Abstract
Purpose
Chickpea is generally cultivated after seed treatment with host-specific Mesorhizobium ciceri, the nitrogen-fixing bacterium forming root nodules. Some species of free-living cyanobacteria are capable of nitrogen fixation. We examined the rhizosphere microbiota changes and the potential for plant growth promotion by applying a free-living, nitrogen-fixing cyanobacterium and the biofilm formulation of cyanobacterium with M. ciceri, relative to M. ciceri applied singly, to two each of desi and kabuli varieties of chickpea.
Materials and methods
Denaturing gradient gel electrophoresis (DGGE) profiles of archaeal, bacterial and cyanobacterial communities and those of phospholipid fatty acids (PLFAs) were obtained to evaluate the changes of the microbial communities in the chickpea rhizosphere. Plant growth attributes, including the pod yields and the availabilities of soil macronutrients and micronutrients, were monitored.
Results and discussion
The DGGE profiles showed distinct and characteristic changes due to the microbial inoculation; varietal differences exerted a marked influence on the archaeal and cyanobacterial communities. However, bacterial communities were modulated more by the type of microbial inoculants. Abundance of Gram-negative bacteria (in terms of notional PLFAs) differed between the desi and the kabuli varieties inoculated with M. ciceri alone, and the principal component analysis of PLFA profiles confirmed the characteristic effect of microbial inoculants tested. Microbial inoculation led to increases in the 100-seed weight and differential effects on the concentrations of available nitrogen and phosphorus, and those of iron, zinc and copper, suggesting their increased cycling in the rhizosphere.
Conclusions
Microbial inoculation of chickpea brought out the characteristic changes in rhizosphere microbiota. Consequently, the growth promotion of chickpea and nutrient cycling in its rhizosphere distinctively differed. Further studies are needed to analyse the association and dynamic changes in the microbial communities to define the subset of microorganisms selected by chickpea in its rhizosphere and the influence of microbial inoculation.
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References
Adak A, Prasanna R, Babu S, Bidyarani N, Verma S, Pal M, Shivay YS, Nain L (2016) Micronutrient enrichment mediated by plant-microbe interactions and rice cultivation practices. J Plant Nutr 39:1216–1232
Adesemoye AO, Kloepper JW (2009) Plant-microbes interactions in enhanced fertilizer-use efficiency. Appl Microbiol Biotechnol 85:1–12
Babu S, Bidyarani N, Chopra P, Monga D, Kumar R, Prasanna R, Kranthi S, Adak A, Saxena AK (2015) Evaluating microbe-plant interactions and varietal differences for enhancing biocontrol efficacy in root rot challenged cotton crop. Eur J Plant Pathol 142: 345-362
Bano N, Ruffin S, Ransom B, Hollibaugh JT (2004) Phylogenetic composition of arctic ocean archaeal assemblages and comparison with antarctic assemblages. Appl Environ Microbiol 70:781–789
Barea J-M, Pozo MJ, Azcon R, Concepcion A-A (2005) Microbial co-operation in the rhizosphere. J Expl Bot 56:1761–1778
Barnett JP, Millard A, Ksibe AZ, Scanlan DJ, Schmid R, Blindaue CA (2012) Mining genomes of marine cyanobacteria for elements of zinc homeostasis. Front Microbiol 3:142–147
Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68:1–13
Burjus SJ, Jawad ALM, Al-Ani NK (2014) Effect of two species of cyanobacteria as biofertilizers on characteristics and yield of chickpea plant. Iraqi J Sci 55:685–696
Buyer JS, Teasdale JR, Roberts DP, Zasada IA, Maul JE (2010) Factors affecting soil microbial community structure in tomato cropping systems. Soil Biol Biochem 42:831–841
