Phytobeneficial Traits and Ecophysiological Stress Tolerance of Rhizobia
DOI:
https://doi.org/10.18034/ra.v6i2.329Keywords:
Phytobeneficial traits, Ecophysiology, nitrogen fixation, Phosphate solubilization, siderophore production, rhizosphereAbstract
The microorganisms with the aim of improving nutrients availabile for plants are an important practice and necessary for agriculture. During the past couple of decades, plant growth-promoting (PGP) rhizobia have been begun to replace the use of chemicals in agriculture, horticulture and environmental cleanup strategies. Scientific researches involve multidisciplinary approaches to understand adaptation of plant growth promoting rhizobacteria (PGPR), their effects on plant physiology and growth, induced systemic resistance, biocontrol of plant pathogens, biofertilization and their tolerance to ecophysiological stresses. This is due to the emerging demand for dependence diminishing of synthetic chemical products, to the growing necessity of sustainable agriculture within a holistic vision of development and to focuss on environmental protection. PGP rhizobia are naturally occurring soil bacteria that aggressively colonize plant roots and benefit plants by providing growth promotion and biological nitrogen fixation (BNF). Inoculation of crop plants with certain strains of PGP rhizobia at an early stage of development improves biomass production and yields through direct and indirect effects on roots and shoots growth. In this review, we have discussed the phytobeneficial traits of rhizobia which act as PGPR, and their ecophysiological properties, biocontrolability, mechanisms and the desirable properties exhibited by them.
Downloads
References
Adesemoye AO, Kloepper J (2009) Plant-microbes interactions in enhanced fertilizer-use efficiency. Applied Microbiology and Biotechnology 14: 1-12.
Ahmad, F., Ahmad, I. and Khan, M.S. (2008) Screening of Free-Living Rhizospheric Bacteria for Their Multiple Plant Growth Promoting Activities. Microbiological Research, 163, 173-181. http://dx.doi.org/10.1016/j.micres.2006.04.001
Ahemad M, Khan MS, Zaidi A andWani PA, (2009) Remediation of herbicides contaminated soil using microbes, in Microbes in Sustainable Agriculture, ed. by Khan MS, Zaidi A and Musarrat J. Nova Science Publishers, New York, USA, pp. 261–284
Ahemad M, Khan MS (2011) Insecticide-tolerant and plant-growthpromoting Rhizobium improves the growth of lentil (Lens esculentus) in insecticide-stressed Soils. Pest Manag Sci; 67: 423–429
Ahemad M, Khan MS (2012c) Effects of pesticides on plant growth promoting traits of Mesorhizobium strain MRC4. J Saudi Soc Agric Sci 11:63–71
Aajoud A, Ravanel P and Tissut M, (2003) Fipronilmetabolism and dissipation in a simplified aquatic ecosystem. J Agric Food Chem 51:1347–1352.
Akhtar N, Qureshi MA, Iqbal A, Ahmad MJ, Khan KH (2012) Influence of Azotobacter and IAA on symbiotic performance of Rhizobium and yield parameters of lentil. J Agric Res 50:361–372.
Anna K., Carole L., Neil Emery R. J., and Florian F,(2013) Bioactive Cytokinins Are Selectively Secreted by Sinorhizobium meliloti Nodulating and Nonnodulating Strains; MPMI Vol. 26, No. 10, 2013, pp. 1225–1231
Anand A, Jaiswal SK, Dhar B, Vaishampayan A (2012) Surviving and thriving in terms of symbiotic performance of antibiotic and phage-resistant mutants of Bradyrhizobium of soybean [Glycine max (L.) Merrill]. Curr Microbiol 65:390–397
Anitha, G. and Kumudini, B. S. (2014) Isolation and characterization of fluorescent pseudomonads and their effect on plant growth promotion.Journal of Environmental biology, 35, 627-634.
