Impact of Piriformospora indica, Pseudomonas species and Mesorhizobium cicer on growth of chickpea (Cicer arietinum L.)
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Abstract
The present study was conducted to examine synergistic interactions among Piriformospora indica (PI) with potential plant growth promoting rhizobacteria (PGPR) and Mesorhizobium cicer (LGR33, MR) in two chickpea (Cicer arietinum L.) varieties viz. desi PBG1 and kabuli BG1053. Different PGPR species were used viz. native isolates of Pseudomonas argentinensis (LPGPR1), Pseudomonas sp. (LPGPR2) along with national check Pseudomonas sp. (LK884). Compatibility of MR, PI and differentPseudomonas spp. was studied by streak assay method and growth of fungal pellicle in-vitro. Consortium of MR+PI+LPGPR1 (0.605 g dry weight fungal pellicle/100ml nutrient broth) was found as the best compatible treatment. In vivo the synergistic effect of consortia was studied for improving dry weight of roots, nutrient acquisition, colonization and stress tolerance ability in chickpea. Significant improvement in dry weight of root was observed with MR+PI+LPGPR1 (1.316 g plant-1) in comparison to MR alone treatment (0.980 g plant-1) at 90 days after sowing (DAS). Percentage colonization of P.indica improved significantly with consortium MR+PI+LPGPR1 (75.5 and 78.3 %) treatment at 90 DAS. All the treatments significantly improved total soluble sugar content (12.2-26.9 %); amino N content (1.36-1.80 fold) and stress tolerance ability (4-6 fold) over the MR alone treatment. Reducing sugar content significantly improved with MR+PI+LPGPR1 (0.62 and 0.79 mg mL–1) over MR alone (0.42 and 0.58 mg mL–1) treatment in desiPBG1 and kabuli BG1053 chickpea, respectively. The tripartite combination MR+LPGPR1+PI can be explored as potent biofertilizer for improvment in chickpea productivity.
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Keywords
Chickpea, Mesorhizobium cicer, Multipartite interactions, Piriformospora indica, Pseudomonas species
References
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Badri, D. V. and Vivanco, J. M. (2009). Regulation and function of root exudates. Plant Cell. Envir., 32: 666-68.
Bagde, U. S., Prasad, R. and Varma, A. (2010). Interaction of Mycobiont: Piriformospora indica with medicinal plants and plants of economic importance. Afr. J. Biotechnol., 9(54): 9214-26.
Baltruschat, H., Fodor, J., Harrach, B.D., Niemczyk, E., Barna, B. and Gullner, G. (2008). Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New Phytol., 180: 501-10.
Bashan, Y. and de-Bashan, L.E. (2010). How the plant growth-promoting bacterium Azospirillum promotes plant growth-a critical assessment. Adv. Agron., 108: 77-136.
Bennett, R.N., Wenke, T., Freudenberg, B., Mellon, F.A. and Ludwig-Müller, J. (2005). The tu8 mutation of Arabidopsis thaliana encoding a heterochromatin protein 1 homolog causes defects in the induction of secondary metabolite biosynthesis. Plant Biol., 4: 348–357.
Bharadwaj, D.P., Lundquist, P.O. and Alstrom, S. (2008). Arbuscular mycorrhizal fungal spore-associated bacteria affect mycorrhizal colonization, plant growth and potato pathogens. Soil. Biol. Biochem., 40(1): 2494-01.
Danesh, Y.R., (2015). The Piriformospora indica, magic fungus and its role on sustainable agriculture. J. Agric. Technol., 11(2): 517-523.
DuBois, M., Gilles, K. A., Hamilton, J.K., Rebers, P.A. and Smith, F. (1956). Colorimetric method for determination of sugars and related substances. Anal. Chem. 28(3): 350-56.
Esfahani, M.N., Mostajeran, A. and Emtiazi, G. (2010). The effect of draught stress on nitrogenase and antioxidant enzyme activities in nodules formed from symbiosis of chickpea with two strains of Mesorhizobium ciceri. World J. Sci., 10(6): 621-26.