Chaparro JM, Badri DV, Vivanco JM (2014) Rhizosphere microbiome assemblage is affected by plant development. The ISME J 8:790–803
Chen W-M, Moulin L, Bontemps C, Vandamme P, Béna G, Boivin-Masson C (2003) Legume symbiotic nitrogen fixation by beta-proteobacteria is widespread in nature. J Bacteriol 185:7266–7272
Elkoca E, Kantar F, Sahin F (2007) Influence of nitrogen fixing and phosphorus solubilizing bacteria on the nodulation, plant growth, and yield of chickpea. J Plant Nutr 31:157–171
Elkoca E, Kocli T, Gunes A, Turan M (2015) The symbiotic performance and plant nutrient uptake of certain nationally registered chickpea ( Cicer arietinum L.) cultivars of Turkey. J Plant Nutr 38:1427–1443
Ellouze W, Hamel C, Vujanovic V, Gan Y, Bouzid S, St-Arnaud M (2013) Chickpea genotypes shape the soil microbiome and affect the establishment of the subsequent durum wheat crop in the semiarid North American Great Plains. Soil Biol Biochem 63:129–141
Esfahani MN, Kusano M, Nguyen KH, Watanabe Y, Ha CV, Saito K, Sulieman S, Herrera-Estrella L, Phan Tran L-S (2016) Adaptation of the symbiotic Mesorhizobium-chickpea relationship to phosphate deficiency relies on reprogramming of whole-plant metabolism. Proc Natl Acad Sci U S A 113:E4610–E4619
FAOSTAT (2010) FAO statistical database. From Food and Agricultural Organization, Rome, Italy. www.faostat.fao.org/site/339/default.aspx#ancor
Frostegård Å, Bååth E (1996) The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biol Fertil Soils 22:59–65
Gaur R, Jeena G, Shah N, Gupta S, Pradhan S, Tyagi AK, Jain M, Chattopadhyay D, Bhatia S (2015) High density linkage mapping of genomic and transcriptomic SNPs for synteny analysis and anchoring the genome sequence of chickpea. Sci Rep. doi:10.1038/srep13387
Heuer H, Krsek M, Baker P, Smalla K, Wellington EMH (1997) Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gel-electrophoretic separation in denaturing gradients. Appl Environ Microbiol 63:3233–3241
Imran A, Mirza MS, Shah TM, Malik KA, Hafeez FY (2015) Differential response of kabuli and desi chickpea genotypes toward inoculation with PGPR in different soils. Front Microbiol 6:1–14
Janse I, Meima M, Kardinaal WEA, Zwart G (2003) High-resolution differentiation of cyanobacteria by using rRNA-internal transcribed spacer denaturing gradient gel electrophoresis. Appl Environ Microbiol 69:6634–6643
Jayasinghearachchi HS, Seneviratne G (2004) A bradyrhizobial-Penicillium spp. biofilm with nitrogenase activity improves N2 fixing symbiosis of soybean. Biol Fertil Soils 40:432–434
Kantar F, Elkoca E,Ogutcu H, Algur OF (2003) Chickpea yields in relation to Rhizobium inoculation from wild chickpea at high altitudes. J Agron Crop Sci 189:1-7
Kennedy IR, Tchan Y-T (1992) Biological nitrogen fixation in non-leguminous field crops: recent advances. Plant Soil 141:93–118
Kim DH, Kaashyap M, Rathore A, Das RR, Parupalli S, Upadhyaya HD, Gopalakrishnan S, Gaur PM, Singh S, Kaur J, Yasin M, Varshney RK (2014) Phylogenetic diversity of Mesorhizobium in chickpea. J Biosci 39:513–517
Lindsay WL, Norvell WA (1978) Development of a DTPA soil test for zinc, iron, manganese and copper. Soil Sci Soc America 42:421–428
Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, del Rio TG, Edgar RC, Eickhorst T, Ley RE, Hugenholtz P, Tringe SG, Dangl JL (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488:86–90
Mackinney G (1941) Absorption of light by chlorophyll. J Biol Chem 140:315–323
Marschner P, Marschner P, Crowley D, Crowley D, Yang CH, Yang CH (2004) Development of specific rhizosphere bacterial communities in relation to plant species, nutrition and soil type. Plant Soil 261:199–208
Mirza BS, Mirza MS, Bano A, Malik KA (2007) Coinoculation of chickpea with Mesorhizobium ciceri isolates from roots and nodules and phytohormone-producing Enterobacter strains. Aust J Expl Agric 47:1008–1015
