Eurasian Journal of Soil Science

Volume 8, Issue 2, Apr 2019, Pages 159 - 166
DOI: 10.18393/ejss.544747
Stable URL: http://ejss.fess.org/10.18393/ejss.544747
Copyright © 2019 The authors and Federation of Eurasian Soil Science Societies



Relative potential of rhizobium species to enhance the growth and yield attributes of cotton (Gossypium hirsutum L.)

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Qureshi,M., Shahzad,H., Saeed,M., Ullah,S., Ali,M., Mujeeb,F., Anjum,M., 2019. Relative potential of rhizobium species to enhance the growth and yield attributes of cotton (Gossypium hirsutum L.). Eurasian J Soil Sci 8(2):159 - 166. DOI : 10.18393/ejss.544747
Qureshi,M.,Shahzad,H.Saeed,M.Ullah,S.Ali,M.Mujeeb,F.,& Anjum,M. Relative potential of rhizobium species to enhance the growth and yield attributes of cotton (Gossypium hirsutum L.) Eurasian Journal of Soil Science, 8(2):159 - 166. DOI : 10.18393/ejss.544747
Qureshi,M.,Shahzad,H.Saeed,M.Ullah,S.Ali,M.Mujeeb,F., and ,Anjum,M."Relative potential of rhizobium species to enhance the growth and yield attributes of cotton (Gossypium hirsutum L.)" Eurasian Journal of Soil Science, 8.2 (2019):159 - 166. DOI : 10.18393/ejss.544747
Qureshi,M.,Shahzad,H.Saeed,M.Ullah,S.Ali,M.Mujeeb,F., and ,Anjum,M. "Relative potential of rhizobium species to enhance the growth and yield attributes of cotton (Gossypium hirsutum L.)" Eurasian Journal of Soil Science,8(Apr 2019):159 - 166 DOI : 10.18393/ejss.544747
M,Qureshi.H,Shahzad.M,Saeed.S,Ullah.M,Ali.F,Mujeeb.M,Anjum "Relative potential of rhizobium species to enhance the growth and yield attributes of cotton (Gossypium hirsutum L.)" Eurasian J. Soil Sci, vol.8, no.2, pp.159 - 166 (Apr 2019), DOI : 10.18393/ejss.544747
Qureshi,M. Amjad ;Shahzad,Haroon ;Saeed,M. Sajjad ;Ullah,Sana ;Ali,M. Asif ;Mujeeb,Fakhar ;Anjum,M.A. Relative potential of rhizobium species to enhance the growth and yield attributes of cotton (Gossypium hirsutum L.). Eurasian Journal of Soil Science, (2019),8.2:159 - 166. DOI : 10.18393/ejss.544747

How to cite

Qureshi, M., Shahzad, H., Saeed, M., Ullah, S., Ali, M., Mujeeb, F., Anjum, M., 2019. Relative potential of rhizobium species to enhance the growth and yield attributes of cotton (Gossypium hirsutum L.). Eurasian J. Soil Sci. 8(2): 159 - 166. DOI : 10.18393/ejss.544747

Author information

M. Amjad Qureshi , Agricultural Biotechnology Research Institute, AARI Faisalabad, Pakistan
Haroon Shahzad , Arid Zone Research Centre, PARC, D. I. Khan, Pakistan
M. Sajjad Saeed , Pulses Research Institute, AARI, Faisalabad, Pakistan
Sana Ullah , Institute of Soil & Environmental Sciences, University of Agriculture Faisalabad, Pakistan
M. Asif Ali , Agricultural Biotechnology Research Institute, AARI Faisalabad, Pakistan
Fakhar Mujeeb , Agricultural Biotechnology Research Institute, AARI Faisalabad, Pakistan
M.A. Anjum , Agricultural Biotechnology Research Institute, AARI Faisalabad, Pakistan

Publication information

Article first published online : 28 Mar 2019
Manuscript Accepted : 25 Mar 2019
Manuscript Received: 02 Oct 2018
DOI: 10.18393/ejss.544747
Stable URL: http://ejss.fesss.org/10.18393/ejss.544747

