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Research article

Environmental Microbiology and Biotechnology (EMB)  |  Agricultural Microbiology

Alleviation of Salt Stress in Pepper (Capsicum annum L.) Plants by Plant Growth-Promoting Rhizobacteria

Mi-Seon Hahm 1, Jin-Soo Son 1, Ye-Ji Hwang 1, Duk-Kee Kwon 2 and Sa-Youl Ghim 1*

1School of Life Science, Institute for Microorganisms, and BK21 Plus KNU Creative BioResearch Group, Kyungpook National University, Daegu 41566, Republic of Korea, 2Department of Biology Education, Kyungpook National University, Daegu 41566, Republic of Korea

Received: September 23, 2016; Accepted: August 4, 2017

J. Microbiol. Biotechnol. 2017; 27(10): 1790-1797

Published October 28, 2017 https://doi.org/10.4014/jmb.1609.09042

Copyright © The Korean Society for Microbiology and Biotechnology.

Abstract

In the present study, we demonstrate that the growth of salt-stressed pepper plants is improved by inoculation with plant growth-promoting rhizobacteria (PGPR). Three PGPR strains (Microbacterium oleivorans KNUC7074, Brevibacterium iodinum KNUC7183, and Rhizobium massiliae KNUC7586) were isolated from the rhizosphere of pepper plants growing in saline soil, and pepper plants inoculated with these PGPR strains exhibited significantly greater plant height, fresh weight, dry weight, and total chlorophyll content than noninoculated plants. In addition, salt-stressed pepper plants that were inoculated with B. iodinum KNUC7183 and R. massiliae KNUC7586 possessed significantly different total soluble sugar and proline contents from non-inoculated controls, and the activity of several antioxidant enzymes (ascorbate peroxidase, guaiacol peroxidase, and catalase) was also elevated in PGPRtreated plants under salt stress. Overall, these results suggest that the inoculation of pepper plants with M. oleivorans KNUC7074, B. iodinum KNUC7183, and R. massiliae KNUC7586 can alleviate the harmful effects of salt stress on plant growth.

Keywords

Salt stress, plant growth-promoting rhizobacteria, pepper, antioxidant enzyme, proline, total soluble sugar