Afzal A, Bano A (2008) Rhizobium and phosphate solubilizing bacteria improve the yield and phosphorus uptake in wheat (Triticum aestivum L.). Int J Agric Biol 10:85–88
Arora NK, Kang SC, Maheshwari DK (2001) Isolation of siderophore producing strains of Rhizobium meliloti and their biocontrol potential against Macrophomina phaseolina that causes charcoal rot of groundnut. Curr Sci 81:673–677
Balassa G (1963) Genetic transformation of Rhizobium: A review of the work of R. Balassa. Bacteriol Rev 27:22
Bandelier S, Renaud R, Durand A. (1997) Production of gibberellic acid by fed batch solid-state fermentation in an aseptic pilot scale reactor. Process Biochem 32: 141-145.
Bashan Y, de Bashan LE (2005) Bacterial plant growth promotion. In: Hillel D (ed) Encyclopedia of soils in the environment. Elsevier, Oxford, pp 103–115
Belachew T (2010) Intrinsic antibiotic resistance, survival of Rhizobium leguminosarum strains and fixation potential of pea varieties (Pisum sativum L.) in southeast Ethiopia. Int J Microbiol Res 2:75–79
Beltra R, Del-Solar G, Sanchez-Serrano JJ, Alonso E (1988) Mutants of Rhizobium phaseoli HM Mel (2) obtained by means of elevated temperatures. Zentbl Mikrobiol 143:529–532
Beneduzi A, Ambrosini A, Luciane Passaglia MP (2012) Plant growth-promoting rhizobacteria (PGPR): Their potential as antagonists and biocontrol agents. Genetics and Molecular Biology 35: 1044-1051.
Berendsen RL, Pieterse CM, Bakker PAHM (2012). The rhizosphere microbiome and plant health. Trends in Plant Science 17: 478-486.
Bhargava1, Y., Murthy, J. S. R., Rajesh Kumar T. V., Narayana Rao M. (2016) Phenotypic, Stress Tolerance and Plant Growth Promoting Characteristics of Rhizobial Isolates from Selected Wild Legumes of Semiarid Region, Tirupati, India Advances in Microbiology, 6, 1-12
Bhattacharyya PN, Jha DK (2012) Plant growth-promoting Rhizobacteria (PGPR): emergence in agriculture. World J Microbiol Biotechnol 28:1327–1350
Bobe A, Coste CM and Cooper JF, (1997) Factors influencing the adsorption of fipronil in soils. J Agric Food Chem 45:4861–4865.
Bodek I, Lyman WJ, Reehl WF, Rosenblatt DH (1988) Environmental inorganic chemistry: properties, processes, and estimation methods. In: Walton BT, Conway RA (eds) SETAC special publication series. Pergamon Press, New York
Boğa A, Binokay S, Sertdemir Y. (2009) The toxicity and teratogenicity of gibberellic acid (GA3) based on the frog embryo teratogenesis assay-Xenopus (FETAX). Turk J Biol 33: 181 188.
Boiero L, Perrig D, Masciarelli O, Penna C, Cassan F, Luna V (2007) Phytohormone production by three strains of Bradyrhizobium japonicum and possible physiological and technological implications. Appl Microbiol Biotechnol 74:874–880
Buol S, Eswaran H (2000) Oxisols. Adv Agron 68:151–195 Caba JM, Centeno ML, Fernandez B, Gresshoff PM, Ligero F (2000) Inoculation and nitrate alter phytohormone levels in soybean roots: differences between a super nodulating mutant and the wild type. Planta 211:98–104
Camerini S, Senatore B, Lonardo E, Imperlini E, Bianco C, Moschetti G, Rotino GL, Campion B, Defez R (2008) Introduction of a novel pathway for IAA biosynthesis to rhizobia alters vetch root nodule development. Arch Microbiol 190:67–77
Cassan F, Perrig D, Sgroy V, Masciarelli O, Penna C, Luna V (2009) Azospirillum brasilense Az39 and Bradyrhizobium japonicum E109, inoculated singly or in combination, promote seed germination and early seedling growth in corn (Zea mays L.) and soybean (Glycine max L.). Eur J Soil Biol 45:28–35
Castro IV, Ferreira EM, McGrath SP (1997) Effectiveness and genetic diversity of Rhizobium leguminosarum bv. trifolii isolates in Portuguese soils polluted by industrial effluents. Soil Biol Biochem 29:1209–1213
Chaudri AM, Allain CMG, Barbosa-Jefferson VL, Nicholson FA, Chambers BJ, McGrath SP (2000) A study of the impacts of Zn and Cu on two rhizobial species in soils of a long-term field experiment. Plant Soil 221:167–179
Chein CT, Maundu J, Cavaness J, Daudurand LM, Orser CS (1992) Characterization of salt-tolerant and salt-sensitive mutants of Rhizobium leguminosarum biovar viciae strain C1204b. FEMS Microbiol Lett 90:135–140
Cocking E C,Webster G, Batchelor C A and Davey M R (1994) Nodulation of non-legume crops. A new look. Agro-Food-Industry Hi-Tech. Jan 21–24.
