Abstract
In present investigation, six potential candidates of Mesorhizobium ciceri were isolated from five different districts of Eastern Uttar Pradesh and were characterized based on biochemical characteristics as well as 16S rDNA sequences. Isolates were analyzed for their multiple plant growth promoting traits, resistance to various environmental stresses such as temperature, pH and salt and were tested individually for growth and yield of three popular varieties of chickpea viz. Avarodi, Uday and PUSA-372, cultivated in the mid-Gangetic region of India. All the isolates exhibited siderophore production and were able to solubilize the inorganic phosphate and zinc. Among total, 50% isolates were found positive to produce ammonia and HCN whereas, IAA production was exhibited in 33.3% isolates. Most of the isolates were found able to tolerate environmental stresses. The growth and yield of Avarodhi and Uday chickpea varieties were found significantly higher when treated with M. ciceri strain S3N1 while in variety PUSA-372 it was exhibited when treated with M. ciceri strain VAR2.2. Present investigation concluded that a particular M. ciceri strain might not be wholly effective for a wide range of chickpea varieties. These strains may be effective bioinoculant for the growth and yield enhancement of chickpea.
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Abdelnaby M, Elnesairy NNB, Mohamed SH, Alkhayali YAA (2015) Symbiotic and phenotypic characteristics of rhizobia nodulaing Cowpea (Vigna Unguiculata L. Walp) Grown in Arid Region of Libya (Fezzan). J Environ Sci Eng 4:227–239. https://doi.org/10.17265/2162-5263/2015.05.001
Adams AS, Currie CR, Cardoza Y, Klepzig KD, Raffa KF (2009) Effects of symbiotic bacteria and tree chemistry on the growth and reproduction of bark beetle fungal symbionts. Can J Res 39:1133–1147
Ahmad F, Ahmad I, Khan MS (2006) Screening of free-living rhizospheric bacteria for their multiple plant growth promoting activities. Microbiol Res 163:173–181
Araujo ASF, Lopes ACA, Gomes RLF, Beserra Junior JEA, Antunes JEL, Lyra MCCP, Figueiredo MDVB (2015) Diversity of native rhizobia-nodulating Phaseolus lunatus in Brazil. Legume Res 38(5):653–657
Arnon DI (1949) Copper enzymes in straind chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15
Arshad M, Frankenberger WT (1993) Microbial production of plant growth regulators. In: Blaine F, Metting JR (eds) Soil microbial ecology. Marcel and Dekker Inc., New York, pp 307–347
Asei R, Ewusi-Mensah N, Abaidoo RC (2015) Response of soybean (Glycine max L.) to rhizobia inoculation and molybdenum application in the Northern savannah zones of Ghana. J Plant Sci 3:64–70. https://doi.org/10.11648/j.jps.2015302.14
Atieno M, Hermann L, Okalebo R, Lesueur D (2012) Efficiency of different formulations of Bradyrhizobium japonicum and effect of co-inoculation of Bacillus subtilis with two different strains of Bradyrhizobium japonicum. World J Microbiol Biotechnol 28:2541–2550
Bakker AW, Schipper B (1987) Microbial cyanide production in the rhizosphere in relation to potato yield reduction and Pseudomonas spp. mediated plant growth stimulation. Soil Biol and Biochem 19: 451 457
Baliah NT, Pandiarajan G, Kumar BM (2016) Isolation, identification and characterization of phosphate solubilizing bacteria from different crop soils of Srivilliputtur Taluk, Virudhunagar District, Tamil Nadu. Tropical Ecol 57(3):465–474
