Characterization of multi-trait plant growth promoting Pseudomonas aeruginosa from chickpea (Cicer arietinum) rhizosphere
Article Main
Abstract
In the current perusal, 12 isolates of Pseudomonas were segregated by rhizospheric soil of chickpea (Cicer arietinum) of Madhya Pradesh, India. Isolated test organisms were characterized morphologically, biochemically and 16S rRNA gene sequencing. Out of 12, one isolate designated as P4 was identified as Pseudomonas aeruginosa through 16S rRNA gene sequencing, which revealed 100% homology with the strains DSM 50071 and NBRC 12689. The phylogenetic examination was accomplished utilizing MEGA-X to confirm the identity of isolate P4. The nucleotide hierarchy of the 16S rRNA gene from P4 isolate was submitted in the National Center for Biotechnology Information (NCBI) database under gene bank with accession number MT116414. The P4 isolate exhibited multiple plant growth promotion properties like phosphate solubility, indole acetic acid (IAA) production, 1-aminocyclopropane-1-carboxylate (ACC) deaminase, siderophores, ammonia (NH3) and hydrogen cyanide (HCN) activities, and biocontrol activities against phytopathogenic fungi Fusarium oxysporum and Macrophomina phaseolina.
Article Details
Article Details
Keywords
Aminocyclopropane carboxylic acid (ACC), Ammonia (NH3), Cicer arietinum, Hydrogen cyanide (HCN), Indole acetic acid (IAA), 16S rRNA gene
References
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Ahmad, F., Ahmad, I. & Khan, M.S. (2008). Screening of free-living rhizospheric bacteria for their multiple plant growth-promoting activities. Micro. Boil, 168, 173-181. doi: 10.1016/j.micres.2006.04.001.
Alexander, D.B. & Zuberer, D.A. (1991). Use of chrome azurol S reagents to evaluate siderophore production by rhizosphere bacteria. Biol Fertil Soils; 12 (1), 39-45. doi: 10.1007/BF00369386.
Ali, S. & Kim, W.C. (2018). Plant growth promotion under water: decrease of water logging-induced ACC and ethylene levels by ACC deaminase-producing bacteria. Front. Microbiol; 9:1096. https://doi.org/10.3389/fmicb.2018.01 096.
Anitha, G. & Kumudini, B.S. (2014). Isolation and characterization of fluorescent Pseudomonas and their effect on plant growth promotion. Journal of Environmental Biology, 35, 627-634.
Anonymous (2014). Agricultural Statistics of Pakistan. Ministry of food, Government of Pakistan, Agriculture and Livestock, Economic Wing, Islamabad, Pakistan.
Araujo, F.F. & Guerreiro, R.T. (2010). Bioprospecção de isolados de Bacillus promotores de crescimento de milho cultivado em solo autoclavado e natural. Ciênc Agrotec, 34(4), 837-844. doi: 10.1590/S1413-70542010000400 007.
Arumugam, S., Vijayabharathi, R. & Gopalakrishnan, S. (2017). Plant growth-promoting actinobacteria: a new strategy for enhancing sustainable production and protection of grain legumes, Biotech; 7:102. doi: 10.1007/s13205-017-0736-3.
Barnawal, D., Bharti, N., Maji, D., Chanotiya, C.S. & Kalra, A. (2014). ACC deaminase-containing Arthrobacter protophormiae induces NaCl stress tolerance through reduced ACC oxidase activity and ethylene production resulting in improved nodulation and mycorrhization in Pisum sativum, J. Plant Physiol; 171, 884–894. doi: 10.1016/j.jplph.2014.03.007.
Bhattacharyya, P.N. & Jha, D.K. (2012). Plant Growth-Promoting Rhizobacteria (PGPR): Emergence in Agriculture. World J Microbiol Biotechnol; 28, 1327-1350. doi: 10.1007/s11274-011-0979-9.
Cappuccino, J.C. & Sherman, N. (1992). In: Microbiology: A Laboratory Manual, third ed. Benjamin/Cummings Pub. Co., New York, 125–179. doi: 10.12691/ajmr-1-4-6.
Chauhan, H., Bagyaraj, D.J., Selvakumar, G. & Sundaram, S.P. (2015). Novel plant growth-promoting rhizobacteria prospects and potential, Appl Soil Ecol; 95, 38-53. doi: 10.1016/j.apsoil.2015.05.011.
