Screening of plant growth-promoting Rhizobium tarimense from root nodules of chickpea (Cicer arietinum)
Article Main
Abstract
Plant growth-promoting rhizobacteria (PGPR) are favourable bacteria that colonize the plant roots and enhance plant growth by direct and/or indirect mechanisms. This study aimed to screen rhizobial isolates of chickpea and evaluate their multiple plant growth-promoting traits. A total of twelve rhizobia-like-bacterial isolates were collected from the root nodules of chickpea (Cicer arietinum L.) from different regions of Madhya Pradesh, India, characterized by morphological, biochemical, and identified by the 16S rRNA gene sequencing. Out of twelve, one rhizobial isolate designated as RH17 was confirmed as Rhizobium tarimense by 16S rRNA gene sequencing, which showed 98% similarity with the strain PL-41. The phylogenetic study was done by using MEGA-X to confirm the identity of RH17 isolate and the nucleotide sequence of the 16S rRNA gene of RH17 isolate was submitted to the National Center for Biotechnology Information (NCBI) database under Genbank with accession number OM996100. The RH17 isolate showed multiple plant growth-promoting traits like nitrogen fixation, solubilization of phosphate (15mm), indole acetic acid (IAA) production (1µg/ml), 1-aminocyclopropane-1-carboxylate (ACC) deaminase (0.5nmol), ammonia (NH3), siderophore, hydrogen cyanide (HCN) production and antagonism against phytopathogenic fungi Fusarium oxysporum and Macrophomina phaseolina. Therefore, the present study suggests that R. tarimense (RH17) isolate can be used as PGP bacteria and a biocontrol agent to enhance the growth, productivity and yield of chickpea.
Article Details
Article Details
Keywords
Chickpea, Molecular Evolutionary Genetics Analysis, Plant Growth-Promoting traits, Root nodules, 16S rRNA gene
References
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Bakker, A.W. & Schipperes, B. (1987). Microbial cyanide production in the rhizosphere in relation to potato yield reduction and Pseudomonas sp. mediated plant growth stimulation. Soil Biol. Biochem., 19, 451-457. https://doi.org/10.1016/0038-0717(87)90037-X
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Datta, B. & Chakrabartty, P.K. (2014). Siderophore biosynthesis genes of Rhizobium sp. isolated from Cicer arietinum L. 3 Biotech., 4(4), 391-401. doi: 10.1007/s13205-013-0164-y
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Dutta, S. & Podile, A.R. (2010). Plant growth promoting rhizobacteria (PGPR): the bugs to debug the root zone. Crit. Rev. Microbiol., 36, 232-244. doi: 10.3109/10408411 003766806.
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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
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Igiehon, N.O., Babalola, O.O. & Aremu, B.R. (2019). Genomic insights into plant growth promoting rhizobia capable of enhancing soybean germination under drought stress. BMC Microbiol., 19, 1-22. https://doi.org/10.1186/s12866-019-1536-1.
Imen, H., Neila, A., Adnane, B., Manel, B., Mabrouk, Y., Saidi, M. & Bouaziz, S. (2015). Inoculation with phosphate solubilizing Mesorhizobium strains improves the performance of chickpea (Cicer arietinum L.) under phosphorus deficiency. J. Plant Nutr., 38, 1656-1671. https://doi.org/10.1080/01904167.2015.1061543.
Jukanti, A.K., Gaur, P.M., Gowda, C.L.L. & Chibbar, R.N. (2012). Nutritional quality and health benefits of chickpea (Cicer arietinum L.): a review. Br. J. Nutr., 108, S11-S26. doi: 10.1017/S0007114512000797.
Kavamura, V.N., Santos, S.N., da Silva, J.L., Parma, M.M., Avila, L.A., Visconti, A. & de Melo, I.S. (2013). Screening of Brazilian cacti rhizobacteria for plant growth promotion under drought. Microbiol. Res., 168, 183-191. doi: 10.1016/J.MICRES.2012.12.002.
Khalid, R., Zhang, X.X., Hayat, R. & Ahmed, M. (2020). Molecular characteristics of rhizobia isolated from Arachis hypogaea grown under stress environment. Sustainability., 12(15), 6259. https://doi.org/10.3390/su12156259.
Kumari, P., Meena, M. & Upadhyay, R.S. (2018). Characterization of plant growth promoting rhizobacteria (PGPR) isolated from the rhizosphere of Vigna radiata (mung bean). Biocatal. Agric Biotechnol., 16, 155-162. doi: 10.1016/J.BCAB.2018.07.029.