Cole MA, Elkan GH (1973) Transmissible resistance to penicillin G, neomycin, and chloramphenicol in Rhizobium japonicum. Antimicrob Agents Chemother 4:248–253
Compant S, Duffy B, Nowak J, Clement C, Barka EA. (2005) Use of plant growth promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl Environ Microbiol;71:4951–9.
Davies PJ (1995) The plant hormones: their nature, occurrence and functions. In: Davies PJ (ed) Plant hormones: physiology, biochemistry and molecular biology. Kluwer Academic Publishers, Dordrecht, pp 1–12
Deanand BJ, Patil AB, Kulkaarni JH, Algawadi AR (2002) Effect of plant growth promoting rhizobacteria on growth and yield of pigeonpea (Cajanus cajan L.) by application of plant growth promoting rhizobacteria. Microbiol Res 159:371–394
Deshwal VK, Dubey RC, Maheshwari DK (2003a) Isolation of plant growth promoting strains of Bradyrhizobium (Arachis) sp. With biocontrol potential against Macrophomina phaseolina causing charcoal rot of peanut. Curr Sci 84:443–444
Downie A (1997) Fixing a symbiotic circle. Nature 387:352–353
El Sheikh EE, Wood M (1990) Salt effects on survival and multiplication of chickpea and soybean rhizobia. Soil Biol Biochem 22:343–347
Etesami, H., Hossein, A.A. and Abolfazl, A.A. (2009) Evaluation of Plant Growth Hormones Production (IAA) Ability by Iranian Soils Rhizobial Strains and Effects of Superior Strains Application on Wheat Growth Indexes. World Applied Sciences Journal, 6, 1576-1584.
Faghire, M., Mohamed, F., Taoufiq, K., Fghire, R., Bargaz, A., Mandri, B., Oufdou, K., Laury, A., Drevon, J.J. and Ghoulam, C. (2013) Genotypic Variation of Nodules’ Enzymatic Activities in Symbiotic Nitrogen Fixation among Common Bean (Phaseolus vulgaris L.) Genotypes Grown under Salinity Constraint. Symbiosis, 60, 115-122. http://dx.doi.org/10.1007/s13199-013-0247-x
Fischer HM. (1994) Genetic regulation of nitrogen fixation in rhizobia. Microbiol Rev. 58:352–86.
Frankenberger WTJ, Arshad M (1995) Photohormones in soil: microbial production and function. Dekker, New York
Fravel D. (1988) Role of antibiosis in the biocontrol of plant diseases. Annu Rev Phytopathol; 26:75–91.
Frioni L, Rodrıguez A, Meerhoff M (2001) Differentiation of rhizobia isolated from native legume trees in Uruguay. Appl Soil Ecol 16:275–282
Gadre S, Mazumdar L, Modi V, Parekh V (1967) Interspecific transformation in Rhizobium. Arch fu¨r Mikrobiologie 57:388–391
Gianfreda L, Rao MA (2004) Potential of extra cellular enzymes in remediation of polluted soils: a review. Enzyme Microb Technol 35:339–354
Gonzalez-Pasayo R, Martinez-Rpmero E (2000) Multiresistance genes of Rhizobium etli CFN42. MPMI 13:572–577
Gopalakrishnan S, Watanabe T, Pearse SJ, Ito O, Hossian AKMZ, Subbarao GV (2009) Biological nitrification inhibition by Brachiaria humidicola roots varies with soil type and inhibits nitrifying bacteria, but not other major soil microorganisms. Soil Sci Plant Nutr 55:725–733
Graham PH, Draeger KJ, Ferrey ML, Conroy MJ, Hammer BE, Martı´nez E, Aarons SR, Quinto C (1994) Acid pH tolerance in strains of Rhizobium and Bradyrhizobium, and initial studies on the basis for acid tolerance of Rhizobium tropici UMR1899. Can J Microbiol 40:198–207
Graham, P.H. and Vance, C.P. (2000) Nitrogen fixation in perspective: an overview of research and extension needs. Field Crops Res. 65:93–106.