Garcia de Salamone, I.E., Hynes, R.K. and Nelson, L.M. (2001). Cytokinin production by plant growth promoting rhizobacteria and selected mutants. Can. J. Microbiol., 47: 404-11.
Ghosh, P.K., Saha, P., Mayilraj, S. and Maiti, T.K. (2013). Role of IAA metabolizing enzymes on production of IAA in root, nodule of Cajanus cajan and its PGP Rhizobium sp. Biocatalysis Agric. Biotechnol., 2:234–239.
Goyal, V., Chetal, S. and Nainawatee, H. S. (1986). Alterations in Rhizobium trifolii catalase under water stress. Folia. Microbiol., 31: 164-66.
Haichar, F.Z., Santaella, C., Heulin, T. and Achouak, W. (2014). Root exudates mediated interactions belowground. Soil. Biol. Biochem., 77: 69–80.
Inceoglu, O., Salles, J.F., Overbeek, L.V., and Elsas, J.D. (2010). Effects of plant genotype and growth stage on the betaproteobacterial communities associated with different potato cultivars in two fields. Appl. Environ. Microbiol., 76: 3675–3684.
Jida, M. and Assefa, F. (2012). Phenotypic diversity and plant growth promoting characteristic of Mesorhizo-bium species isolated from chickpea (Cicer arietinum L.) growing areas Ethiopia. Afr. J. Biotechnol., 11(29): 7483-93.
Johnson, J.M., Alex, T. and Oelmuller, R. (2014). Piriformospora indica: The versatile and multifunctional root endophytic fungus for enhanced yield and tolerance to biotic and abiotic stress in crop plants. J. Trop. Agric., 52 (2): 103-122,
Kaur, N. and Sharma, P. (2013). Screening and characterization of native Pseudomonas sp. as plant growth promoting rhizobacteria in chickpea (Cicer arietinum L.) rhizosphere. Afr. J. Microbiol. Res., 7: 1465-1474.
Kumar, M., Yadav, V., Tuteja, N. and Johri, A. (2009). Antioxidant enzyme activities in maize plants colonized with Piriformospora indica. Microbiol., 155: 780-90.
Lakshman, H.C. and Kadam, M.A. (2011). Influence of AMF and Rhizobium on the growth and nutrient uptake of Lens esculenta. Biosci. Disc., 2(2): 256-60.
Leveau, J.H.J. and Preston, G.M. (2008). Tansley review: bacterial mycophagy: definition and diagnosis of a unique bacterial-fungal interaction. New Phytol., 177: 859-76.
Mamatha, G., Bagyaraj, D.J. and Jaganath, S. (2002). Inoculation of field-established mulberry and papaya with arbuscular mycorrhizal fungi and a mycorrhiza helper bacterium. Mycorrhiza, 12: 313-16.
Marklund, S. and Marklund, G. (1974). Involvement of the Superoxide anion radical in auto-oxidation of pyragallol and a convenient assay for superoxide dismutase. Eur. J. Biochem., 47: 469-74.
Meena, K., Mesapogu, S. Kumar, M., Yandigeri, M.S., Singh, G. and Saxena, A.K. (2010). Co-inoculation of the endophytic fungus Piriformospora indica with the phosphate-solubilising bacterium Pseudomonas striata affects population dynamics and plant growth in chickpea. Biol. Fertil. Soils, 46: 169-74.
Mhadhbi, H., Jebara, M., Limam, F. and Aauani (2004). Rhizobial strain involvement in plant growth, nodule protein composition and antioxidant enzyme activities of chickpea-rhizobia symbiosis: modulation by salt stress. Plant Physiol. Biochem., 42: 717-22.
Mishra, P.K., Bisht, S.C., Jeevanandan, K, Kumar S., Bisht, J.K. and Jagdish Chandra Bhatt, J.C. (2014). Synergistic effect of inoculating plant growthpromoting Pseudomonas spp. and Rhizobium leguminosarum- FB1 on growth and nutrient uptake of rajmash (Phaseolus vulgaris L. Archives of Agronomy and Soil Science. 60: 799-815 DOI:10.1080/ 03650340.2013.843773.