References

  1. Bano A, Fatima M. 2009. Salt tolerance in Zea mays (L). following inoculation with Rhizobium and Pseudomonas. Biol. Fert. Soils 45: 405-413.
    CrossRef
  2. Munns R, Tester M. 2008. Mechanisms of salinity tolerance. Annu. Rev. Plant Biol. 59: 651-681.
    Pubmed CrossRef
  3. Schubert S, Neubert A, Schierholt A, Sumer A, Zorb C. 2009. Development of salt-resistant maize hybrids: the combination of physiological strategies using conventional breeding methods. Plant Sci. 177: 196-202.
    CrossRef
  4. Ahmad M, Zahir ZA, Nazli F, Akram F, Arshad M, Khalid M. 2013. Effectiveness of halo-tolerant, auxin producing Pseudomonas and Rhizobium strains to improve osmotic stress tolerance in mung bean (Vigna radiata L.). Braz. J. Microbiol. 44: 1341-1348.
    Pubmed CrossRef
  5. Bharti N, Yadav D, Barnawal D, Maji D, Kalra A. 2013. Exiguobacterium oxidotolerans, a halotolerant plant growth promoting rhizobacteria, improves yield and content of secondary metabolites in Bacopa monnieri (L.) Pennell under primary and secondary salt stress. World J. Microbiol. Biotechnol. 29: 379-387.
    Pubmed CrossRef
  6. Hamdia ABE, Shaddad MAK, Doaa MM. 2004. Mechanisms of salt tolerance and interactive effects of Azospirillum brasilense inoculation on maize cultivars grown under salt stress conditions. Plant Growth Regul. 44: 165-174.
    CrossRef
  7. Kohler J, Hernandez JA, Caravaca F, Roldan A. 2009. Induction of antioxidant enzymes is involved in the greater effectiveness of a PGPR versus AM fungi with respect to increasing the tolerance of lettuce to severe salt stress. Environ. Exp. Bot. 65: 245-252.
    CrossRef
  8. Shukla PS, Agarwal PK, Jha B. 2012. Improved salinity tolerance of Arachis hypogaea (L.) by the interaction of halotolerant plant-growth-promoting rhizobacteria. J. Plant Growth Regul. 31: 195-206.
    CrossRef
  9. Egamberdiyeva D, Islam KR. 2008. Salt-tolerant rhizobacteria:plant growth promoting traits and physiological characterization within ecologically stressed environments, pp. 257-281. In Ahmad I, Pichtel J, Hayat S (eds.), Plant-Bacteria Interactions. Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim, Germany.
    CrossRef
  10. Tank N, Saraf M. 2010. Salinity-resistant plant growth promoting rhizobacteria ameliorates sodium chloride stress on tomato plants. J. Plant Interact. 5: 51-58.
    CrossRef
  11. Siddikee MA, Glick BR, Chauhan PS, Yim WJ, Sa TM. 2011. Enhancement of growth and salt tolerance of red pepper seedlings (Capsicum annuum L.) by regulating stress ethylene synthesis with halotolerant bacteria containing 1-aminocyclopropane-1-carboxylic acid deaminase activity. Plant Physiol. Biochem. 49: 427-434.
    Pubmed CrossRef
  12. Ahmad M, Zahir ZA, Asghar HN, Arshad M. 2012. The combined application of rhizobial strains and plant growth promoting rhizobacteria improves growth and productivity of mung bean (Vigna radiata L.) under salt-stressed conditions. Ann. Microbiol. 62: 1321-1330.
    CrossRef
  13. Gururani MA, Upadhyaya CP, Baskar V, Venkatesh J, Nookaraju A, Park SW. 2012. 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. J. Plant Growth Regul. 32: 245-258.
    CrossRef
  14. Habib SH, Kausar H, Saud HM. 2016. Plant growth-promoting rhizobacteria enhance salinity stress tolerance in Okra through ROS-scavenging enzymes. Biomed Res. Int. 2016: 10.
    Pubmed PMC CrossRef
  15. Sang MK, Chun SC, Kim KD. 2008. Biological control of Phytophthora blight of pepper by antagonistic rhizobacteria selected from a sequential screening procedure. Biol. Control 46: 424-433.
    CrossRef
  16. Dodd IC, Perez-Alfocea F. 2012. Microbial amelioration of crop salinity stress. J. Exp. Bot. 63: 3415-3428.
    Pubmed CrossRef
  17. Yang J, Kloepper JW, Ryu CM. 2009. Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci. 14: 1-4.
    Pubmed CrossRef
  18. Hahm MS, Son JS, Kim BS, Ghim SY. 2017. Comparative study of rhizobacterial communities in pepper greenhouses and examination of the effects of salt accumulation under different cropping systems. Arch. Microbiol. 199: 303-315.
    Pubmed CrossRef
  19. González L, González-Vilar M. 2001. Determination of relative water content, pp. 207-212. In Reigosa Roger MJ (ed.), Handbook of Plant Ecophysiology Techniques. Springer Netherlands, Dordrecht.
    Pubmed
  20. Arnon DI. 1949. Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol. 24: 1-15.
    Pubmed PMC CrossRef