Abstract

Legumes compensate mineral fertilizer by fixing nitrogen due to the specialized structures i.e. nodules by Rhizobium species. Literature revealed that legumes fixed nitrogen due to Rhizobium inoculation from 50-300 kg NPK ha-1 year-1. Rhizobium besides nitrogen fixation, solubilized phosphates, produced growth hormones and due to its root colonizing ability improved the growth and yield of non-legumes also and performed as plant growth promoting rhizobacteria (PGPR). Study was conducted to assess the relative efficiency of Rhizobium species for the growth and yield of cotton. Different isolates of five species of Rhizobium species responsible for different nodule formation in legumes were assessed for the auxin biosynthesis potential as IAA equivalents and isolates having higher values for IAA equivalents were used for experimentation. Results revealed that isolates of Rhizobium species improved the growth and physiological parameters of cotton. Higher values were root/shoot length and mass were observed with Rhizobium species of berseem (Br5). Bacterial inoculation with isolate (Br5) produced 60.94, 64.40 g shoot/root mass that is 16.70 and 23.80 % higher than control and percent increase improvements of cotton shoot/root length with Br5 i.e. 18.3, 24.8 % higher than that of control. Higher values of IAA equivalents were observed in root/shoot content of cotton with isolate of Br5. Bacterial inoculation improved the plant height, boll weight, number of bolls plant-1 and seed cotton yield with Br5 inoculation. The chlorophyll content, photosynthetic rate, transpiration rate and photo active radiation were also higher in the inoculated treatments. Results of present study clearly demonstrated that different isolates of Rhizobium species improved the growth and yield parameters of cotton and thus Rhizobium sp can be effectively utilized as bacterial inoculants in non-legumes.

Keywords

Rhizobium species, PGPR, auxin biosynthesis, growth and yield, cotton.

Corresponding author

References

Adnan, M., Shah, Z., Saleem, N., Basir, A., Rahman, I., Ulah, H., Ibrahim, M., Shah, J.A., Muhammad, Khan, A., Shah, S.R.A.,  2016. Isolation and evaluation of summer legumes Rhizobia as PGPR. Pure and Applied Biology 5(1): 127-133.

Arnon, D.I., 1949. Copper enzymes in isolated chloroplasts.polyphenoloxidase in Beta vulgaris. Plant Physiology 24(1): 1-15.

Arshad, M., Leveaue, J.H., Asad, S., Imran A., Mirza, M.S., 2016. Comparison of rhizospheric bacterial populations and growth promotion of avp1 transgenic and non-transgenic cotton by bacterial inoculations. Journal of Animal and Plant Sciences 26(5): 1284-1290.

Asghar, N., Zahir, Z.A., Akram, M.A., Ahmad, H.T., Hussain, M.B., 2015. Isolation and screening of beneficial bacteria to ameliorate drought stress in wheat. Soil and Environment 34(1): 100-110.

Biswas, C., Ladha, J.K., Dazzo, F.B., 2000. Rhizobia inoculation improves nutrient uptake and growth of lowland rice. Soil Science Society of America Journal 64(5): 1644-1650.

Boivin, S. Fonouni-Farde, C., Frugier, F., 2016. How auxin and cytokinin phytohormones modulate root microbe interactions. Frontiers in Plant Science 7, 1240.

Cassán, F., Maiale, S., Masciarelli, O., Vidal, A., Luna, V., Ruiz, O., 2009. Cadaverine production by Azospirillum brasilense and its possible role in plant growth promotion and osmotic stress mitigation. European Journal of Soil Biology 45(1): 12–19.

Dakora, F.D., 2003. Defining new roles for plant and rhizobial molecules in sole and mixed plant cultures involving symbiotic legumes. New Phytologist 158(1): 39–49.

Dakora, F.D., Matiru, V., King, M., Phillips, D.A., 2002.Plant growth promotion in legumes and cereals by lumichrome, a rhizobial signal metabolite. In: Nitrogen Fixation: Global Perspectives. Finan, T.M., O’Brian, M.R., Layzell, D.B., Vessey, K., Newton, W.E. (Eds.). CABI Publishing, Wallingford, U.K. pp.321–322.