Dobereiner, J. (1995). Isolation and identification of aerobic nitrogen-fixing bacteria from soil and plants. In: Alef, K. and P. Nanniperi (eds.), Methods Appl Soil Microbiol Biochem, Academic Press, London, 134–141.
Duke, J.A. (1981). Handbook of legumes of world economic importance. Plenum Press, New York and London, 52-57. https://doi.org/10.1002/star.19820341011.
Egamberdieva, D., Wirth, SJ., Alqarawi, AA., et al.., (2017). Phytohormones and beneficial microbes: essential components for plants to balance stress and fitness. Front Microbiol; 8:2104. https://doi.org/10.3389/fmicb.20 17.021 04.
FAOSTAT, (2011). http://faostat.fao.org/site/567/default. aspx#ancor (Accessed 18 July 2014).
Glick, B.R. (2005). Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase. FEMS Microbiol Lett; 251, 1-7. https://doi.org/10.1016/j.femsle.2005.07.0 30.
Harley, J.P. & Prescott, L.M. (2002). Laboratory Exercises in Microbiology, 5th Edition, The McGraw-Hill Companies.
Hassan, M.N., Afghan, S. & Hafeez, P.Y. (2010). Suppression of red rot caused by Colletotrichum falcatum on sugarcane plants using plant growth promoting rhizobacteria. Biocontrol; 55, 531-542. doi:10.1007/s10526-010-9268-z.
Heydarian, Z., Yu, M., Gruber, M., Glick, B. R., Zhou, R. & Hegedus, D. D. (2016). Inoculation of soil with plant growth promoting bacteria producing 1-aminocyclopropane-1-carboxylate deaminase or expression of the corresponding acdS gene in transgenic plants increases salinity tolerance in Camelina sativa. Front. Microbiol., 7:1966. doi: 10.3389/fmicb.2016.01966.
Honma, M. & Shimomura, T. (1978). Metabolism of 1-aminocyclopropane-1-carboxylic acid. Agric Biol Chem; 42, 1825-1831.https:doi.org/10.1080/00021369.1978.10863 261.
Khan, A., Geetha, R., Akolkar. A., et al.., (2006). Differential cross utilization of heterologous siderophores by nodule bacteria of Cajanus cajan and its possible role in growth under iron-limited conditions. Appl. Soil Ecol., 34, 19–26. doi: 10.1016/j.apsoil.2005.12.001.
King, E.O., Ward, M.K. & Raney, D.E. (1954). Two simple media for the demonstration of pycocynin and fluorescein. J Lab Clin Med; 44, 301-307.
Kotasthane, AS., Agrawal, T., Zaidi, NW. & Singh, US. (2017). Identification of siderophore producing and cynogenic fluorescent Pseudomonas and a simple confrontation assay to identify potential bio-control agent for collar rot of chickpea. 3 Biotech; 7(2), 137. doi: 10.1007/s13205-017-0761-2.
Kumar, A., Devi, S., Patil, S., Payal, C. & Negi, S. (2012). Isolation, screening and characterization of bacteria from rhizospheric soils for different plant growth promoting (PGP) activities: An in vitro study. Recent Res Sci Technol; 4 (1), 1-5.
Lev-Yadun, S., Gopher, A., & Abbo, S. (2000). The caradle of agriculture. Science; 288, 1062-1063. doi: 10.1126/science.288.5471.1602.
Malunga, L.N., Bar-EI, S.D, Zinal, E., Berkovich, Z., Abbo, S. & Reifen, R. (2014). The potential use of chickpeas in development of infant follow-on formula. Nutrition Journal; 13 (1), 8. doi: 10.1186/1475-2891-13-8.
Mehta, S. & Nautiyal, C.S. (2001). An efficient method for qualitative screening of phosphate-solubilizing bacteria, Current Microbiology, 43, 51-56. doi: 10.1007/s002840010259.
Muchlbauer, F.J., Redden, R.J., Nassib, A.M., Robertson, L.D. & Smithson, J.B. (1988). Population improvement in pulse crops: an assessment of methods and techniques, 943-966. In: R.J. Summerfield (ed.), world crops: cool season food legumes. Kluwer Academic Publishers, Dordrecht, The Netherlands.