  21. Asada K. 1992. Ascorbate peroxidase - a hydrogen peroxidescavenging enzyme in plants. Physiol. Plant 85: 235-241.
    CrossRef
  22. Upadhyay SK, Singh JS, Saxena AK, Singh DP. 2012. Impact of PGPR inoculation on growth and antioxidant status of wheat under saline conditions. Plant Biol. 14: 605-611.
    Pubmed CrossRef
  23. Hammerschmidt R, Nuckles EM, Kuć J. 1982. Association of enhanced peroxidase activity with induced systemic resistance of cucumber to Colletotrichum lagenarium. Physiol. Plant Pathol. 20: 73-82.
    CrossRef
  24. Bates LS, Waldren RP, Teare ID. 1973. Rapid determination of free proline for water-stress studies. Plant Soil 39: 205-207.
    CrossRef
  25. Irigoyen JJ, Einerich DW, Sánchez-Díaz M. 1992. Water stress induced changes in concentrations of proline and total soluble sugars in nodulated alfalfa (Medicago sativd) plants. Physiol. Plant 84: 55-60.
    CrossRef
  26. Han HS, Lee KD. 2005. Plant growth-promoting rhizobacteria:effect on antioxidant status, photosynthesis, mineral uptake and growth of lettuce under soil salinity. Res. J. Agric. Biol. Sci. 1: 210-215.
  27. Barassi CA, Ayrault G, Creus CM, Sueldo RJ, Sobrero MT. 2006. Seed inoculation with Azospirillum mitigates NaCl effects on lettuce. Sci. Hort. 109: 8-14.
    CrossRef
  28. Mayak S, Tirosh T, Glick BR. 2004. Plant growth-promoting bacteria that confer resistance to water stress in tomatoes and peppers. Plant Sci. 166: 525-530.
    CrossRef
  29. Nadeem SM, Zahir ZA, Naveed M, Arshad M. 2007. Preliminary investigations on inducing salt tolerance in maize through inoculation with rhizobacteria containing ACC deaminase activity. Can. J. Microbiol. 53: 1141-1149.
    Pubmed CrossRef
  30. Pick U, Rental M, Chitlaru E, Weiss M. 1990. Polyphosphatehydrolysis - a protective mechanism against alkaline stress? FEBS Lett. 274: 15-18.
    CrossRef
  31. Weisany W, Sohrabi Y, Heidari G, Siosemardeh A, GhassemiGolezani K. 2012. Changes in antioxidant enzymes activity and plant performance by salinity stress and zinc application in soybean (Glycine max L.). Plant Omics 5: 60-67.
  32. Zaidi PH, Rafique S, Rai PK, Singh NN, Srinivasan G. 2004. Tolerance to excess moisture in maize (Zea mays L.): susceptible crop stages and identification of tolerant genotypes. Field Crops Res. 90: 189-202.
    CrossRef
  33. Afzal I, Basra SMA, Iqbal A. 2005. The effects of seed soaking with plant growth regulators on seedling vigor of wheat under salinity stress. J. Stress Physiol. Biochem. 1: 6-14.
  34. Spaepen S, Vanderleyden J. 2011. Auxin and plant-microbe interactions. Cold Spring Harb. Perspect. Biol. 3: a001438.
    Pubmed PMC CrossRef
  35. Dimkpa C, Svatoš A, Merten D, Büchel G, Kothe E. 2008. Hydroxamate siderophores produced by Streptomyces acidiscabies E13 bind nickel and promote growth in cowpea (Vigna unguiculata L.) under nickel stress. Can. J. Microbiol. 54: 163-172.
    Pubmed CrossRef
  36. Dimkpa CO, Merten D, Svatoš A, Büchel G, Kothe E. 2009. Siderophores mediate reduced and increased uptake of cadmium by Streptomyces tendae F4 and sunflower (Helianthus annuus), respectively. J. Appl. Microbiol. 107: 1687-1696.
    Pubmed CrossRef
  37. Egamberdiyeva D. 2007. The effect of plant growth promoting bacteria on growth and nutrient uptake of maize in two different soils. Appl. Soil Ecol. 36: 184-189.
    CrossRef
  38. Dimkpa C, Weinand T, Asch F. 2009. Plant-rhizobacteria interactions alleviate abiotic stress conditions. Plant Cell Environ. 32: 1682-1694.
    Pubmed CrossRef
  39. Karlidag H, Yildirim E, Turan M, Pehluvan M, Donmez F. 2013. Plant growth promoting rhizobacteria mitigate deleterious effects of salt stress on strawberry plants (Fragaria ananassa). Hort. Sci. 48: 563-567.
  40. Paczkowska M, Kozlowska M, Golinski P. 2007. Oxidative stress enzyme activity in Lemna minor L. exposed to cadmium and lead. Acta Biol. Cracov. Bot. 49: 33-37.
  41. Caverzan A, Passaia G, Rosa SB, Ribeiro CW, Lazzarotto F, Margis-Pinheiro M. 2012. Plant responses to stresses: role of ascorbate peroxidase in the antioxidant protection. Genet. Mol. Biol. 35: 1011-1019.
    Pubmed PMC CrossRef
  42. Debez A, Chaibi W, Bouzid S. 2001. Effect of NaCl and growth regulators on germination of Atriplex halimus L. Cahiers Agricultures 10: 135-138.
  43. Kerepesi I, Galiba G. 2000. Osmotic and salt stress-induced alteration in soluble carbohydrate content in wheat seedlings. Crop Sci. 40: 482-487.
    CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2017; 27(10): 1790-1797