Duncan, B., 1955. Multiple Range and Multiple F Test. Biometrics 11: 1-42.

Egamberdieva, D., 2011. Survival of Pseudomonas extremorientalis TSAU20 and P.chlororaphis TSAU13 in the rhizosphere of common bean (Phaseolus vulgaris) under saline conditions. Plant, Soil and Environment 57(3): 122–127.

Egamberdieva, D., Kucharova, Z., 2009. Selection for root colonizing bacteria stimulating wheat growth in saline soils. Biology and Fertility of Soils 45(6): 563–571.

Egamberdieva, D.F., Kamilova, F., Validov, S., Gafurova, L., Kucharova, Z., Lugtenberg B., 2008. High incidence of plant growth-stimulating bacteria associated with the rhizosphere of wheat grown on salinated soil in Uzbekistan. Environmental Microbiology 10(1): 1-9.

Galal, Y.G., El-Gandaour, J.A., El-Akel, F.A., 2001. Stimulation of wheat growth and N Fixation through Azospirillum and Rhizobium inoculation. A Field trial with 15N techniques. Plant Nutrition. Developments in Plant and Soil Sciences.  Horst, W.J., Schenk, M.K., Bürkert, A., Claassen, N., Flessa, H., Frommer, W. B., Goldbach, H., Olfs, H.W., Römheld, V., Sattelmacher, B., Schmidhalter, U., Schubert, S., Wirén, N., Wittenmayer, L. (Eds.). vol 92. Springer, Dordrecht. pp. 666-667.

Gepts, P., Beavis, W.D., Brummer, E.C., Shoemaker, R.C., Stalker, H.T., Weeden, N.F., Young, N.D., 2005. Legumes as a model plant family: Genomics for food and feed report of cross-legume advances through genomics conference. Plant Physiology 137: 1228-1235.

Glick, B.R., 1995. The enhancement of plant growth by free living bacteria. Canadian Journal of Microbiology 41(2): 109-117.

Gopalakrishnan, S., Sathya, A., Vijayabharathi, R., Varshney, R.K., Gowda, C.L.L., Krishnamurthy, L., 2015. Plant growth promoting rhizobia: challenges and opportunities. Biotechnology 5(4): 355–377.

Gyaneshwar, P., Kumar, G.N., Parekh, L.J., 1998. Effect of buffering on the phosphate solubilizing ability of microorganisms. World Journal of Microbiology and Biotechnology 14(5): 669-673.

Habig, J., Hassen, A., Swart, A., 2015. Application of microbiology in conservation agriculture. In: Conservation Agriculture, Farooq, M., Siddique, K.H.M. (Eds.) Springer International Publishing, Switzerland. pp.525-557.

Hafeez, F.Y., Safdar, M.E., Chaudhry, A.U., Malik, K.A., 2004. Rhizobial inoculation improves seedling emergence, nutrient uptake and growth of cotton. Australian Journal of Experimental Agriculture 44(6): 617-622.

Hossain, Md.S. Mårtensson, A., 2008. Potential use of Rhizobium spp. to improve fitness of non-nitrogen-fixing plants. Acta Agriculturae Scandinavica, Section B -  Soil & Plant Science 58(4): 352-358.

Hussain, M.B., Mehboob, I., Zahir, Z.A., Naveed, M., Asghar, H.N., 2009. Potential of Rhizobium spp. for improving growth and yield of rice (Oryza sativa L.). Soil and Environment 28(1): 49-55.

Hussain, M.B., Zahir, Z.A., Asghar, H.N., Asgher, N., 2014. Can catalase and exopolysaccharides producing rhizobia ameliorate drought stress in wheat?. International Journal of Agriculture and Biology 16(1): 3‒13.

Kloepper, J.W., Beauchamp, C.J., 1992. A review of issues related to measuring colonization of plant roots by bacteria. Canadian Journal of Microbiology 38(12): 1219–1232.

Kumar, H., Jagadeesh, K.S., 2016. Microbial consortia-mediated plant defense against phytopathogens and growth benefits. South Indian Journal of Biological Sciences 2(4): 395-403.