Murphy, B.R., Hodkinson, T.H. and Doohan F.M. (2013). Mechanism of beneficial colonization of barley fungal root endophytes. Aspects Appl. Biol., 120: 35-44.
Moore, S. and Stein, W.H. (1948). Methods in Enzymology. Academic press, New York, pp 68.
Oberwinkler, F., Riess, K., Bauer, R., Selosse, M.A., Weiss, M., Garnica, S. and Zucaro, A. (2013). Enigmatic Sebacinales. Mycological Progress, 12:1-27.
Oelmuller, R., Sherameti, I., Tripathi, S. and Varma, A. (2009). Piriformospora indica, cultivable root endophyte with multiple biotechnological applications. Symbiosis, 49: 1-17.
Parmar, N. and Dadarwal, K.R. (1999). Stimulation of nitrogen fixation and induction of flavonoid like compounds by rhizobacteria. J. Appl. Microbiol., 86: 36-44.
Phillips, J.M. and Hayman, D.S. (1970). Improved procedures for clearing roots and staining parasitic and VAMF for rapid assessment of infection. Trans. Br. Mycol. Soc., 55: 158-61.
Prusty, R., Grisafi, P. and Fink, G.R. (2004). The plant hormone indole acetic acid induces invasive growth in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 101: 4153-57.
Qiang, X., Weiss, M., Kogel, K.H. and Schafer, P. (2014). Piriformospora indica–a mutualistic basidiomycete with an exceptionally large plant host range. Mol. Plant Pathol., DOI: 10.1111/J.1364-3703.2011.00764.
Rai, M., Acharya, D., Singh, A. and Varma, A. (2001). Positive growth response of the medicinal plants Spilanthes calva and Withania somnifera to inoculation by Piriformospora indica in a field trial. Mycorrhiza, 11: 123-28.
Raja, P., Uma, S., Gopal, H. and Govindarajan (2006). Impact of bioinoculants consortium on rice root exudates, biological nitrogen fixation and plant growth. J. Biol. Sci., 6(5): 815-23.
Sartipnia, N., Nejad, R.A.K., Babaeizad, V., Nejad, T., Sattari, T., Najafi, F. (2013). Effect of Piriformospora indica on antioxidant enzymes activity of tomato (Lycopersicon esculentum) under lead stress. Int. J. Biosci., 3:55-64.
Sharma, M., Schmid, M., Rothballer, M., Hause, G., Zuccaro, A., Imani, J., Kampfer, P., Domann, E., Schafer, P., Hartmann, A. and Kogel, K.H. (2008). Detection and identification of bacteria intimately associated with fungi of the order Sebacinales. Cell Microbiol., 10(11): 2235-46.
Singh, L.P., Gill, S.S. and Tuteja, N. (2011). Unravelling the role of fungal symbionts in plant abiotic stress tolerance. Plant Signal Behaviour, 6(2): 175-91.
Singh, N.P. (2014). Presented to the All India Coordinated Research Project in Chickpea, Indian Institute of Pulses Research, Kanpur, Project Coordinater’s report Volume 25: 3.
Sirrenberg, A., Gobel, C., Grond, S., Czempinski, N., Ratzinger, A., Karlovsky, P., Santos, P., Feussner, I. and Pawlowski, K. (2007). Piriformospora indica affects plant growth by auxin production. Physiologia Plantarum., 131(4): 581-89.
Slaughter, S.J. and Delwiche, L.D. (2010). The Little SAS Book for Enterprise Guide 4.2. (Cary, NC, USA: SAS Institute, Inc.) (www.sas.com).
Somogyi, M. (1952). Determination of reducing sugars by Nelson-Somogyi method. J. Biol. Chem., 200: 245.
Sun, C., Johnson, J. M., Cai, D., Sheramati, I., Oelmuller, R. and Lou, B. (2010). Piriformospora indica confers draught tolerance in Chinese cabbage leaves by stimulating antioxidant enzymes, the expression of drought related genes and the plastid localized CAS protein. J. Plant Physiol., 167: 1009-17.