Miller, C.S., Handley, K.M., Wrighton, K.C., Frischkorn, K.R., Thomas, B.C. & Banfield, J.F. (2013). Short-read assembly of full-length 16S amplicons reveals bacterial diversity in subsurface sediments. PLOS ONE; 8(2), e56018. doi: 10.1371/journal.pone.0056018.
Naureen, Z., Price, A.H., Wilson, M.J., Hafeez, F.Y. & Roberts, M.R. (2009). Suppression of rice blast disease by siderophore-producing bioantagonistic bacterial isolates isolated from the rhizosphere of rice grown in Pakistan. Crop Prot.; 28, 1052-1060. http://dx.doi.org/10.1016/j.cropro.2009.08.007.
Pal, K.K., Tilak, K.V.B.R., Saxena, A.K., Dey, R. & Singh, C.S. (2001). Suppression of maize root diseases caused by Macrophomina phaseolina, Fusarium moniliforme and Fusarium graminearum by plant growth promoting rhizobacteria. Microbiol. Res., 156, 209-223. https://doi.org/10.1078/0944-5013-00103.
Panhwar, Q.A., Othman, R., Rahman, Z.A., Meon, S. & Ismail, M.R. (2012). Isolation and characterization of phosphate solubilizing bacteria from aerobic rice. Afr. J. Biotechnol., 11, 2711-2719. doi: 10.5897/AJB10.2218.
Panhwar, QA., Naher, UA., Jusop, S., et al.., (2014). Biochemical and molecular characterization of potential phosphate-solubilizing bacteria in acid sulfate soils and their beneficial effects on rice growth. PLoS ONE, 9, 1–14. https://doi.org/10.1371/journal.pone.0116035.
Patten, CL. & Glick, BR. (2002). Role of Pseudomonas putida indole acetic acid in development of the host plant root system. Appl Environ Microbiol; 68, 3795–3801. Doi: 10.1128/AEM.68.3795-3801.2002.
Pérez-Montaño, F., Alías-Villegas, C., Bellogín, RA., et al.., (2014). Plant growth promotion in cereal and leguminous agricultural important plants: from microorganism capacities to crop production. Microbiol. Res., 169, 325–336. https://doi.org/10.1016/j.micres.2013.09.011.
Saleem, A. R., Brunetti, C., Khalid, A., Della Rocca, G., Raio, A., Emiliani, G., et al.., (2018). Drought response of Mucuna pruriens (L.) DC. Inoculated with ACC deaminase and IAA producing rhizobacteria. PLoS One, 13, e0191218. doi: 10.1371/journal.pone.0191218.
Saleem, M., Arshad, M., Hussain, S. & Bhatti, A.S. (2007). Perspective of plant growth promoting rhizobacteria (PGPR) containing ACC deaminase in stress agriculture. J. Ind. Microbiol. Biotechnol., 34, 635-648. doi: 10.1007/s10295-007-0240-6.
Sawar, M. & Kremer, R. (1995). Determination of bacterially derived auxins using a microplate method. Lett. App. Microbiol., 20, 282-5. Doi: 10.1111/j.1472-765x.1995.tb00 446.x.
Shekhar, N.C. (2002). Biologically pure culture of bacteria which suppresses diseases caused by pathogens in chickpea crops and a culture of bacteria compromising a strain of Pseudomonas fluorescens, Official Gazette of the United States Patent and Trademark Office Patents, pp: 1265.
Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013). MEGA 6: Molecular Evolutionary Genetics Analysis Version 6.0. Mol. Biol. Evol., 30, 2725-2729. doi: 10.1093/molbev/mst197.
Thompson, J.D., Higgins, D.G. & Gibson, T.J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting position-specific gap penalties and weight matrix choice. Nucleic Acids Res, 22, 4673-4680. doi: 10.1093/nar/2 2.22.4673.
Verma, J.P., Yadav J., Tiwari, K.N., Lavkush, & Singh, V. (2010). Impact of plant growth-promoting rhizobacteria on crop production. Int J Agric Res, 5, 954-983.
Wang, C., Knill, E., Glick, B.R. & Defago, G. (2000). Effect of transferring 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase genes into Pseudomonas fluorescens strain CHA0 and its gac A derivative CHA96 on their growth-promoting and disease-suppressive capacities. Can. J. Microbiol., 46, 898-907. doi: 10.1139/w00-071.
Wood, J.A. & Grusak, M.A. (2007). Nutritional value of chickpea. Chickpea Breeding and Management, 101-142. http://dx.doi.org/10.1079/9781845932138.005.