Martinez-Hidalgo, P. & Hirsch, A.M. (2017). The nodule microbiome: N2-fixing rhizobia do not live alone. Phytobiomes J., 1, 70-82. https://doi.org/10.1094/PBIOMES-12-16-0019-RVW
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.
Menendez, E., Perez-Yepez, J., Hernandez, M., Rodriguez-Perez, A., Velazquez, E. & Leon-Barrios, M. (2020). Plant growth promotion abilities of phylogenetically diverse Mesorhizobium strains: Effect in the root colonization and development of tomato seedlings. Microorganisms., 8, 412. doi: 10.3390/microorganisms8030412.
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. https://doi.org/10.1016/j.cropro.2009.08.007.
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Rasool, A., Mir, M.I., Zulfajri, M., Hanafiah, M.M., Unnisa, S.A. & Mahboob, M. (2021). Plant growth promoting and antifungal asset of indigenous rhizobacteria secluded from saffron (Crocus sativus L.) rhizosphere. Microb. Pathog., 150, 1047. doi: 10.1016/j.micpath.2021.104734.
Sagolshemcha, R., Devi, Y.N., & Singh, R. (2017). Plant growth promoting effect and biocontrol potential of Rhizobium spp. against Macrophomina phaseolina. Int. J. Curr. Microbiol. App. Sci., 6(6), 2695-2701. https://doi.org/10.20546/ijcmas.2017.606.320.
Saidi, S., Chebil, S., Gtari, M. & Mhamdi, R. (2013). Characterization of root-nodule bacteria isolated from Vicia faba and selection of plant growth-promoting traits. World J. Microbiol. Biotechnol., 29(6), 1099-1106. doi: 10.1007/s11274-013-178-4.
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.tb0 0446.x
Shahid, M., Khan, M.S., Syed, A., Marraiki, N. & Elgorban, A.M. (2021). Mesorhizobium ciceri as biological tool for improving physiological, biochemical and antioxidant state of Cicer arietinum (L.) under fungicide stress. Sci. Rep., 11, 1-18. doi: 10.1038/s41598-021-89103-9.
Singha, B., Mazumdar, P.B. & Pandey P. (2018). Characterization of plant growth promoting Rhizobia from root nodule of two legume species cultivated in Assam, India. Proc. Natl. Acad. Sci. India B Biol. Sci., 88, 1007-1016. doi: 10.1007/s40011-016-0836-6.
Solanki, M.K., Wang, Z., Wang, F.Y., Li, C.N., Lan, T.J., Singh, R.K. & Li, Y.R. (2017). Intercropping in sugarcane cultivation influenced the soil properties and enhanced the diversity of vital diazotrophic bacteria. Sugar Tech., 19, 136-147. doi: 10.1007/s12355-016-0445-y
Subramanian, P., Kim, K., Krishnamoorthy, R., Sundaram, S. & Sa, T. (2015). Endophytic bacteria improve nodule function and plant nitrogen in soybean on co-inoculation with Bradyrhizobium japonicum MN110. Plant Growth Regul, 76, 327-332. doi: 10.1007/s10725-014-9993-x
Tagele, S.B., Kim, S.W., Lee, H.G. & Lee, Y.S. (2019). Potential of novel sequence type of Burkholderia cenocepacia for biological control of root rot of maize (Zea mays L.) caused by Fusarium temperatum. Int. J. Mol. Sci, 20(5), 1005. doi: 10.3390/ijms20051005.
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.
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Angus, A.A., Lee, A., Lum, M.R., Shehayeb, M., Hessabi, R., Fujishige, N.A., Yerrapragada, S., Kano, S., Song, N., Yang, P., Estrada de los Santos, P., de Faria, S.M., Dakora, F.D., Weinstock, G. & Hirrsch, A. (2013). Nodulation and effective nitrogen fixation of Macroptilium atropurpureum (siratro) by Burkholderia tuberum, a nodulating and plant growth promoting beta-proteobacterium are influenced by environmental factors. Plant Soil., 369, 543-562. doi: 10.1007/s11104-013-1590-7.
Arafoui, A., Sifi, B., Boudabous, A., Hadrami, I.E., & Cherif, M. (2006). Identification of Rhizobium isolate possessing antagonistic activity against Fusarium oxysporum f. sp. ciceries, the causal agent of Fusarium wilt of chickpea. Journal of Plant Pathology, 88, 67-65. https://dx.doi.org/10.4454/jpp.v88i1.832.