Varma, A., Verma, S., Sahay N.S., Britta, B. and Franken, P. (1999). Piriformospora indica-a cultivable plant growth promoting root endophyte with similarities to arbuscular mycorrhizal fungi. Appl. Envir. Microbiol., 65: 2741-44,USA.
Varma, S., Varma, A., Rexer, K.H., Hassel, A., Kost, G., Sarabhoy, A., Bisen, P., Butenhorn, B. and Franken, P. (1998). Piriformospora indica, a new root colonizing fungus. Mycologia., 90: 896-903.
Verma, J.P., Yadav, J., Tiwari, K.N. and Kumar, A. (2013). Effect of indigenous Mesorhizobium spp. and plant growth promoting rhizobacteria on yields and nutrients uptake of chickpea (Cicer arietinum L.) under sustainable agriculture. Ecol. Eng., 51: 282– 286.
Badri, D. V. and Vivanco, J. M. (2009). Regulation and function of root exudates. Plant Cell. Envir., 32: 666-68.
Bagde, U. S., Prasad, R. and Varma, A. (2010). Interaction of Mycobiont: Piriformospora indica with medicinal plants and plants of economic importance. Afr. J. Biotechnol., 9(54): 9214-26.
Baltruschat, H., Fodor, J., Harrach, B.D., Niemczyk, E., Barna, B. and Gullner, G. (2008). Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New Phytol., 180: 501-10.
Bashan, Y. and de-Bashan, L.E. (2010). How the plant growth-promoting bacterium Azospirillum promotes plant growth-a critical assessment. Adv. Agron., 108: 77-136.
Bennett, R.N., Wenke, T., Freudenberg, B., Mellon, F.A. and Ludwig-Müller, J. (2005). The tu8 mutation of Arabidopsis thaliana encoding a heterochromatin protein 1 homolog causes defects in the induction of secondary metabolite biosynthesis. Plant Biol., 4: 348–357.
Bharadwaj, D.P., Lundquist, P.O. and Alstrom, S. (2008). Arbuscular mycorrhizal fungal spore-associated bacteria affect mycorrhizal colonization, plant growth and potato pathogens. Soil. Biol. Biochem., 40(1): 2494-01.
Danesh, Y.R., (2015). The Piriformospora indica, magic fungus and its role on sustainable agriculture. J. Agric. Technol., 11(2): 517-523.
DuBois, M., Gilles, K. A., Hamilton, J.K., Rebers, P.A. and Smith, F. (1956). Colorimetric method for determination of sugars and related substances. Anal. Chem. 28(3): 350-56.
Esfahani, M.N., Mostajeran, A. and Emtiazi, G. (2010). The effect of draught stress on nitrogenase and antioxidant enzyme activities in nodules formed from symbiosis of chickpea with two strains of Mesorhizobium ciceri. World J. Sci., 10(6): 621-26.
Garcia de Salamone, I.E., Hynes, R.K. and Nelson, L.M. (2001). Cytokinin production by plant growth promoting rhizobacteria and selected mutants. Can. J. Microbiol., 47: 404-11.
Ghosh, P.K., Saha, P., Mayilraj, S. and Maiti, T.K. (2013). Role of IAA metabolizing enzymes on production of IAA in root, nodule of Cajanus cajan and its PGP Rhizobium sp. Biocatalysis Agric. Biotechnol., 2:234–239.
Goyal, V., Chetal, S. and Nainawatee, H. S. (1986). Alterations in Rhizobium trifolii catalase under water stress. Folia. Microbiol., 31: 164-66.
Haichar, F.Z., Santaella, C., Heulin, T. and Achouak, W. (2014). Root exudates mediated interactions belowground. Soil. Biol. Biochem., 77: 69–80.
Inceoglu, O., Salles, J.F., Overbeek, L.V., and Elsas, J.D. (2010). Effects of plant genotype and growth stage on the betaproteobacterial communities associated with different potato cultivars in two fields. Appl. Environ. Microbiol., 76: 3675–3684.