Yuliar, Nion, Y.A, Toyota, K. (2015). Recent trends in control methods for bacterial wilt diseases caused by Ralstonia solanacearum. Microbes Environ; 30 (1), 1-11. Doi: 10.1264/jsme2.ME14144.
Zhang, G., Sun, Y., Sheng, H., Li, H. & Liu, X. (2018). Effects of the inoculations using bacteria producing ACC deaminase on ethylene metabolism and growth of wheat grown under different soil water contents. Plant Physiol. Biochem, 125, 178–184. doi: 10.1016/j.plaphy.2018.02.0 05.
Ahmad, F., Ahmad, I. & Khan, M.S. (2008). Screening of free-living rhizospheric bacteria for their multiple plant growth-promoting activities. Micro. Boil, 168, 173-181. doi: 10.1016/j.micres.2006.04.001.
Alexander, D.B. & Zuberer, D.A. (1991). Use of chrome azurol S reagents to evaluate siderophore production by rhizosphere bacteria. Biol Fertil Soils; 12 (1), 39-45. doi: 10.1007/BF00369386.
Ali, S. & Kim, W.C. (2018). Plant growth promotion under water: decrease of water logging-induced ACC and ethylene levels by ACC deaminase-producing bacteria. Front. Microbiol; 9:1096. https://doi.org/10.3389/fmicb.2018.01 096.
Anitha, G. & Kumudini, B.S. (2014). Isolation and characterization of fluorescent Pseudomonas and their effect on plant growth promotion. Journal of Environmental Biology, 35, 627-634.
Anonymous (2014). Agricultural Statistics of Pakistan. Ministry of food, Government of Pakistan, Agriculture and Livestock, Economic Wing, Islamabad, Pakistan.
Araujo, F.F. & Guerreiro, R.T. (2010). Bioprospecção de isolados de Bacillus promotores de crescimento de milho cultivado em solo autoclavado e natural. Ciênc Agrotec, 34(4), 837-844. doi: 10.1590/S1413-70542010000400 007.
Arumugam, S., Vijayabharathi, R. & Gopalakrishnan, S. (2017). Plant growth-promoting actinobacteria: a new strategy for enhancing sustainable production and protection of grain legumes, Biotech; 7:102. doi: 10.1007/s13205-017-0736-3.
Barnawal, D., Bharti, N., Maji, D., Chanotiya, C.S. & Kalra, A. (2014). ACC deaminase-containing Arthrobacter protophormiae induces NaCl stress tolerance through reduced ACC oxidase activity and ethylene production resulting in improved nodulation and mycorrhization in Pisum sativum, J. Plant Physiol; 171, 884–894. doi: 10.1016/j.jplph.2014.03.007.
Bhattacharyya, P.N. & Jha, D.K. (2012). Plant Growth-Promoting Rhizobacteria (PGPR): Emergence in Agriculture. World J Microbiol Biotechnol; 28, 1327-1350. doi: 10.1007/s11274-011-0979-9.
Cappuccino, J.C. & Sherman, N. (1992). In: Microbiology: A Laboratory Manual, third ed. Benjamin/Cummings Pub. Co., New York, 125–179. doi: 10.12691/ajmr-1-4-6.
Chauhan, H., Bagyaraj, D.J., Selvakumar, G. & Sundaram, S.P. (2015). Novel plant growth-promoting rhizobacteria prospects and potential, Appl Soil Ecol; 95, 38-53. doi: 10.1016/j.apsoil.2015.05.011.
Dobereiner, J. (1995). Isolation and identification of aerobic nitrogen-fixing bacteria from soil and plants. In: Alef, K. and P. Nanniperi (eds.), Methods Appl Soil Microbiol Biochem, Academic Press, London, 134–141.
Duke, J.A. (1981). Handbook of legumes of world economic importance. Plenum Press, New York and London, 52-57. https://doi.org/10.1002/star.19820341011.
Egamberdieva, D., Wirth, SJ., Alqarawi, AA., et al.., (2017). Phytohormones and beneficial microbes: essential components for plants to balance stress and fitness. Front Microbiol; 8:2104. https://doi.org/10.3389/fmicb.20 17.021 04.
FAOSTAT, (2011). http://faostat.fao.org/site/567/default. aspx#ancor (Accessed 18 July 2014).