Lippmann, B., Leinhos, V., Bergmann, H., 1995. Influence of auxin producing rhizobacteria on root morphology and nutrient accumulation of crops. I. Changes in root morphology and nutrient accumulation in maize (Zea mays L.) caused by inoculation with indole-3-acetic acid (IAA) producing Pseudomonas and Acinetobacter strains or IAA applied exogenously. Angewandte Botanik 69(1-2): 31-36

Lugtenberg, K.J.J., Dekkers, L., Bloemberg, J.V., 2001. Molecular determinants of rhizosphere colonization by Pseudomonas. Annual Review of Phytopathology 39: 461-490.

Mehboob, I., Naveed, M., Zahir, Z.A., 2009. Rhizobial association with non-legumes: mechanisms and applications. Critical Reviews in Plant Sciences 28(6): 432–456.

Naveed, M., Mitter, B., Reichenauer, T.G., Wieczorek, K., Sessitsch, A., 2014. Increased drought stress resilience of maize through endophytic colonization by Burkholderia phytofirmans PsJN and Enterobacter sp. FD17. Environmental and Experimental Botany 97: 30–39.

Noreen, S., Ali, B., Hasnain, S., 2012. Growth promotion of Vigna mungo (L.) by Pseudomonas spp. exhibiting auxin production and ACC-deaminase activity. Annals of Microbiology 62(1): 411–417.

Pacheco-Villalobos, D., Diaz-Moreno, S.M., Schuren, A.V.D., Tamaki, T., Kang, Y.H., Gujas, B., Novak, O., Jaspert, N., Li, Z., Wolf, S., Oecking, C., Ljung, K., Bulone, V., Hardtke, C.S., 2016. The effects of high steady state auxin levels on root cell elongation in Brachypodium. The Plant Cell 28: 1009–1024.

Parthiban P., Shijila Rani A.S., Mahesh V., Ambikapathy V., 2016. Studies on biosynthesis of auxin in rhizobium and their impact on growth of Vigna mungo L. Pharmaceutical and Biological Evaluations 3(3): 371-376.

Qureshi, A., Shahzad, H., Imran, Z., Mushtaq, M., Akhtar, N., Ali, M.A., Mujeeb, F., 2013. Potential of Rhizobium species to enhance growth and fodder yield of maize in the presence and absence of L-tryptophan. Journal of Animal and Plant Sciences 23(5): 1448-1454.

Sarwar, M., Martens, D.A., Arshad, M., Frankenberger Jr., W.T., 1992. Tryptophan-dependent biosynthesis of auxins in soil. Plant and Soil 147(2): 207-215.

Sessitsch, A., Howieson, J.G., Perret, X., Antoun, H., Martínez-Romero, E., 2002. Advances in Rhizobium research. Critical Reviews in Plant Sciences 21(4): 323-387.

Steel, R.G.D., Torrie, J.H., Dickey, D.A., 1997. Principles and Procedures of Statistics: A Biometrical Approach. 3rd Ed. McGraw-Hill Book International Co., Singapore. 666p.

Ullah, S., Qureshi, M.A., Ali, M.A., Mujeeb, F., Yasin, S., 2017a.Comparative potential of Rhizobium species for the growth promotion of sunflower (Helianthus annuus L.). Eurasian Journal of Soil Science 6(3): 189-196.

Ullah, S., Khan, M.Y., Asghar, H.N., Akhtar, M.J., Zahir, Z.A., 2017b. Differential response of single and co-inoculation of Rhizobium leguminosarum and Mesorhizobiumciceri for inducing water deficit stress tolerance in wheat. Annals of Microbiology 67(11): 739-749.

Verbon, E.H., Liberman, L.M., 2016. Beneficial microbes affect endogenous mechanisms controlling root development. Trends in Plant Science 21(3): 218–229.