Published online October 28, 2017 https://doi.org/10.4014/jmb.1609.09042

Copyright © The Korean Society for Microbiology and Biotechnology.

Alleviation of Salt Stress in Pepper (Capsicum annum L.) Plants by Plant Growth-Promoting Rhizobacteria

Mi-Seon Hahm 1, Jin-Soo Son 1, Ye-Ji Hwang 1, Duk-Kee Kwon 2 and Sa-Youl Ghim 1*

1School of Life Science, Institute for Microorganisms, and BK21 Plus KNU Creative BioResearch Group, Kyungpook National University, Daegu 41566, Republic of Korea, 2Department of Biology Education, Kyungpook National University, Daegu 41566, Republic of Korea

Received: September 23, 2016; Accepted: August 4, 2017

Abstract

In the present study, we demonstrate that the growth of salt-stressed pepper plants is
improved by inoculation with plant growth-promoting rhizobacteria (PGPR). Three PGPR
strains (Microbacterium oleivorans KNUC7074, Brevibacterium iodinum KNUC7183, and
Rhizobium massiliae KNUC7586) were isolated from the rhizosphere of pepper plants growing
in saline soil, and pepper plants inoculated with these PGPR strains exhibited significantly
greater plant height, fresh weight, dry weight, and total chlorophyll content than noninoculated
plants. In addition, salt-stressed pepper plants that were inoculated with B. iodinum
KNUC7183 and R. massiliae KNUC7586 possessed significantly different total soluble sugar
and proline contents from non-inoculated controls, and the activity of several antioxidant
enzymes (ascorbate peroxidase, guaiacol peroxidase, and catalase) was also elevated in PGPRtreated
plants under salt stress. Overall, these results suggest that the inoculation of pepper
plants with M. oleivorans KNUC7074, B. iodinum KNUC7183, and R. massiliae KNUC7586 can
alleviate the harmful effects of salt stress on plant growth.

Keywords: Salt stress, plant growth-promoting rhizobacteria, pepper, antioxidant enzyme, proline, total soluble sugar