Glick, B.R. (2005). Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase. FEMS Microbiol Lett; 251, 1-7. https://doi.org/10.1016/j.femsle.2005.07.0 30.
Harley, J.P. & Prescott, L.M. (2002). Laboratory Exercises in Microbiology, 5th Edition, The McGraw-Hill Companies.
Hassan, M.N., Afghan, S. & Hafeez, P.Y. (2010). Suppression of red rot caused by Colletotrichum falcatum on sugarcane plants using plant growth promoting rhizobacteria. Biocontrol; 55, 531-542. doi:10.1007/s10526-010-9268-z.
Heydarian, Z., Yu, M., Gruber, M., Glick, B. R., Zhou, R. & Hegedus, D. D. (2016). Inoculation of soil with plant growth promoting bacteria producing 1-aminocyclopropane-1-carboxylate deaminase or expression of the corresponding acdS gene in transgenic plants increases salinity tolerance in Camelina sativa. Front. Microbiol., 7:1966. doi: 10.3389/fmicb.2016.01966.
Honma, M. & Shimomura, T. (1978). Metabolism of 1-aminocyclopropane-1-carboxylic acid. Agric Biol Chem; 42, 1825-1831.https:doi.org/10.1080/00021369.1978.10863 261.
Khan, A., Geetha, R., Akolkar. A., et al.., (2006). Differential cross utilization of heterologous siderophores by nodule bacteria of Cajanus cajan and its possible role in growth under iron-limited conditions. Appl. Soil Ecol., 34, 19–26. doi: 10.1016/j.apsoil.2005.12.001.
King, E.O., Ward, M.K. & Raney, D.E. (1954). Two simple media for the demonstration of pycocynin and fluorescein. J Lab Clin Med; 44, 301-307.
Kotasthane, AS., Agrawal, T., Zaidi, NW. & Singh, US. (2017). Identification of siderophore producing and cynogenic fluorescent Pseudomonas and a simple confrontation assay to identify potential bio-control agent for collar rot of chickpea. 3 Biotech; 7(2), 137. doi: 10.1007/s13205-017-0761-2.
Kumar, A., Devi, S., Patil, S., Payal, C. & Negi, S. (2012). Isolation, screening and characterization of bacteria from rhizospheric soils for different plant growth promoting (PGP) activities: An in vitro study. Recent Res Sci Technol; 4 (1), 1-5.
Lev-Yadun, S., Gopher, A., & Abbo, S. (2000). The caradle of agriculture. Science; 288, 1062-1063. doi: 10.1126/science.288.5471.1602.
Malunga, L.N., Bar-EI, S.D, Zinal, E., Berkovich, Z., Abbo, S. & Reifen, R. (2014). The potential use of chickpeas in development of infant follow-on formula. Nutrition Journal; 13 (1), 8. doi: 10.1186/1475-2891-13-8.
Mehta, S. & Nautiyal, C.S. (2001). An efficient method for qualitative screening of phosphate-solubilizing bacteria, Current Microbiology, 43, 51-56. doi: 10.1007/s002840010259.
Muchlbauer, F.J., Redden, R.J., Nassib, A.M., Robertson, L.D. & Smithson, J.B. (1988). Population improvement in pulse crops: an assessment of methods and techniques, 943-966. In: R.J. Summerfield (ed.), world crops: cool season food legumes. Kluwer Academic Publishers, Dordrecht, The Netherlands.
Miller, C.S., Handley, K.M., Wrighton, K.C., Frischkorn, K.R., Thomas, B.C. & Banfield, J.F. (2013). Short-read assembly of full-length 16S amplicons reveals bacterial diversity in subsurface sediments. PLOS ONE; 8(2), e56018. doi: 10.1371/journal.pone.0056018.
Naureen, Z., Price, A.H., Wilson, M.J., Hafeez, F.Y. & Roberts, M.R. (2009). Suppression of rice blast disease by siderophore-producing bioantagonistic bacterial isolates isolated from the rhizosphere of rice grown in Pakistan. Crop Prot.; 28, 1052-1060. http://dx.doi.org/10.1016/j.cropro.2009.08.007.
Pal, K.K., Tilak, K.V.B.R., Saxena, A.K., Dey, R. & Singh, C.S. (2001). Suppression of maize root diseases caused by Macrophomina phaseolina, Fusarium moniliforme and Fusarium graminearum by plant growth promoting rhizobacteria. Microbiol. Res., 156, 209-223. https://doi.org/10.1078/0944-5013-00103.