Jida, M. and Assefa, F. (2012). Phenotypic diversity and plant growth promoting characteristic of Mesorhizo-bium species isolated from chickpea (Cicer arietinum L.) growing areas Ethiopia. Afr. J. Biotechnol., 11(29): 7483-93.
Johnson, J.M., Alex, T. and Oelmuller, R. (2014). Piriformospora indica: The versatile and multifunctional root endophytic fungus for enhanced yield and tolerance to biotic and abiotic stress in crop plants. J. Trop. Agric., 52 (2): 103-122,
Kaur, N. and Sharma, P. (2013). Screening and characterization of native Pseudomonas sp. as plant growth promoting rhizobacteria in chickpea (Cicer arietinum L.) rhizosphere. Afr. J. Microbiol. Res., 7: 1465-1474.
Kumar, M., Yadav, V., Tuteja, N. and Johri, A. (2009). Antioxidant enzyme activities in maize plants colonized with Piriformospora indica. Microbiol., 155: 780-90.
Lakshman, H.C. and Kadam, M.A. (2011). Influence of AMF and Rhizobium on the growth and nutrient uptake of Lens esculenta. Biosci. Disc., 2(2): 256-60.
Leveau, J.H.J. and Preston, G.M. (2008). Tansley review: bacterial mycophagy: definition and diagnosis of a unique bacterial-fungal interaction. New Phytol., 177: 859-76.
Mamatha, G., Bagyaraj, D.J. and Jaganath, S. (2002). Inoculation of field-established mulberry and papaya with arbuscular mycorrhizal fungi and a mycorrhiza helper bacterium. Mycorrhiza, 12: 313-16.
Marklund, S. and Marklund, G. (1974). Involvement of the Superoxide anion radical in auto-oxidation of pyragallol and a convenient assay for superoxide dismutase. Eur. J. Biochem., 47: 469-74.
Meena, K., Mesapogu, S. Kumar, M., Yandigeri, M.S., Singh, G. and Saxena, A.K. (2010). Co-inoculation of the endophytic fungus Piriformospora indica with the phosphate-solubilising bacterium Pseudomonas striata affects population dynamics and plant growth in chickpea. Biol. Fertil. Soils, 46: 169-74.
Mhadhbi, H., Jebara, M., Limam, F. and Aauani (2004). Rhizobial strain involvement in plant growth, nodule protein composition and antioxidant enzyme activities of chickpea-rhizobia symbiosis: modulation by salt stress. Plant Physiol. Biochem., 42: 717-22.
Mishra, P.K., Bisht, S.C., Jeevanandan, K, Kumar S., Bisht, J.K. and Jagdish Chandra Bhatt, J.C. (2014). Synergistic effect of inoculating plant growthpromoting Pseudomonas spp. and Rhizobium leguminosarum- FB1 on growth and nutrient uptake of rajmash (Phaseolus vulgaris L. Archives of Agronomy and Soil Science. 60: 799-815 DOI:10.1080/ 03650340.2013.843773.
Murphy, B.R., Hodkinson, T.H. and Doohan F.M. (2013). Mechanism of beneficial colonization of barley fungal root endophytes. Aspects Appl. Biol., 120: 35-44.
Moore, S. and Stein, W.H. (1948). Methods in Enzymology. Academic press, New York, pp 68.
Oberwinkler, F., Riess, K., Bauer, R., Selosse, M.A., Weiss, M., Garnica, S. and Zucaro, A. (2013). Enigmatic Sebacinales. Mycological Progress, 12:1-27.
Oelmuller, R., Sherameti, I., Tripathi, S. and Varma, A. (2009). Piriformospora indica, cultivable root endophyte with multiple biotechnological applications. Symbiosis, 49: 1-17.
Parmar, N. and Dadarwal, K.R. (1999). Stimulation of nitrogen fixation and induction of flavonoid like compounds by rhizobacteria. J. Appl. Microbiol., 86: 36-44.
Phillips, J.M. and Hayman, D.S. (1970). Improved procedures for clearing roots and staining parasitic and VAMF for rapid assessment of infection. Trans. Br. Mycol. Soc., 55: 158-61.