Bano N, Musarrat J (2003) Characterizationof anew Pseudomonas aeruginosa strain NJ-15 as a potential biocontrol agent. Curr Microbiol 46:324–328
Ben-David A, Davidson CE (2014) Estimation method for serial dilution. J Microbio Methods 107:214–221
Bertamini M, Zulini L, Muthuchelian K, Nedunchezhian N (2006) Effect of water deficit on photosynthetic and other physiological responses in grapevine (Vitis vinifera L. cv.Riesling) plants. Photosynthetica 44:151–154
Bertrand A, Dhont C, Bipfubusa M, Chalifour FP, Drouin P, Beauchamp CJ (2015) Improving salt stress responses of the symbiosis in alfalfa using salt-tolerant cultivar and rhizobial strain. Appl Soil Ecol 87:108–117
Bhagat D, Sharma P, Sirari A, Kumawat KC (2014) Screening of Mesorhizobium spp. for control of Fusarium wilt in chickpea in vitro conditions. Int J Curr Microbiol Appl Sci 3(4):923–930
Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbio Biotech 28:1327–1350
Boddey RM, Dobereiner J (1995) Nitrogen fixation associated with grasses and cereals: recent progress and perspectives for the future. Fertil Res 42:241–250
Brígido C, Alexandre A, Oliveira S (2012) Transcriptional analysis of major chaperone genes in salt-tolerant and salt-sensitive mesorhizobia. Microbiol Res 167:623–629
Cappuccino JC, Sherman N (1992) In: Microbiology: a laboratory manual, New York, pp 125–179
Cecchin I, Terezinha FF (2004) Effect of nitrogen supply on growth and photosynthesis of sunflower plants grown in the greenhouse. Plant Sci 166:1379–1385
Chaudhary D, Sindhu SS (2015) Inducing salinity tolerance in chickpea (Cicer arientinum L.) by inoculation of 1-aminocyclopropane-1-caroxylic acid deaminase containing Mesorhizobium strains. African J Microbiol Res 9(2):117–124
De Freitas JR, Banerjee MR, Germida JJ (1997) Phosphate-solubilizing rhizobacteria enhance the growth and yield but not phosphorus uptake of canola (Brassica napus L.). Biol Fert Soils 24:358–364
Dong R, Zhang J, Huan H, Bai C, Chen Z, Liu G (2017) High salt tolerance of a bradyrhizobium strain and its promotion of the growth of stylosanthes guianensis. Int J Mol Sci 18:1625–1642
Elizabeth W, O’Hara GW, Howieson J, Glenn AR (2000) Identification of tolerance to soil acidity in inoculant strains of Rhizobium leguminosarum bv Trifolii. Soil Biol Biochem 32(10):193–1403
Gaur AC (1990) Phosphate solubilizing microorganisms as biofertilizers. Omega Scientific Publishers, New Delhi, p 198
Hameeda B, Harini G, Rupela OP, Wani SP, Reddy G (2008) Growth promotion of maize by phosphate-solubilizing bacteria isolated from composts and macrofauna. Microbiol Res 163:234–242
Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant Soil 237(2):173–195
Hogg DE (1976) Effect of the soil aeration on the growth of white clover in a glass house pot experiment. New Zealand J of Exp Ag 4(4):467–468
Huda S, Siddique NA, Khatun N, Rahman MH, Morshed M (2003) Regeneration of shoot from cotyledon derived callus of chickpea (Cicer arietinum L.). Pak J Biol Sci 6:1310–1313
Jida M, Assefa F (2012) Phenotypic diversity and plant growth promoting characteristics of Mesorhizobium species isolated from chickpea (Cicer arietinum L.) growing areas of Ethiopia. Afr J Biotech 11(29):7483–7493
Jukanti AK, Gaur PM, Gowda CL, Chibbar RN (2012) Nutritional quality and health benefits of chickpea (Cicer arietinum L.): a review. Br J Nutri 108:11–26
