaka M., Katsuhara M. (2011). Mechanisms of water transport mediated by PIP aquaporins and their regulation via phosphorylation events under salinity stress in barley roots, Plant Cell Physiol,52: 663-675.
    13. Hussein, T.M., Chandrasekhar, T., Hazara, M., Sultan, Z., Saleh, B.K., Gopal, G.R. (2008). Recent advances in salt stress biology – a review. Biotechnology and Molecular Biology, 3 (1): 8-13. 
    14. Jamei, R., Heidari, R., Khara, J., Zare, S. (2009). Hypoxia Induced changes in the lipid peroxidation, membrane permeability, reactive oxygen species generation, and antioxidative response systems in Zea mays leaves. Turk. J. Biol, 33: 45-52. 
    15. Jebara, S., Jebara, M., Liman, F., Aouani, E. (2005). Changes in ascorbate peroxidase, catalase, guaicol peroxidase and superoxide dismutase activities in common bean nodules under salt stres. J. of Plant Physiol,162: 929-936.
    16. Khan, A., Zhao, X. Q., Javed, M. T., Khan, K. S., Bano, A., Shen, R. F., Masood, S. (2016). Bacillus pumilus enhances tolerance in rice (Oryza sativa L.) to combined stresses of NaCl and high boron due to limited uptake of Na+. Environmental and Experimental Botany, 124: 120-129.
    17. Kim, K., Jang, Y.J., Lee, S.M., Oh, B.T., Chae, J.C., Lee, K.J. (2014). Alleviation of salt stress by Enterobacter sp. EJ01 in tomato and Arabidopsis is accompanied by upregulation of conserved salinity responsive factors in plants. Mol. Cells,37: 109-117.
    18. Kim, S.Y., Lim, J.H., Park, M. R., Kim, Y.J., Park, T.I.I., Seo, Y.W., Choi, K.G., Yun, S.J., (2005). Enhanced antioxidant enzymes are associated with reduced hydrogen peroxide in barley roots under salt stress. J. Biochem. Mol. Biol, 38: 218–224.
    19. Kloepper, J. W., Reddy, M. S., Rodriguez K, R., Kenney, D. S., Kokalis B. N., Martinez O. N., Vavrina, C. S. (2004). Application for rhizobacteria in transplant production and yield enhancement. Acta Hort,631: 217-229.
    20. Koca, H., Bor, M., Ozdemir, F., Türkan, G. (2007). The effect of salt stress on lipid peroxidation, antioxidative enzymes and proline content of sesame cultivars. Environmental and Experimental Botany, 60: 344-351. 
    21. Kotan, R. and Sahin, F. (2002). First record of bacterial cancer by Pseudomonas syringae pv. syringae, on apricot trees in Turkey. Plant Pathology, 51: 798.
    22. Lata, C. and Prasad, M. (2011). Role of DREBs in regulation of abiotic stress responses in plants. J. Exp. Bot,62: 4731-4748.
    23. Li, H., Lei, P., Pang, X., Li, S., Xu, H., Xu, Z., Feng, X. (2017). Enhanced tolerance to salt stress in canola (Brassica napus L.) seedlings inoculated with the halotolerant Enterobacter cloacae HSNJ4. Applied Soil Ecology, 119: 26-34.
    24. Liang, W., Ma, X., Wan, P., Liu, L. (2014). Plant salt-tolerance mechanism: A review. Biochemical and Biophysical Research Communi- cations, 495(1): 286-291.
    25. Melchiorre, M., Quero, G.E., Parola, R., Racca, R., Trippi, V.S., Lascano, R. (2009). Physiological characterization of four model Lotus diploid genotypes: L. japonicus (MG20 and Gifu), L. filicaulis, and L. burttii under salt stress. Plant Science, 177: 618-628.
    26. Mittler, R. (2002). Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci.,7: 405-410.
    27. Noel, T. C., C. Sheng, C. K. Yost, R. P. Pharis., M. F. Hynes. (1996). Rhizobium leguminosarum as a plant growth-promoting rhizobacterium: direct growth promotion of canola and lettuce. Can J. Microbiol., 42:279-283.
    28. Rahnama, H. and Ebrahimzadeh, H. (2005). The effect of NaCl on antioxidant enzyme activities in potato seedlings. Biol. Planta, 49: 93-97.
    29. Reddy. M. S., Ryu, C. M., Zhang, S., Yan, Z., Kenney, D. S., Rodriguez K. R., Kloepper, J. W. (2000). Approaches for enhancing Pgpr-    mediated ýsr on varýous vegetable transplant plugs. Proc.5th Int. Conf. Plant Growth Promoting Rhizobacteria, Brasil.
    30. Sahin, F., Cakmakci, R., Kantar, F. (2004). Sugar beet and barley yields in relation to inoculation with N2-fixing and phosphate solubilizing bacteria. Plant Soil, 265: 123-129.
    31. Sairam, R. K., Srivastava, G. C., Agarwal, S., Meena, R. C. (2005). Differences in antioxidant activity in response to salinity stres in tolerant and susceptible wheat genotypes. Biol. Planta,49: 85-91.
    32. Sairam, R.K. and Saxena, D.C,. (2000). Oxidative stres and antioksidants in wheat genotypes: possible mechanism of water stres tolerance. J. Agron. and Crop Science,184: 55-61.
    33. Sevengor, S., Yasar, F., Kusvuran, S., Ellialtioglu, S. (2011). The effect of salt stress on growth, chlorophyll content, lipid peroxidation and antioxidative enzymes of pumpkin seedling. African Journal of Agricultural Research, 6(21): 4920-4924.
    34. Smirhoff, N. (1993). The role of active oxygen in the response of plants to water deficit and desiccation. New Phytol., 186:69-74.
    35. Turhan, O. and Emekci, Y. (2008). Soðuk stresinin bitkiler üzerine etkileri ve tolerans mekanizmalarý. Anadolu Üniversitesi Bilim Ve Teknoloji Dergisi,2: 177-198.
    36. Velikova, P., Yordanov, I., Edreva, A. (2000). Oxidative stress and some antioxidant systems in acid rain-treated bean plants: Protective role of exogenous polyamines. Plant Science, 15: 59–66.
    37. Younesi, O. and Moradi A. (2014). Effects of plant growth promoting rhizobacterium (PGPR) and arbuscular mycorrhizal fungus (AM) on antioxidant enzyme activities in salt stressed bean (Phaseolus vulgaris L.). Agriculture, 60: 10-21. 
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