Vincent, J.M., 1970. A manual of practical study of root nodule bacteria. IBP Handbook No. 15. Blackwell Scientific Publications Oxford and Edinburgh, UK,

Abstract

Legumes compensate mineral fertilizer by fixing nitrogen due to the specialized structures i.e. nodules by Rhizobium species. Literature revealed that legumes fixed nitrogen due to Rhizobium inoculation from 50-300 kg NPK ha-1 year-1. Rhizobium besides nitrogen fixation, solubilized phosphates, produced growth hormones and due to its root colonizing ability improved the growth and yield of non-legumes also and performed as plant growth promoting rhizobacteria (PGPR). Study was conducted to assess the relative efficiency of Rhizobium species for the growth and yield of cotton. Different isolates of five species of Rhizobium species responsible for different nodule formation in legumes were assessed for the auxin biosynthesis potential as IAA equivalents and isolates having higher values for IAA equivalents were used for experimentation. Results revealed that isolates of Rhizobium species improved the growth and physiological parameters of cotton. Higher values were root/shoot length and mass were observed with Rhizobium species of berseem (Br5). Bacterial inoculation with isolate (Br5) produced 60.94, 64.40 g shoot/root mass that is 16.70 and 23.80 % higher than control and percent increase improvements of cotton shoot/root length with Br5 i.e. 18.3, 24.8 % higher than that of control. Higher values of IAA equivalents were observed in root/shoot content of cotton with isolate of Br5. Bacterial inoculation improved the plant height, boll weight, number of bolls plant-1 and seed cotton yield with Br5 inoculation. The chlorophyll content, photosynthetic rate, transpiration rate and photo active radiation were also higher in the inoculated treatments. Results of present study clearly demonstrated that different isolates of Rhizobium species improved the growth and yield parameters of cotton and thus Rhizobium sp can be effectively utilized as bacterial inoculants in non-legumes.

Keywords: Rhizobium species, PGPR, auxin biosynthesis, growth and yield, cotton.

References

Adnan, M., Shah, Z., Saleem, N., Basir, A., Rahman, I., Ulah, H., Ibrahim, M., Shah, J.A., Muhammad, Khan, A., Shah, S.R.A.,  2016. Isolation and evaluation of summer legumes Rhizobia as PGPR. Pure and Applied Biology 5(1): 127-133.

Arnon, D.I., 1949. Copper enzymes in isolated chloroplasts.polyphenoloxidase in Beta vulgaris. Plant Physiology 24(1): 1-15.

Arshad, M., Leveaue, J.H., Asad, S., Imran A., Mirza, M.S., 2016. Comparison of rhizospheric bacterial populations and growth promotion of avp1 transgenic and non-transgenic cotton by bacterial inoculations. Journal of Animal and Plant Sciences 26(5): 1284-1290.

Asghar, N., Zahir, Z.A., Akram, M.A., Ahmad, H.T., Hussain, M.B., 2015. Isolation and screening of beneficial bacteria to ameliorate drought stress in wheat. Soil and Environment 34(1): 100-110.

Biswas, C., Ladha, J.K., Dazzo, F.B., 2000. Rhizobia inoculation improves nutrient uptake and growth of lowland rice. Soil Science Society of America Journal 64(5): 1644-1650.

Boivin, S. Fonouni-Farde, C., Frugier, F., 2016. How auxin and cytokinin phytohormones modulate root microbe interactions. Frontiers in Plant Science 7, 1240.

Cassán, F., Maiale, S., Masciarelli, O., Vidal, A., Luna, V., Ruiz, O., 2009. Cadaverine production by Azospirillum brasilense and its possible role in plant growth promotion and osmotic stress mitigation. European Journal of Soil Biology 45(1): 12–19.

Dakora, F.D., 2003. Defining new roles for plant and rhizobial molecules in sole and mixed plant cultures involving symbiotic legumes. New Phytologist 158(1): 39–49.

Dakora, F.D., Matiru, V., King, M., Phillips, D.A., 2002.Plant growth promotion in legumes and cereals by lumichrome, a rhizobial signal metabolite. In: Nitrogen Fixation: Global Perspectives. Finan, T.M., O’Brian, M.R., Layzell, D.B., Vessey, K., Newton, W.E. (Eds.). CABI Publishing, Wallingford, U.K. pp.321–322.