Backer, R., Rokem, J.S., Ilangumaran, G., Lamont, J., Praslickova, D., Ricci, E. & Smith, D.L. (2018). Plant growth-promoting rhizobacteria: context, mechanisms of action, and roadmap to commercialization of biostimulants for sustainable agriculture. Front. Plant Sci., 9, 1473. https://doi.org/10.3389/fpls.2018.01473.
Bakker, A.W. & Schipperes, B. (1987). Microbial cyanide production in the rhizosphere in relation to potato yield reduction and Pseudomonas sp. mediated plant growth stimulation. Soil Biol. Biochem., 19, 451-457. https://doi.org/10.1016/0038-0717(87)90037-X
Datta, A., Singh, R.K. & Kumar, S. (2015). Isolation, characterization and growth of Rhizobium strains under optimum conditions for effective biofertilizer production. Int. J. Pharm. Sci. Rev. Res., 32(1), 199-208.
Datta, B. & Chakrabartty, P.K. (2014). Siderophore biosynthesis genes of Rhizobium sp. isolated from Cicer arietinum L. 3 Biotech., 4(4), 391-401. doi: 10.1007/s13205-013-0164-y
Dobbelaere, S., Vanderleyden, J. & Okon, Y. (2003). Plant growth-promoting effects of diazotrophs in the rhizosphere. Crit. Rev. Plant Sci., 22, 107-149. https://doi.org/10.1080/713610853.
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.
Dutta, S. & Podile, A.R. (2010). Plant growth promoting rhizobacteria (PGPR): the bugs to debug the root zone. Crit. Rev. Microbiol., 36, 232-244. doi: 10.3109/10408411 003766806.
Ehteshamul-Haque, S. & Ghaffar, A. (1993). Uses of rhizobia in the control of root rot diseases of sunflower, okra, soybean and mungbean. J Phytopathol., 138, 157-163. doi: 10.1111/j.1439-0434.1993.tb01372.x
Gopalakrishnan, S., Srinivas, V., Prakash, B., Sathya, A. & Vijayabharathi, R. (2015). Plant growth-promoting traits of Pseudomonas geniculata isolated from chickpea nodules. 3 Biotech., 5, 653-661. https://doi.org/10.1007/s13205-014-0263-4.
Gopalkrishnan, S., Srinivas, V., Vemula, A., Samineni, S. & Rathore, A. (2018). Influence of diazotrophic bacteria on nodulation, nitrogen fixation, growth promotion and yield traits in five cultivars of chickpea. Biocatal. Agric. Biotech., 15, 35-42. https://doi.org/10.1016/j.bab.2018.05.006.
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
Honma, M. & Shimomura, T. (1978). Metabolism of 1-aminocyclopropane-1-carboxylic acid. Agric. Biol. Chem., 42, 1825-1831. https:// doi.org/10.1080/00021369.197 8.10863261.
Igiehon, N.O., Babalola, O.O. & Aremu, B.R. (2019). Genomic insights into plant growth promoting rhizobia capable of enhancing soybean germination under drought stress. BMC Microbiol., 19, 1-22. https://doi.org/10.1186/s12866-019-1536-1.
Imen, H., Neila, A., Adnane, B., Manel, B., Mabrouk, Y., Saidi, M. & Bouaziz, S. (2015). Inoculation with phosphate solubilizing Mesorhizobium strains improves the performance of chickpea (Cicer arietinum L.) under phosphorus deficiency. J. Plant Nutr., 38, 1656-1671. https://doi.org/10.1080/01904167.2015.1061543.
Jukanti, A.K., Gaur, P.M., Gowda, C.L.L. & Chibbar, R.N. (2012). Nutritional quality and health benefits of chickpea (Cicer arietinum L.): a review. Br. J. Nutr., 108, S11-S26. doi: 10.1017/S0007114512000797.
Kavamura, V.N., Santos, S.N., da Silva, J.L., Parma, M.M., Avila, L.A., Visconti, A. & de Melo, I.S. (2013). Screening of Brazilian cacti rhizobacteria for plant growth promotion under drought. Microbiol. Res., 168, 183-191. doi: 10.1016/J.MICRES.2012.12.002.
Khalid, R., Zhang, X.X., Hayat, R. & Ahmed, M. (2020). Molecular characteristics of rhizobia isolated from Arachis hypogaea grown under stress environment. Sustainability., 12(15), 6259. https://doi.org/10.3390/su12156259.
Kumari, P., Meena, M. & Upadhyay, R.S. (2018). Characterization of plant growth promoting rhizobacteria (PGPR) isolated from the rhizosphere of Vigna radiata (mung bean). Biocatal. Agric Biotechnol., 16, 155-162. doi: 10.1016/J.BCAB.2018.07.029.