References

  1. Bano A, Fatima M. 2009. Salt tolerance in Zea mays (L). following inoculation with Rhizobium and Pseudomonas. Biol. Fert. Soils 45: 405-413.
    CrossRef
  2. Munns R, Tester M. 2008. Mechanisms of salinity tolerance. Annu. Rev. Plant Biol. 59: 651-681.
    Pubmed CrossRef
  3. Schubert S, Neubert A, Schierholt A, Sumer A, Zorb C. 2009. Development of salt-resistant maize hybrids: the combination of physiological strategies using conventional breeding methods. Plant Sci. 177: 196-202.
    CrossRef
  4. Ahmad M, Zahir ZA, Nazli F, Akram F, Arshad M, Khalid M. 2013. Effectiveness of halo-tolerant, auxin producing Pseudomonas and Rhizobium strains to improve osmotic stress tolerance in mung bean (Vigna radiata L.). Braz. J. Microbiol. 44: 1341-1348.
    Pubmed CrossRef
  5. Bharti N, Yadav D, Barnawal D, Maji D, Kalra A. 2013. Exiguobacterium oxidotolerans, a halotolerant plant growth promoting rhizobacteria, improves yield and content of secondary metabolites in Bacopa monnieri (L.) Pennell under primary and secondary salt stress. World J. Microbiol. Biotechnol. 29: 379-387.
    Pubmed CrossRef
  6. Hamdia ABE, Shaddad MAK, Doaa MM. 2004. Mechanisms of salt tolerance and interactive effects of Azospirillum brasilense inoculation on maize cultivars grown under salt stress conditions. Plant Growth Regul. 44: 165-174.
    CrossRef
  7. Kohler J, Hernandez JA, Caravaca F, Roldan A. 2009. Induction of antioxidant enzymes is involved in the greater effectiveness of a PGPR versus AM fungi with respect to increasing the tolerance of lettuce to severe salt stress. Environ. Exp. Bot. 65: 245-252.
    CrossRef
  8. Shukla PS, Agarwal PK, Jha B. 2012. Improved salinity tolerance of Arachis hypogaea (L.) by the interaction of halotolerant plant-growth-promoting rhizobacteria. J. Plant Growth Regul. 31: 195-206.
    CrossRef
  9. Egamberdiyeva D, Islam KR. 2008. Salt-tolerant rhizobacteria:plant growth promoting traits and physiological characterization within ecologically stressed environments, pp. 257-281. In Ahmad I, Pichtel J, Hayat S (eds.), Plant-Bacteria Interactions. Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim, Germany.
    CrossRef
  10. Tank N, Saraf M. 2010. Salinity-resistant plant growth promoting rhizobacteria ameliorates sodium chloride stress on tomato plants. J. Plant Interact. 5: 51-58.
    CrossRef
  11. Siddikee MA, Glick BR, Chauhan PS, Yim WJ, Sa TM. 2011. Enhancement of growth and salt tolerance of red pepper seedlings (Capsicum annuum L.) by regulating stress ethylene synthesis with halotolerant bacteria containing 1-aminocyclopropane-1-carboxylic acid deaminase activity. Plant Physiol. Biochem. 49: 427-434.
    Pubmed CrossRef
  12. Ahmad M, Zahir ZA, Asghar HN, Arshad M. 2012. The combined application of rhizobial strains and plant growth promoting rhizobacteria improves growth and productivity of mung bean (Vigna radiata L.) under salt-stressed conditions. Ann. Microbiol. 62: 1321-1330.
    CrossRef
  13. Gururani MA, Upadhyaya CP, Baskar V, Venkatesh J, Nookaraju A, Park SW. 2012. 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. J. Plant Growth Regul. 32: 245-258.
    CrossRef
  14. Habib SH, Kausar H, Saud HM. 2016. Plant growth-promoting rhizobacteria enhance salinity stress tolerance in Okra through ROS-scavenging enzymes. Biomed Res. Int. 2016: 10.
    Pubmed KoreaMed CrossRef
  15. Sang MK, Chun SC, Kim KD. 2008. Biological control of Phytophthora blight of pepper by antagonistic rhizobacteria selected from a sequential screening procedure. Biol. Control 46: 424-433.
    CrossRef
  16. Dodd IC, Perez-Alfocea F. 2012. Microbial amelioration of crop salinity stress. J. Exp. Bot. 63: 3415-3428.
    Pubmed CrossRef
  17. Yang J, Kloepper JW, Ryu CM. 2009. Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci. 14: 1-4.
    Pubmed CrossRef
  18. Hahm MS, Son JS, Kim BS, Ghim SY. 2017. Comparative study of rhizobacterial communities in pepper greenhouses and examination of the effects of salt accumulation under different cropping systems. Arch. Microbiol. 199: 303-315.
    Pubmed CrossRef
  19. González L, González-Vilar M. 2001. Determination of relative water content, pp. 207-212. In Reigosa Roger MJ (ed.), Handbook of Plant Ecophysiology Techniques. Springer Netherlands, Dordrecht.
    Pubmed
  20. Arnon DI. 1949. Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol. 24: 1-15.
    Pubmed KoreaMed CrossRef