Gray J, Murphy B (2002) Parent material and world soil distribution, 17th world congress of soil science. Bangkok, Thailand
Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica, Article ID 963401. doi:http://dx.doi. org/10.6064/2012/963401
Gupta A, Saxena AK, Gopal M, Tilak KVBR (1998) Effect of plant growth promoting rhizobacteria on competitive ability of introduced Bradyrhizobium sp. (Vigna) for nodulation. Microbiol Res 153:113–117
Gupta CP, Dubey RC, Kang SC, Maheshwari DK.(2001).Antibiosis mediated necrotrophiceffect of Pseudomonas GRC2 against two fungal pathogens. Curr Sci;81:91–4.
Halder AK, Chakrabarty PK (1993) Solubilization of inorganic phosphate by Rhizobium. Folia Microbiol 38:325–330
Halder AK, Mishra AK, Bhattacharya P, Chakrabarthy PK (1990) Solubilization of rock phosphate by Rhizobium and Bradyrhizobium. J Gen Appl Microbiol 36:1–92
Hall AE (2004) Breeding for adaptation to drought and heat in cowpea. Eur J Agron 21:447–454
Haas D, Defago G (2005). Biological control of soil-borne pathogens by fluorescent pseudomonads. Nature. Rev. Microbiol., 1038: 1-13.
Hernandez-Lucas, I., Segovia, L., Martínez-Romero, E., and Pueppke, S.G. (1995). Appl. Environ. Microbiol. 61, 2775–2779.
Höflich, G., Wiehe, W., and Kühn, G. (1994) Plant growth stimulation by inoculation with the symbiotic and associative rhizosphere microorganisms. Experientia 50:897–905.
Höflich, G., Wiehe, W., and Hecht-Buchholz, C., (1995) Rhizosphere colonization of different crops with growth promoting Pseudomonas and Rhizobium bacteria. Microbiol. Res. 150:139–147
Hungria M, Franco AA (1993) Effects of high temperature on nodulation and nitrogen fixation by Phaseolus vulgaris L. Plant Soil 149:95–102
Jebara M, Mhamdi R, Aouani ME, Ghrir R, Mars M (2001) Genetic diversity of Sinorhizobium populations recovered from different Medicago varieties cultivated in Tunisian soils. Can J Microbiol 47:139–147
Karanja NK, Wood M (1988) Selecting Rhizobium phaseoli strains for use with beans (Phaseolus vulgaris L.) in Kenya. Tolerance of high temperature and antibiotic resistance. Plant Soil 112:15–22
Khan, M.S., Zaidi, A. and Wani, P.A. (2006) Role of Phosphate-Solubilizing Microorganisms in Sustainable Agriculture-A Review. Agronomy for Sustainable Development, 27, 29-43. http://dx.doi.org/10.1051/agro:2006011
Kinkle BK, Sadowsky MJ, Johnstone K, Kokinen WC (1994) Tellurium and selenium resistance in rhizobia and its potential use for direct isolation of Rhizobium meliloti from Soil. Appl Environ Microbiol 60:1674–1677
Kloepper JW, Schroth MN (1981) Relationship of in vitro antibiosis of plant growth promoting rhizobacteria to plant growth and the displacement of root microflora. Phytopathol 71: 1020-1024.