Kamran S, Shahid I, Baig DN, Rizwan M, Malik KA, Mehnaz S (2017) Contribution of zinc solubilizing bacteria in growth promotion and zinc content of wheat. Front Microbiol 8:2593
Kaur N, Sharma P (2013) Screening and characterization of native Pseudomonas sp. as plant growth promoting rhizobacteria in chickpea (Cicer arietinum L.) rhizospere. Afr J Microbiol Res 7:1465–1474
Kaur N, Sharma P, Sharma S (2015) Co-inoculation of Mesorhizobium sp. and plant growth promoting rhizobacteria Pseudomonas sp. as bio-enhancer and biofertilizer in chickpea (Cicer arietinum L.). Legume Res 38:367–374
Khande R, Sushil KS, Ramesh A, Mahaveer PS (2017) Zinc solubilizing Bacillus strains that modulate growth, yield and zinc biofortification of soybean and wheat. Rhizosphere 4:126–138
Koli DK, Swarnalakshmi K (2017) Isolation and characterization of nodule associated bacteria from chickpea and their potential for plant growth promotion. Int J Curr Microbiol App Sci 6(5):1992–2004
Korir H, Mungai NW, Thuita M, Hamba Y, Masso C (2017) Co-inoculation effect of rhizobia and plant growth promoting rhizobacteria on common bean growth in a low phosphorus soil. Front Plant Sci 8:141
Küçük C, Kıvanç M (2008) Preliminary characterization of Rhizobium strains isolated from chickpea nodules. Afr J Biotech 7:772–775
Kumar J, Abbo S (2001) Genetics of flowering time in chickpea and its bearing on productivity in semiarid environments. Adv Agron 72:107–138
Laranjo M, Oliveira S (2011) Tolerance of Mesorhizobium type strains to different environmental stresses. Antoni van Leeuwenhoek 99:651–662
Maâtallah J, Berraho EB, Sanjuan J, Lluch C (2002) Phenotypic characterization of rhizobia isolated from chickpea (Cicer arietinum) growing in Moroccan soils. Agronomie 22:321–329
Malik DK, Sindhu SS (2011) Production of indole acetic acid by Pseudomonas sp.: effect of coinoculation with Mesorhizobium sp. Cicer on nodulation and plant growth of chickpea (Cicer arietinum). Physiol Mol Bio Plants 17(1):25–32
Mathu S, Herrmann L, Pypers P, Matiru R, Lesueur D (2017) Potential of indigenous bradyrhizobia versus commercial inoculants to improve cowpea (Vigna unguiculata L. walp) and green gram (Vigna radiate L. wilczek.) yields in Kenya. Soil Sci Plant Nutr 58:750–763
Messaoud BB, Aboumerieme I, Nassiri LE, Fahime E, Ibijbijen J (2014) Phenotypic and genotypic characteristics of rhizobia Straind from meknes-tafilalet soils and study of their ability to nodulate Bituminaria bituminosa. Br Microbiol Res J 4(4):405–417
Mishra PK, Mishra S, Selvakumar G, Bishr JK, Kundu S, Gupta HS (2009) Co-inoculation of Bacillus thuringeinsis-KR1 with Rhizobium leguminosarum enhances plant growth and nodulation of pea (Pisum sativum L.) and lentil (Lens culinaris L.). World J Microbiol Biotechnol 25:753–761
Mishra I, Sapre GS, Tiwar S (2017) Zinc solubilizing bacteria from the hizosphere of rice as prospective modulator of zinc biofortification in rice. Rhizosphere 3:185–190
Moussaid S, Domínguez-Ferreras A, Muñoz S, Aurag J, Sanjuán J (2017) Increased trehalose biosynthesis improves Mesorhizobium ciceri growth and symbiosis establishment in saline conditions. Symbiosis 67:103–111
Muneer S, Jeong BR (2015) Proteomic analysis provides new insights in phosphorus homeostasis subjected to pi (inorganic phosphate) starvation in tomato plants (Solanum lycopersicum L.). PLoS ONE 10:1–18