  21. Asada K. 1992. Ascorbate peroxidase - a hydrogen peroxidescavenging enzyme in plants. Physiol. Plant 85: 235-241.
    CrossRef
  22. Upadhyay SK, Singh JS, Saxena AK, Singh DP. 2012. Impact of PGPR inoculation on growth and antioxidant status of wheat under saline conditions. Plant Biol. 14: 605-611.
    Pubmed CrossRef
  23. Hammerschmidt R, Nuckles EM, Kuć J. 1982. Association of enhanced peroxidase activity with induced systemic resistance of cucumber to Colletotrichum lagenarium. Physiol. Plant Pathol. 20: 73-82.
    CrossRef
  24. Bates LS, Waldren RP, Teare ID. 1973. Rapid determination of free proline for water-stress studies. Plant Soil 39: 205-207.
    CrossRef
  25. Irigoyen JJ, Einerich DW, Sánchez-Díaz M. 1992. Water stress induced changes in concentrations of proline and total soluble sugars in nodulated alfalfa (Medicago sativd) plants. Physiol. Plant 84: 55-60.
    CrossRef
  26. Han HS, Lee KD. 2005. Plant growth-promoting rhizobacteria:effect on antioxidant status, photosynthesis, mineral uptake and growth of lettuce under soil salinity. Res. J. Agric. Biol. Sci. 1: 210-215.
  27. Barassi CA, Ayrault G, Creus CM, Sueldo RJ, Sobrero MT. 2006. Seed inoculation with Azospirillum mitigates NaCl effects on lettuce. Sci. Hort. 109: 8-14.
    CrossRef
  28. Mayak S, Tirosh T, Glick BR. 2004. Plant growth-promoting bacteria that confer resistance to water stress in tomatoes and peppers. Plant Sci. 166: 525-530.
    CrossRef
  29. Nadeem SM, Zahir ZA, Naveed M, Arshad M. 2007. Preliminary investigations on inducing salt tolerance in maize through inoculation with rhizobacteria containing ACC deaminase activity. Can. J. Microbiol. 53: 1141-1149.
    Pubmed CrossRef
  30. Pick U, Rental M, Chitlaru E, Weiss M. 1990. Polyphosphatehydrolysis - a protective mechanism against alkaline stress? FEBS Lett. 274: 15-18.
    CrossRef
  31. Weisany W, Sohrabi Y, Heidari G, Siosemardeh A, GhassemiGolezani K. 2012. Changes in antioxidant enzymes activity and plant performance by salinity stress and zinc application in soybean (Glycine max L.). Plant Omics 5: 60-67.
  32. Zaidi PH, Rafique S, Rai PK, Singh NN, Srinivasan G. 2004. Tolerance to excess moisture in maize (Zea mays L.): susceptible crop stages and identification of tolerant genotypes. Field Crops Res. 90: 189-202.
    CrossRef
  33. Afzal I, Basra SMA, Iqbal A. 2005. The effects of seed soaking with plant growth regulators on seedling vigor of wheat under salinity stress. J. Stress Physiol. Biochem. 1: 6-14.
  34. Spaepen S, Vanderleyden J. 2011. Auxin and plant-microbe interactions. Cold Spring Harb. Perspect. Biol. 3: a001438.
    Pubmed KoreaMed CrossRef
  35. Dimkpa C, Svatoš A, Merten D, Büchel G, Kothe E. 2008. Hydroxamate siderophores produced by Streptomyces acidiscabies E13 bind nickel and promote growth in cowpea (Vigna unguiculata L.) under nickel stress. Can. J. Microbiol. 54: 163-172.
    Pubmed CrossRef
  36. Dimkpa CO, Merten D, Svatoš A, Büchel G, Kothe E. 2009. Siderophores mediate reduced and increased uptake of cadmium by Streptomyces tendae F4 and sunflower (Helianthus annuus), respectively. J. Appl. Microbiol. 107: 1687-1696.
    Pubmed CrossRef
  37. Egamberdiyeva D. 2007. The effect of plant growth promoting bacteria on growth and nutrient uptake of maize in two different soils. Appl. Soil Ecol. 36: 184-189.
    CrossRef
  38. Dimkpa C, Weinand T, Asch F. 2009. Plant-rhizobacteria interactions alleviate abiotic stress conditions. Plant Cell Environ. 32: 1682-1694.
    Pubmed CrossRef
  39. Karlidag H, Yildirim E, Turan M, Pehluvan M, Donmez F. 2013. Plant growth promoting rhizobacteria mitigate deleterious effects of salt stress on strawberry plants (Fragaria ananassa). Hort. Sci. 48: 563-567.
  40. Paczkowska M, Kozlowska M, Golinski P. 2007. Oxidative stress enzyme activity in Lemna minor L. exposed to cadmium and lead. Acta Biol. Cracov. Bot. 49: 33-37.
  41. Caverzan A, Passaia G, Rosa SB, Ribeiro CW, Lazzarotto F, Margis-Pinheiro M. 2012. Plant responses to stresses: role of ascorbate peroxidase in the antioxidant protection. Genet. Mol. Biol. 35: 1011-1019.
    Pubmed KoreaMed CrossRef
  42. Debez A, Chaibi W, Bouzid S. 2001. Effect of NaCl and growth regulators on germination of Atriplex halimus L. Cahiers Agricultures 10: 135-138.
  43. Kerepesi I, Galiba G. 2000. Osmotic and salt stress-induced alteration in soluble carbohydrate content in wheat seedlings. Crop Sci. 40: 482-487.
    CrossRef