Krasova-Wade T, Diouf O, Ndoye I, Sall CE, Braconnier S, Neyra M (2006) Water condition effects on rhizobia competition for cowpea nodule occupancy. African J Biotech 5:1457–1463
Kumar S, Mukerji KG, Lai R (1996) Molecular aspects of pesticide degradation by microorganisms. Crit Rev Microbiol 22:1–26
Lakzian A, Murphy P, Turner A, Beynon JL, Giller KE (2002) Rhizobium leguminosarum bv. viciae populations in soils with increasing heavy metal contamination: abundance, plasmid profiles, diversity and metal tolerance. Soil Biol Biochem 34:519–529
Lloret J, Wulff BBH, Rubio JM, Downie JA, Bonilla I, Rivilla R (1998) Exo-polysaccharide II production is regulated by salt in the halotolerant strain Rhizobium meliloti EFB1. J Bacteriol 179:5366–5371
Lloret J, Bolanos L, Lucas MM, Peart JM, Brewin NJ, Bonilla I, Rivilla R (1995) Ionic stress and osmotic pressure induce different alterations in the lipopolysaccharide of a Rhizobium meliloti strain. Appl Environ Microbiol 61:3701–3704
Lugtenberg B, Kamilova F (2009) Plant growth promoting rhizobacteria. Ann Rev Microbiol 63:541–556
Lucy M, Reed E, Glick BR (2004) Applications of free living plant growth promoting rhizobacteria. Antonie Van Leeuwenhoek 86:1–25
Ma W, Charles TC, Glick BR. (2004) Expression of an exogenous 1-aminocyclopropane-1-carboxylate deaminase gene in Sinorhizobium meliloti increases its ability tonodulate alfalfa. Appl Environ Microbiol;70:5891–7.
Ma Y, Prasad MNV, Rajkumar M, Freitas H (2011) Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnol Adv 29:248–258
Ma Z, Ge L, Lee ASY et al. (2008) Simultaneous analysis of different classes of phytohormones in coconut (Cocos nucifera L.) water using high-performance liquid chromatography and liquid chromatography-tandem mass spectrometry after solid-phase extraction. Anal Chim Acta 610: 274-281.
Mathur SC (1999) Future of Indian pesticides industry in next millennium. Pestic Inf 24:9–23
Martinez-Toledo MV, Salmeron V, Rodelas B, Pozo C, Gonzalez-Lopez J (1996) Studies on the effects of the herbicide simazine on microflora of four agricultural soils. Environ Toxicol Chem 15:1115–1118
Meghvansi, M.K. (2006) Isolation, Identification and Effectiveness of Rhizobial Strains and Arbuscular Mycorrhizal (AM) Fungi of Soybean Cultivars Grown in Bundi and Udaipur, Rajasthan. PhD Thesis, Maharshi Dayanand Saraswati University, Ajmer.
Mehboob I, Naveed M, Zahir ZA, Ashraf M (2012) Potential of rhizobia for sustainable production of non-legumes. In: Ashraf M, O ¨ ztu¨rk M, Ahmad M, Aksoy A (eds) Crop production for agricultural improvement. Springer, Netherlands, pp 659–704
Miller-Williams M, Loewen PC, Oresnik IJ (2006) Isolation of salt sensitive mutants of Sinorhizobium meliloti strain Rm1021. Microbiol 152:2049–2059
Mishra RPN, Singh RK, Jaiswal HK, Kumar V, Maurya S (2006) Rhizobium-mediated induction of phenolics and plant growth promotion in rice (Oryza sativa L.). Curr Microbiol 52:383–389
Mpepereki SF, Makoneses Wollum AG (1997) Physiological characterization of indigenous rhizobia nodulating Vigna unguiculata in Zimbabwean soils. Symbiosis 22:275–292
Muglia CI, Grasso DH, Aguilar OM (2007) Rhizobium tropici response to acidity involves activation of glutathione synthesis. Microbiol 153:1286–1296
Munns DN, Keyser HH, Fogle VW, Hohenberg JS, Righetti TL, Lauter DL, Zaruog MG, Clarkin KL, Whitacre KW (1979) Tolerance of soil acidity in symbiosis of mung bean with rhizobia. Agron J 71:256–260
Nandal K, Sehrawat AR, Yadav AS, Vashishat RK, Boora KS (2005) High temperature-induced changes in exo-polysaccharides, lipopolysaccharides and protein profile of heat-resistant mutants of Rhizobium sp. (Cajanus). Microbiol Res 160:367–373
Naamala J, Jaiswal SK. Dakora FD. (2016) Antibiotics Resistance in Rhizobium: Type, Process, Mechanism and Benefit for Agriculture Curr Microbiol.72:804–816
Nascimento F, Brı´gido C, Alho L, Glick BR, Oliveira S (2012) Enhanced chickpea growth promotion ability of a mesorhizobia expressing an exogenous ACC deaminase gene. Plant Soil 353:221–230
Neubauer U, Furrer G, Kayser A, Schulin R (2000) Siderophores, NTA, and citrate: potential soil amendments to enhance heavy metal mobility in phytoremediation. Int J Phytoremed 2:353–368
Nieto KF, Frankenberger WT Jr (1991) Influence of adenine, isopentyl alcohol and Azotobacter chroococcum on the vegetative growth of Zea mays. Plant Soil 135:213–221
Nonnoi F, Chinnaswamy A, de la Torre VSG, de la Pe˜na TC, Lucas MM, Pueyo JJ (2012) Metal tolerance of rhizobial strains isolated from nodules of herbaceous legumes (Medicago spp. and Trifolium spp.) growing in mercury-contaminated soils. Appl Soil Ecol 61:49–59
Oldroyd GED (2013). Signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol;11:252–63.