Prusty, R., Grisafi, P. and Fink, G.R. (2004). The plant hormone indole acetic acid induces invasive growth in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 101: 4153-57.
Qiang, X., Weiss, M., Kogel, K.H. and Schafer, P. (2014). Piriformospora indica–a mutualistic basidiomycete with an exceptionally large plant host range. Mol. Plant Pathol., DOI: 10.1111/J.1364-3703.2011.00764.
Rai, M., Acharya, D., Singh, A. and Varma, A. (2001). Positive growth response of the medicinal plants Spilanthes calva and Withania somnifera to inoculation by Piriformospora indica in a field trial. Mycorrhiza, 11: 123-28.
Raja, P., Uma, S., Gopal, H. and Govindarajan (2006). Impact of bioinoculants consortium on rice root exudates, biological nitrogen fixation and plant growth. J. Biol. Sci., 6(5): 815-23.
Sartipnia, N., Nejad, R.A.K., Babaeizad, V., Nejad, T., Sattari, T., Najafi, F. (2013). Effect of Piriformospora indica on antioxidant enzymes activity of tomato (Lycopersicon esculentum) under lead stress. Int. J. Biosci., 3:55-64.
Sharma, M., Schmid, M., Rothballer, M., Hause, G., Zuccaro, A., Imani, J., Kampfer, P., Domann, E., Schafer, P., Hartmann, A. and Kogel, K.H. (2008). Detection and identification of bacteria intimately associated with fungi of the order Sebacinales. Cell Microbiol., 10(11): 2235-46.
Singh, L.P., Gill, S.S. and Tuteja, N. (2011). Unravelling the role of fungal symbionts in plant abiotic stress tolerance. Plant Signal Behaviour, 6(2): 175-91.
Singh, N.P. (2014). Presented to the All India Coordinated Research Project in Chickpea, Indian Institute of Pulses Research, Kanpur, Project Coordinater’s report Volume 25: 3.
Sirrenberg, A., Gobel, C., Grond, S., Czempinski, N., Ratzinger, A., Karlovsky, P., Santos, P., Feussner, I. and Pawlowski, K. (2007). Piriformospora indica affects plant growth by auxin production. Physiologia Plantarum., 131(4): 581-89.
Slaughter, S.J. and Delwiche, L.D. (2010). The Little SAS Book for Enterprise Guide 4.2. (Cary, NC, USA: SAS Institute, Inc.) (www.sas.com).
Somogyi, M. (1952). Determination of reducing sugars by Nelson-Somogyi method. J. Biol. Chem., 200: 245.
Sun, C., Johnson, J. M., Cai, D., Sheramati, I., Oelmuller, R. and Lou, B. (2010). Piriformospora indica confers draught tolerance in Chinese cabbage leaves by stimulating antioxidant enzymes, the expression of drought related genes and the plastid localized CAS protein. J. Plant Physiol., 167: 1009-17.
Varma, A., Verma, S., Sahay N.S., Britta, B. and Franken, P. (1999). Piriformospora indica-a cultivable plant growth promoting root endophyte with similarities to arbuscular mycorrhizal fungi. Appl. Envir. Microbiol., 65: 2741-44,USA.
Varma, S., Varma, A., Rexer, K.H., Hassel, A., Kost, G., Sarabhoy, A., Bisen, P., Butenhorn, B. and Franken, P. (1998). Piriformospora indica, a new root colonizing fungus. Mycologia., 90: 896-903.
Verma, J.P., Yadav, J., Tiwari, K.N. and Kumar, A. (2013). Effect of indigenous Mesorhizobium spp. and plant growth promoting rhizobacteria on yields and nutrients uptake of chickpea (Cicer arietinum L.) under sustainable agriculture. Ecol. Eng., 51: 282– 286.
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Impact of Piriformospora indica, Pseudomonas species and Mesorhizobium cicer on growth of chickpea (Cicer arietinum L.). (2015). Journal of Applied and Natural Science, 7(1), 373-380. https://doi.org/10.31018/jans.v7i1.619