Duncan, B., 1955. Multiple Range and Multiple F Test. Biometrics 11: 1-42.

Egamberdieva, D., 2011. Survival of Pseudomonas extremorientalis TSAU20 and P.chlororaphis TSAU13 in the rhizosphere of common bean (Phaseolus vulgaris) under saline conditions. Plant, Soil and Environment 57(3): 122–127.

Egamberdieva, D., Kucharova, Z., 2009. Selection for root colonizing bacteria stimulating wheat growth in saline soils. Biology and Fertility of Soils 45(6): 563–571.

Egamberdieva, D.F., Kamilova, F., Validov, S., Gafurova, L., Kucharova, Z., Lugtenberg B., 2008. High incidence of plant growth-stimulating bacteria associated with the rhizosphere of wheat grown on salinated soil in Uzbekistan. Environmental Microbiology 10(1): 1-9.

Galal, Y.G., El-Gandaour, J.A., El-Akel, F.A., 2001. Stimulation of wheat growth and N Fixation through Azospirillum and Rhizobium inoculation. A Field trial with 15N techniques. Plant Nutrition. Developments in Plant and Soil Sciences.  Horst, W.J., Schenk, M.K., Bürkert, A., Claassen, N., Flessa, H., Frommer, W. B., Goldbach, H., Olfs, H.W., Römheld, V., Sattelmacher, B., Schmidhalter, U., Schubert, S., Wirén, N., Wittenmayer, L. (Eds.). vol 92. Springer, Dordrecht. pp. 666-667.

Gepts, P., Beavis, W.D., Brummer, E.C., Shoemaker, R.C., Stalker, H.T., Weeden, N.F., Young, N.D., 2005. Legumes as a model plant family: Genomics for food and feed report of cross-legume advances through genomics conference. Plant Physiology 137: 1228-1235.

Glick, B.R., 1995. The enhancement of plant growth by free living bacteria. Canadian Journal of Microbiology 41(2): 109-117.

Gopalakrishnan, S., Sathya, A., Vijayabharathi, R., Varshney, R.K., Gowda, C.L.L., Krishnamurthy, L., 2015. Plant growth promoting rhizobia: challenges and opportunities. Biotechnology 5(4): 355–377.

Gyaneshwar, P., Kumar, G.N., Parekh, L.J., 1998. Effect of buffering on the phosphate solubilizing ability of microorganisms. World Journal of Microbiology and Biotechnology 14(5): 669-673.

Habig, J., Hassen, A., Swart, A., 2015. Application of microbiology in conservation agriculture. In: Conservation Agriculture, Farooq, M., Siddique, K.H.M. (Eds.) Springer International Publishing, Switzerland. pp.525-557.

Hafeez, F.Y., Safdar, M.E., Chaudhry, A.U., Malik, K.A., 2004. Rhizobial inoculation improves seedling emergence, nutrient uptake and growth of cotton. Australian Journal of Experimental Agriculture 44(6): 617-622.

Hossain, Md.S. Mårtensson, A., 2008. Potential use of Rhizobium spp. to improve fitness of non-nitrogen-fixing plants. Acta Agriculturae Scandinavica, Section B -  Soil & Plant Science 58(4): 352-358.

Hussain, M.B., Mehboob, I., Zahir, Z.A., Naveed, M., Asghar, H.N., 2009. Potential of Rhizobium spp. for improving growth and yield of rice (Oryza sativa L.). Soil and Environment 28(1): 49-55.

Hussain, M.B., Zahir, Z.A., Asghar, H.N., Asgher, N., 2014. Can catalase and exopolysaccharides producing rhizobia ameliorate drought stress in wheat?. International Journal of Agriculture and Biology 16(1): 3‒13.

Kloepper, J.W., Beauchamp, C.J., 1992. A review of issues related to measuring colonization of plant roots by bacteria. Canadian Journal of Microbiology 38(12): 1219–1232.

Kumar, H., Jagadeesh, K.S., 2016. Microbial consortia-mediated plant defense against phytopathogens and growth benefits. South Indian Journal of Biological Sciences 2(4): 395-403.