Ozkoc I, Deliveli MH (2001) In vitro inhibition of the mycelia growth of some root rot fungi by Rhizobium leguminosarum biovar phaseoli isolates. Turk J Biol 25:435–445
Parker JH (1972) How fertilizer moves and reacts in soil. Crops Soils 72:7–11
Patten CL, Glick BR (1996) Bacterial biosynthesis of indole-3-acetic acid. Can J Microbiol 42:207–220
Paton GI, Palmer G, Burton M, Rattray EAS, McGrath SP, Glover LA, Killham K (1997) Development of an acute and chronic ecotoxicity assay using lux-marked Rhizobium leguminosarum biovar trifolii. Lett Appl Microbiol 24:296–300
Paudyal SP, Aryal RR, Chauhan SVS, Maheshwari DK (2007) Effect of heavy metals on growth of rhizobium strains and symbiotic efficiency of two species of tropical legumes. Sci World 5:27–32
Peoples MB, Crasswell ET (1992) Biological nitrogen fixation: investments, expectations and actual contributions to agriculture. Plant Soil 141:13–39
Peix A, Rivas-Boyero AA, Mateos PF, Rodriguez-Barrueco C, Martı´nez-Molina E, Velazquez E (2001) Growth promotion of chickpea and barley by a phosphate solubilizing strain of Mesorhizobium mediterraneum under growth. Soil Biol Biochem 33:103–110
Pereira SIA, Lima AIG, Figueira EMAP (2006a) Heavy metal toxicity in Rhizobium leguminosarum biovar viciae isolated from soils subjected to different sources of heavy-metal contamination: effects on protein expression. Appl Soil Ecol 33:286–293
Pereira SIA, Lima AIG, Figueira EMAP (2006b) Screening possible mechanisms mediating cadmium resistance in Rhizobium leguminosarum bv. viciae isolated from contaminated Portuguese soils. Microbial Ecol 52:176–186
Plessner, O., Klapatch, T., and Guerinot, M.L. (1993) Siderophore utilization by Bradyrhizobium japonicum. Appl. Environ. Microbiol. 59:1688–1690.
Prabha C, Maheshwari DK, Bajpai VK (2013) Diverse role of fast growing rhizobia in growth promotion and enhancement of psoralen content in Psoralea corylifolia L. Pharmacogn Mag 9:S57–S65
Pulsawat W, Leksawasdi N, Rogers PL, Foster LJR (2003) Anions effects on biosorption of Mn(II) by extracellular polymeric substance (EPS) from Rhizobium etli. Biotechnol Lett 25:1267–1270
Rajendran G, Sing F, Desai AJ, Archana G (2008) Enhanced growth and nodulation of pigeonpea by co-inoculation of Bacillus strains with Rhizobium sp. Bioresour Technol 99:544–550
Rajkumar M, Ae N, Prasad MNV, Freitas H (2010) Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol 28:142–149.
Reigh, G. and O’Connell, M. (1993) Siderophore iron transport correlates with the presence of specific ironregulated proteins in the outer membrane of Rhizobium meliloti. J. Bacteriol. 175:94–102.