Panhwar, Q.A., Othman, R., Rahman, Z.A., Meon, S. & Ismail, M.R. (2012). Isolation and characterization of phosphate solubilizing bacteria from aerobic rice. Afr. J. Biotechnol., 11, 2711-2719. doi: 10.5897/AJB10.2218.
Panhwar, QA., Naher, UA., Jusop, S., et al.., (2014). Biochemical and molecular characterization of potential phosphate-solubilizing bacteria in acid sulfate soils and their beneficial effects on rice growth. PLoS ONE, 9, 1–14. https://doi.org/10.1371/journal.pone.0116035.
Patten, CL. & Glick, BR. (2002). Role of Pseudomonas putida indole acetic acid in development of the host plant root system. Appl Environ Microbiol; 68, 3795–3801. Doi: 10.1128/AEM.68.3795-3801.2002.
Pérez-Montaño, F., Alías-Villegas, C., Bellogín, RA., et al.., (2014). Plant growth promotion in cereal and leguminous agricultural important plants: from microorganism capacities to crop production. Microbiol. Res., 169, 325–336. https://doi.org/10.1016/j.micres.2013.09.011.
Saleem, A. R., Brunetti, C., Khalid, A., Della Rocca, G., Raio, A., Emiliani, G., et al.., (2018). Drought response of Mucuna pruriens (L.) DC. Inoculated with ACC deaminase and IAA producing rhizobacteria. PLoS One, 13, e0191218. doi: 10.1371/journal.pone.0191218.
Saleem, M., Arshad, M., Hussain, S. & Bhatti, A.S. (2007). Perspective of plant growth promoting rhizobacteria (PGPR) containing ACC deaminase in stress agriculture. J. Ind. Microbiol. Biotechnol., 34, 635-648. doi: 10.1007/s10295-007-0240-6.
Sawar, M. & Kremer, R. (1995). Determination of bacterially derived auxins using a microplate method. Lett. App. Microbiol., 20, 282-5. Doi: 10.1111/j.1472-765x.1995.tb00 446.x.
Shekhar, N.C. (2002). Biologically pure culture of bacteria which suppresses diseases caused by pathogens in chickpea crops and a culture of bacteria compromising a strain of Pseudomonas fluorescens, Official Gazette of the United States Patent and Trademark Office Patents, pp: 1265.
Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013). MEGA 6: Molecular Evolutionary Genetics Analysis Version 6.0. Mol. Biol. Evol., 30, 2725-2729. doi: 10.1093/molbev/mst197.
Thompson, J.D., Higgins, D.G. & Gibson, T.J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting position-specific gap penalties and weight matrix choice. Nucleic Acids Res, 22, 4673-4680. doi: 10.1093/nar/2 2.22.4673.
Verma, J.P., Yadav J., Tiwari, K.N., Lavkush, & Singh, V. (2010). Impact of plant growth-promoting rhizobacteria on crop production. Int J Agric Res, 5, 954-983.
Wang, C., Knill, E., Glick, B.R. & Defago, G. (2000). Effect of transferring 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase genes into Pseudomonas fluorescens strain CHA0 and its gac A derivative CHA96 on their growth-promoting and disease-suppressive capacities. Can. J. Microbiol., 46, 898-907. doi: 10.1139/w00-071.
Wood, J.A. & Grusak, M.A. (2007). Nutritional value of chickpea. Chickpea Breeding and Management, 101-142. http://dx.doi.org/10.1079/9781845932138.005.
Yuliar, Nion, Y.A, Toyota, K. (2015). Recent trends in control methods for bacterial wilt diseases caused by Ralstonia solanacearum. Microbes Environ; 30 (1), 1-11. Doi: 10.1264/jsme2.ME14144.
Zhang, G., Sun, Y., Sheng, H., Li, H. & Liu, X. (2018). Effects of the inoculations using bacteria producing ACC deaminase on ethylene metabolism and growth of wheat grown under different soil water contents. Plant Physiol. Biochem, 125, 178–184. doi: 10.1016/j.plaphy.2018.02.0 05.
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Characterization of multi-trait plant growth promoting Pseudomonas aeruginosa from chickpea (Cicer arietinum) rhizosphere. (2021). Journal of Applied and Natural Science, 13(3), 1003-1010. https://doi.org/10.31018/jans.v13i3.2782