Nieto-Jacobo MF, Steyaert JM, Salazar-Badillo FB, Nguyen DV, Rostás M, Braithwaite M, De Souza JT, Jimenez-Bremont JF, Ohkura M, Stweart A et al (2017) Environmental growth conditions of Trichoderma spp. affects indole acetic adic derivates, volatile organic compounds, and plant growth promotion. Front Plant Sci 8:102. https://doi.org/10.3389/fpls.2017.00102
Ozer S, Karakoy T, Toklu F, Baloch FS, Kilian B, Ozkan H (2010) Nutritional and physico-chemical variation in Turkish Kabuli chickpea (Cicer arietinum L.) landraces. Euphytica 175:237–249
Pandey RP, Srivastava AK, Srivastava AK, Ramteke PW (2018) Antagonistic activity of Mesorhizobium ciceri against phytopathogenic fungi Fusarium oxysporum f. sp. ciceris. Trends in Biosci 11(5):637–639
Pérez-Fernández M, Alexander V (2017) Enhanced plant performance in Cicer arietinum L. due to the addition of a combination of plant growth-promoting bacteria. Agriculture 7:40
Qu LQ, Huang YY, Zhu CM, Zeng HQ, Shen CJ, Liu C, Zhao Y, Pi EX (2016) Rhizobia-inoculation enhances the soybean’s tolerance to salt stress. Plant Soil 400:209–222
Rai R, Dash PK, Mohapatra T, Singh A (2012) Phenotypic and molecular characterization of indigenious rhizobia nodulating chickpea in India. Indian J Exp Bio 50(5):340–350
Rupela OP (1987) Nodulation and nitrogen fixation in chickpea. CAB International, Wallingford, pp 196–206
Sammauria R, Kumawat S (2018) Legume plant growth-promoting rhizobacteria (PGPRs): role in soil sustainability. in book: legumes for soil health and sustainable management. pp 409–443. https://doi.org/10.1007/978-981-13-0253-4_13
Sankar PM, Vanitha S, Kamalakannan A, Raju PA, Jeyakumar P (2018) Prevalence of Fusarium oxysporum f. sp. ciceris causing wilt in chickpea and its pathogenic, cultural and morphological characterization. Int J Curr Microbiol Appl Sci 7(2):1301–1313
Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56
Sharma SB, Sayyed RZ, Trivedi MH, Gobi TA (2013a) Phosphate solubilising microbes:sustainable approach for managing phosphorus deficiency in agricultural soils. Springerplus 2:587
Sharma P, Khanna V, Kaur N, Dhillon G, Singh G, Sharma S, Kaur H, Saxena AK (2013b) Effect of dual inoculation of Pseudomonas argentinensis LPGPR1 and Mesorhizobium on growth of chickpea (Cicer arietinum L.). J Res Punjab Agril Univ 50:1–4
Singh RK, Malik N, Singh S (2013) Improved nutrient use efficiency increases plant growth of rice with the use of IAA-overproducing strains of endophytic Burkholderia cepacia strain RRE25. Microbial Ecol 66:375–384
Singh RP, Manchanda G, Singh RN, Srivastava AK, Dubey RC (2015) Selection of alkalotolerant and symbiotically efficient chickpea nodulating rhizobia from North-West Indo Gangetic Plains. J Basic Microbiol 55:1–12
Singh P, Shahi B, Singh KM (2017a) Trends of pulses production, consumption and import in India: current scenario and strategies. 04:5581589 (http://mrpa.ub.uni-muenchen.de/81589/)
Singh Z, Singh G, Aggarwal N (2017b) Effect of Mesorhizobium, plant growth promoting rhizobacteria and phosphorus on plant biometery and growth indices of desi chickpea (Cicer arietinum L.). J Appl Natural Sci 9(3):1422–1428
Talbi C, Argandoña M, Salvador M, Alché JD, Vargas C, Bedmar EJ, Delgado MJ (2013) Burkholderia phymatum improves salt tolerance of symbiotic nitrogen fixation in Phaseolus vulgaris. Plant Soil 367:673–685