Lippmann, B., Leinhos, V., Bergmann, H., 1995. Influence of auxin producing rhizobacteria on root morphology and nutrient accumulation of crops. I. Changes in root morphology and nutrient accumulation in maize (Zea mays L.) caused by inoculation with indole-3-acetic acid (IAA) producing Pseudomonas and Acinetobacter strains or IAA applied exogenously. Angewandte Botanik 69(1-2): 31-36

Lugtenberg, K.J.J., Dekkers, L., Bloemberg, J.V., 2001. Molecular determinants of rhizosphere colonization by Pseudomonas. Annual Review of Phytopathology 39: 461-490.

Mehboob, I., Naveed, M., Zahir, Z.A., 2009. Rhizobial association with non-legumes: mechanisms and applications. Critical Reviews in Plant Sciences 28(6): 432–456.

Naveed, M., Mitter, B., Reichenauer, T.G., Wieczorek, K., Sessitsch, A., 2014. Increased drought stress resilience of maize through endophytic colonization by Burkholderia phytofirmans PsJN and Enterobacter sp. FD17. Environmental and Experimental Botany 97: 30–39.

Noreen, S., Ali, B., Hasnain, S., 2012. Growth promotion of Vigna mungo (L.) by Pseudomonas spp. exhibiting auxin production and ACC-deaminase activity. Annals of Microbiology 62(1): 411–417.

Pacheco-Villalobos, D., Diaz-Moreno, S.M., Schuren, A.V.D., Tamaki, T., Kang, Y.H., Gujas, B., Novak, O., Jaspert, N., Li, Z., Wolf, S., Oecking, C., Ljung, K., Bulone, V., Hardtke, C.S., 2016. The effects of high steady state auxin levels on root cell elongation in Brachypodium. The Plant Cell 28: 1009–1024.

Parthiban P., Shijila Rani A.S., Mahesh V., Ambikapathy V., 2016. Studies on biosynthesis of auxin in rhizobium and their impact on growth of Vigna mungo L. Pharmaceutical and Biological Evaluations 3(3): 371-376.

Qureshi, A., Shahzad, H., Imran, Z., Mushtaq, M., Akhtar, N., Ali, M.A., Mujeeb, F., 2013. Potential of Rhizobium species to enhance growth and fodder yield of maize in the presence and absence of L-tryptophan. Journal of Animal and Plant Sciences 23(5): 1448-1454.

Sarwar, M., Martens, D.A., Arshad, M., Frankenberger Jr., W.T., 1992. Tryptophan-dependent biosynthesis of auxins in soil. Plant and Soil 147(2): 207-215.

Sessitsch, A., Howieson, J.G., Perret, X., Antoun, H., Martínez-Romero, E., 2002. Advances in Rhizobium research. Critical Reviews in Plant Sciences 21(4): 323-387.

Steel, R.G.D., Torrie, J.H., Dickey, D.A., 1997. Principles and Procedures of Statistics: A Biometrical Approach. 3rd Ed. McGraw-Hill Book International Co., Singapore. 666p.

Ullah, S., Qureshi, M.A., Ali, M.A., Mujeeb, F., Yasin, S., 2017a.Comparative potential of Rhizobium species for the growth promotion of sunflower (Helianthus annuus L.). Eurasian Journal of Soil Science 6(3): 189-196.

Ullah, S., Khan, M.Y., Asghar, H.N., Akhtar, M.J., Zahir, Z.A., 2017b. Differential response of single and co-inoculation of Rhizobium leguminosarum and Mesorhizobiumciceri for inducing water deficit stress tolerance in wheat. Annals of Microbiology 67(11): 739-749.

Verbon, E.H., Liberman, L.M., 2016. Beneficial microbes affect endogenous mechanisms controlling root development. Trends in Plant Science 21(3): 218–229.

Vincent, J.M., 1970. A manual of practical study of root nodule bacteria. IBP Handbook No. 15. Blackwell Scientific Publications Oxford and Edinburgh, UK,



Eurasian Journal of Soil Science