Moulin L, Munive A, Dreyfus B, Boivin-Masson C (2001) Nodulation of legumes by members of the beta-subclass of proteobacteria. Nature 411:948–950
Muyzer G, Waal ED, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700
Namvar A, Sharifi RS, Khandan T, Moghadam MJ (2013) Seed inoculation and inorganic nitrogen fertilization effects on some physiological and agronomical traits of chickpea (Cicer arietinum L.) in irrigated condition. J Central Eur Agric 14:28–40
Nour SM, Fernandez MP, Normand P, Cleyet-Marel J-C (1994) Rhizobium ciceri sp. nov., consisting of strains that nodulate chickpeas (Cicer arietinum L.) Int J Syst Bacteriol 44:511–522
Olsen SR (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. US Dept Agric Circ 339, USDA, Washington
Prasanna R, Jaiswal P, Nayak S, Sood A, Kaushik BD (2009) Cyanobacterial diversity in the rhizosphere of rice and its ecological significance. Indian J Microbiol 49: 89-97
Prasanna R, Rana A, Chaudhary V, Joshi M, Nain L (2012) Cyanobacteria-PGPR interactions for effective nutrient and pest management strategies in agriculture. In: Satyanarayana T, Johri BN, Prakash A (eds) Microorganisms in sustainable agriculture and biotechnology. Springer, Dordrecht, pp 173–195
Prasanna R, Triveni S, Bidyarani N, Babu S, Yadav K, Adak A, Khetarpal S, Pal M, Shivay YS, Saxena AK (2014) Evaluating the efficacy of cyanobacterial formulations and biofilmed inoculants for leguminous crops. Arch Agron Soil Sci 60:349–366
Prasanna R, Bidyarani N, Babu S, Hossain F, Shivay YS, Nain L (2015a) Cyanobacterial inoculation elicits plant defense response and enhanced Zn mobilization in maize hybrids. Cogent Food Agric 1:995807
Prasanna R, Babu S, Bidyarani N, Kumar A, Triveni S, Monga D, Mukherjee AK, Kranthi S, Gokte-Narkhedhar Adak A, Yadav K, Nain L, Saxena AK (2015b) Prospecting cyanobacteria fortified composts as plant growth promoting and biocontrol agents in cotton. Exp Agric 51:42–65
Prasanna R, Kanchan A, Ramakrishnan B, Ranjan K, Venkatachalam S, Hossain F, Shivay YS, Krishnan P, Nain L (2016) Cyanobacteria-based bioinoculants influence growth and yields by modulating the microbial communities favourably in the rhizospheres of maize hybrids. Eur J Soil Biol 75:15–23
Ramsey PW, Rillig MC, Feris KP, Holben WE, Gannon JE (2006) Choice of methods for soil microbial community analysis : PLFA maximizes power compared to CLPP and PCR-based approaches. Pedobiologia 50:275–280
Ringelberg DB, Stair JO, Almeida J, Norby RJ, O’Neill EG, White DC (1997) Consequences of rising atmospheric carbon dioxide levels for the belowground microbiota associated with white oak. J Environ Quality 26:495–503
Roesti D, Gaur R, Johri BN (2006) Plant growth stage, fertiliser management and bio-inoculation of arbuscular mycorrhizal fungi and plant growth promoting rhizobacteria affect the rhizobacterial community structure in rain-fed wheat fields. Soil Biol Biochem 38:1111–1120
Rokhzadi A, Toashih V (2011) Nutrient uptake and yield of chickpea (Cicer arietinum L.) inoculated with plant growth- promoting rhizobacteria. J Plant Nutr 5:44–48
Romdhane SB, Aouani ME, Mhamdi R (2007) Inefficient nodulation of chickpea (Cicer arietinum L.) in the arid and Saharan climates in Tunisia by Sinorhizobium ciceri meliloti biovar medicaginis. Ann Microbiol 57:15–19
Rouhrazi K, Khodakaramian G (2015) Phenotypic and genotypic diversity of root-nodulating bacteria isolated from chickpea (Cicer arietinum L.) in Iran. Ann Microbiol 65:2219–2227
Schwieger F, Tebbe CC (2000) Effect of field inoculation with Sinorhizobium ciceri meliloti L33 on the composition of bacterial communities in rhizospheres of a target plant (Medicago sativa) and a non-target plant (Chenopodium album)—linking of 16S rRNA gene-based single-strand conformation polymorphism community profiles to the diversity of cultivated bacteria. Appl Environ Microbiol 66:3556–3565