Martinez-Hidalgo, P. & Hirsch, A.M. (2017). The nodule microbiome: N2-fixing rhizobia do not live alone. Phytobiomes J., 1, 70-82. https://doi.org/10.1094/PBIOMES-12-16-0019-RVW
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.
Menendez, E., Perez-Yepez, J., Hernandez, M., Rodriguez-Perez, A., Velazquez, E. & Leon-Barrios, M. (2020). Plant growth promotion abilities of phylogenetically diverse Mesorhizobium strains: Effect in the root colonization and development of tomato seedlings. Microorganisms., 8, 412. doi: 10.3390/microorganisms8030412.
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. https://doi.org/10.1016/j.cropro.2009.08.007.
Ozkoc, I. & Deliveli, M.H. (2001). In vitro inhibition of the mycelial growth of some root rot fungi by Rhizobium leguminosarum Biovar phaseoli isolates. Tur. J Biol., 25, 435-445.
Rasool, A., Mir, M.I., Zulfajri, M., Hanafiah, M.M., Unnisa, S.A. & Mahboob, M. (2021). Plant growth promoting and antifungal asset of indigenous rhizobacteria secluded from saffron (Crocus sativus L.) rhizosphere. Microb. Pathog., 150, 1047. doi: 10.1016/j.micpath.2021.104734.
Sagolshemcha, R., Devi, Y.N., & Singh, R. (2017). Plant growth promoting effect and biocontrol potential of Rhizobium spp. against Macrophomina phaseolina. Int. J. Curr. Microbiol. App. Sci., 6(6), 2695-2701. https://doi.org/10.20546/ijcmas.2017.606.320.
Saidi, S., Chebil, S., Gtari, M. & Mhamdi, R. (2013). Characterization of root-nodule bacteria isolated from Vicia faba and selection of plant growth-promoting traits. World J. Microbiol. Biotechnol., 29(6), 1099-1106. doi: 10.1007/s11274-013-178-4.
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.tb0 0446.x
Shahid, M., Khan, M.S., Syed, A., Marraiki, N. & Elgorban, A.M. (2021). Mesorhizobium ciceri as biological tool for improving physiological, biochemical and antioxidant state of Cicer arietinum (L.) under fungicide stress. Sci. Rep., 11, 1-18. doi: 10.1038/s41598-021-89103-9.
Singha, B., Mazumdar, P.B. & Pandey P. (2018). Characterization of plant growth promoting Rhizobia from root nodule of two legume species cultivated in Assam, India. Proc. Natl. Acad. Sci. India B Biol. Sci., 88, 1007-1016. doi: 10.1007/s40011-016-0836-6.
Solanki, M.K., Wang, Z., Wang, F.Y., Li, C.N., Lan, T.J., Singh, R.K. & Li, Y.R. (2017). Intercropping in sugarcane cultivation influenced the soil properties and enhanced the diversity of vital diazotrophic bacteria. Sugar Tech., 19, 136-147. doi: 10.1007/s12355-016-0445-y
Subramanian, P., Kim, K., Krishnamoorthy, R., Sundaram, S. & Sa, T. (2015). Endophytic bacteria improve nodule function and plant nitrogen in soybean on co-inoculation with Bradyrhizobium japonicum MN110. Plant Growth Regul, 76, 327-332. doi: 10.1007/s10725-014-9993-x
Tagele, S.B., Kim, S.W., Lee, H.G. & Lee, Y.S. (2019). Potential of novel sequence type of Burkholderia cenocepacia for biological control of root rot of maize (Zea mays L.) caused by Fusarium temperatum. Int. J. Mol. Sci, 20(5), 1005. doi: 10.3390/ijms20051005.
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.
Tariq, M., Hameed, S., Yasmeen, T., Zahid, M. & Zafar, M. (2014). Molecular characterization and identification of plant growth promoting endophytic bacteria isolated from the root nodules of pea (Pisum sativum L.). World J. Microbiolol. Biotechnol., 30(2), 719-725. doi: 10.1007/s11274-013-1488-9.
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/22.22.4673.
Verma, J.P., Yadav, J., Tiwaric, K.N. & Kumarb, 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. doi:10.1016/J.ECOLENG.2012.12.022.
Vincent, J.M. (1970). A manual for the practical study of root-nodule bacteria. Blackwell Scientific Publication., Oxford, 164p
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How to Cite
Screening of plant growth-promoting Rhizobium tarimense from root nodules of chickpea (Cicer arietinum). (2022). Journal of Applied and Natural Science, 14(2), 550-558. https://doi.org/10.31018/jans.v14i2.3439