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729
Tena W, Wolde-Meskel E, Walley F (2016) Response of chickpea (Cicer arietinum L.) to inoculation with native and exotic Mesorhizobium strains in Southern Ethiopia. Afr J Biotechnol 15(35):1920–1929
Ulzen J, Abaidoo RC, Mensah NA, Masso C, AbdelGadir AH (2016) Bradyrhizobium inoculants enhance grain yields of soybean and cowpea in Northern Ghana. Front Plant Sci 7:1770
van der Maesen LJG (1984) Taxonomy, distribution and evolution of the chickpea and its wild relatives, pp 95–104. In: Genetic Resources and their ExploitationChickpea, Faba beans and Lentils (Eds. J.R. Witcombe and W. Erskine), Martinus Nijhoff/Dr. W. Junk Publishers, The Hague, The Netherlands
Verma JP, Yadav J, Tiwari KN (2012) Enhancement of nodulation and yield of chickpea by co-inoculation of indigenous Mesorhizobium spp. and plant growth-promoting rhizobacteria in eastern Uttar Pradesh. Commun Soil Sci Plant Anal 43:605–621
Verma JP, Yadav J, Tiwari KN, 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
Vincent JM (1970) A manual for the practical study of root-nodule bacteria. Intern Biol Prog. Blackwell Scientific, Oxford
Vishnu-Mittre B (1974) The beginnings of agriculture: palaeobotanical evidence in India. In: Hutchinson J (ed) Evolutionary studies in world crops. Cambridge University Press, London, p 3-3Q
Vylkova S (2017) Environmental pH modulation by pathogenic fungi as a strategy to conquer the host. Plos Pathol 13(2):e1006149
Wang YF, Zhang ZQ, Zhang P, Cao YM, Hu TM, Yang PZ (2016) Rhizobium symbiosis contribution to short-term salt stress tolerance in alfalfa (Medicago sativa L.). Plant Soil 402:247–261
Wolde-meskel E, van Heerwaarden J, Abdulkadir B, Kassa S, Aliyi I, Degefu T, Wakweya K, Kanampin F, Giller KE (2018) Additive yield response of chickpea (Cicer arietinum L.) to rhizobium inoculation and phosphorus fertilizer across smallholder farms in Ethiopia. Agric Ecosyst Environ 261:144–152
Yadav K (2009) Cultivation of chickpea (Cicer arientinum L.). Agropedia, ICAR-NAIP (http://agropedia.iitk.ac.in/content/cultivation-chick-pea-cicer-arientinum-l)
Yadav P, Chandra R, Pareek N, Raverkar KP (2018) Screening of multi-trait mesorhizobium isolates for plant growth promotion and nitrogen fixation in chickpea (Cicer arietinum L.). Int J Curr Microbiol App Sci 7(8):2592–2599. https://doi.org/10.20546/ijcmas.2018.708.266
Yan N, Zhang YL, Xue HM, Zhang XH, Wang ZD, Shi LY, Guo DP (2015) Changes in plant growth and photosynthetic performance of Zizania latifolia exposed to different phosphorous concentrations under hydroponic condition. Photosynthetica 53:630–635
Zapata F, Zaharah AR (2002) Phosphate availability from phosphate rock and sewage sludge as influenced by addition of water soluble phosphate fertilizers. Nutri Cycl Agroeco 63(1):43–48
Zhang H, Sun Y, Xie X, Kim MS, Dowd SE, Paré PW (2009) A soil bacterium regulates plant acquisition of iron via deficiency inducible mechanisms. Plant J 58:568–577
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Pandey, R.P., Srivastava, A.K., Gupta, V.K. et al. Enhanced yield of diverse varieties of chickpea (Cicer arietinum L.) by different isolates of Mesorhizobium ciceri. Environmental Sustainability 1, 425–435 (2018). https://doi.org/10.1007/s42398-018-00039-9
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DOI: https://doi.org/10.1007/s42398-018-00039-9