Simon HM, Jahn CE, Bergerud LT, Sliwinski K, Weimer PJ, Willis DK, Robert M, Sliwinski MK, Goodman RM (2005) Cultivation of mesophilic soil crenarchaeotes in enrichment cultures from plant roots cultivation of mesophilic soil crenarchaeotes in enrichment cultures from plant roots. Appl Environ Microbiol 71:4751–4760
Singh M, Awasthi A, Soni SK, Singh R, Verma RK, Kalra A (2015) Complementarity among plant growth promoting traits in rhizospheric bacterial communities promotes plant growth. Sci Rep 5:15500
Snell F D and Snell C T (1954) Colorimetric Methods of Analysis, 3rd Edition, 4 Dyan Nostrand Company Inc, pp 512-513 & 516- 518, New York
Subbiah B, Asija G (1956) A rapid procedure for the estimation of available nitrogen in soils. Curr Sci 25: 259-260
Svitlana D (2013) Ecological safe growing of chickpea in the area of steppe of Ukraine. J Life Sci 7:1185–1190
Tagore GS, Namdeo SL, Sharma SK, Kumar N (2013) Effect of Mesorhizobium ciceri and phosphate solubilizing bacterial inoculants on symbiotic traits, nodule leghemoglobin, and yield of chickpea genotypes. Int J Agron Article ID 581627:8 pp
Trabelsi D, Mengoni A, Ben Ammar H, Mhamdi R (2011) Effect of on-field inoculation of Phaseolus vulgaris with rhizobia on soil bacterial communities. FEMS Microbiol Ecol 77:211–222
Van Cauwenberghe J, Michiels J, Honnay O (2015) Effects of local environmental variables and geographical location on the genetic diversity and composition of Mesorhizobium ciceri leguminosarum nodulating Vicia cracca populations. Soil Biol Biochem 90:71–79
Vessey J (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586
Virtanen AI, Jorma J, Linkola H, Linnasalmi A (1947) Relation between nitrogen fixation and leghaemoglobin. Acta Chem Scand 1:90–111
Yao H, He Z, Wilson MJ, Campbell CD (2000) Microbial biomass and community structure in a sequence of soil with increasing fertility and changing land use. Microb Ecol 40:223–237
Zelles L (1999) Fatty acid patterns of phospholipids and lipopolysaccharides in the characterisation of microbial communities in soil: a review. Biol Fertil Soils 29:111–129
Zhang L, Chen W, Burger M, Yang L, Gong P, Wu Z (2015) Changes in soil carbon and enzyme activity as a result of different long-term fertilization regimes in a greenhouse field. PLoS One 10:1–13
Zhou J, Guan D, Zhou B, Zhao B, Ma M, Qin J, Jiang X, Chen S, Cao F, Shen D, Li J (2015) Influence of 34 years of fertilization on bacterial communities in an intensively cultivated black soil in northeast China. Soil Biol Biochem 90:42–51
Acknowledgements
This investigation was partially funded by the funds from the Network Project on Microorganisms ‘Application of Microorganisms in Agricultural and Allied Sectors’ (AMAAS) granted by the Indian Council of Agricultural Research (ICAR), New Delhi, to RP and SERB project, DST, Government of India to BR. The authors gratefully acknowledge the support of Dr. Hegde, Division of Genetics, ICAR-IARI, in providing the chickpea germplasm and the Division of Agronomy, ICAR-IARI, New Delhi, for providing necessary facilities for the analyses of soil samples. The authors are also thankful to the Division of Microbiology, ICAR-IARI, New Delhi, for providing the necessary facilities to undertake this study.
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Ramakrishnan, B., Kaur, S., Prasanna, R. et al. Microbial inoculation of seeds characteristically shapes the rhizosphere microbiome in desi and kabuli chickpea types. J Soils Sediments 17, 2040–2053 (2017). https://doi.org/10.1007/s11368-017-1685-5
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DOI: https://doi.org/10.1007/s11368-017-1685-5