Reitz M, Rudolph K, Schroder I, Hoffmann-Hergarten S, Hallmann J, Sikora RA (2000) Lipopolysaccharides of Rhizobium etli strain G12 act in potato roots as an inducing agent of systemic resistance to infection by the cyst nematode Globodera pallida. Appl Environ Microbiol 66:3515–3518
Remans R, Ramaekers L, Schelkens S, Hernandez G, Garcia A, Reyes JL, Mendez N, Toscano V, Mulling M, Galvez L, Vanderleyden J (2008) Effect of Rhizobium-Azospirillum coinoculation on nitrogen fixation and yield of two contrasting Phaseolus vulgaris L. genotypes cultivated across different environments in Cuba. Plant Soil 312:25–37
Richardson AE, Henderson AP, James GS, Simpson RJ (1988) Consequences of soil acidity and the effect of lime on the nodulation of Trifolium subterraneum L. growing in an acid soil. Soil Biol Biochem 20:439–445
Saxena D, Amin M, Khanna S (1996) Modulation of protein profiles in Rhizobium sp. under salt stress. Can J Microbiol 42:617–620
Schippers, B., Bakker, A.W., Van peer, R. (1990) Beneficial and deleterious pseudomonads on rhizosphere interactions.Plant Soil, 129, 75-83.
Senthilkumar M, Madhaiyan M, Sundaram SP, Kannaiyan S (2009) Intercellular colonization and growth promoting effects of Methylobacterium sp. with plant-growth regulators on rice (Oryza sativa L. CvCO-43). Microbiol Res 164:92–104
Sharma P, Padh H, Shrivastava N (2013) Hairy root cultures: a suitable biological system for studying secondary metabolic pathways in plants. Eng Life Sci 13:62–75
Singh, Y., Ramteke, P.W. and Shukla, P.K., (2013) Characterization of Rhizobium isolates of pigeon pea rhizosphere from Allahabad soils and their potential pgpr characteristics. International Journal of Research in Pure and Applied Microbiology, 3(1), 4-7.
Spaepen S, Vanderleyden J (2011) Auxin and plant-microbe interactions. Cold Spring Harb Perspect Biol 3:a001438
Stan V, Gament E, Cornea CP, Voaides C, Dusa M, Plopeanu G (2011) Effects of heavy metal from polluted soils on the Rhizobium diversity. Not Bot Hort Agrobot Cluj 39:88–95
Subbarao GV, Johansen C, Jana MK, Kumar Rao JVDK (1990) Effects of the sodium/calcium ratio in modifying salinity responses in pigeonpea (Cajanus cajan). Plant Physiol 136:439–443
Subbarao GV, Sahrawat KL, Nakahara K, Ishikawa T, Kishii M, Rao IM, Hash CT, George TS, Srinivasa Rao P, Nardi P, Bonnett D, Berry W, Suenaga K, Lata JC (2012) Bio-logical nitrification inhibition—a novel strategy to regulate nitrification in agricultural systems. Adv Agron 114:249–302
Sutherland IW (2001) Exo-polysaccharides in biofilms, flocs and related structure. Water Sci Technol 43:77–86
Tao G, Tian S, Cai M, Xie G (2008) Phosphate solubilizing and mineralizing abilities of bacteria isolated from soils. Pedosphere 18:515–523
Tchebotar VK, Kang UG, Asis CA Jr, Akao S (1998) The use of GUS-reporter gene to study the effect of Azospirillum-Rhizobium co-inoculation on nodulation of white clover. Biol Fertil Soils 27:349–352
Thami-Alami I, Elboutahiri N, Udupa SM (2010) Variability in natural populations of Sinorhizobium meliloti in Morocco. In: Porqueddu C, Rı´os S (eds) The contributions of grasslands to the conservation of Mediterranean biodiversity. Zaragoza, CIHEAM/ CIBIO/FAO/SEEP, pp 265–269
Tokala RK, Strap JL, Jung CM, Crawford DF, Salove MH, Deobald LA, Bailey JF, Morra MJ (2002) Novel plant-microbe rhizosphere interaction involving Streptomyces lydicus Wyec 108 and the pea plant (Pisum sativum). Appl Environ Microbiol 68:2161–2171
Uren NC (2007) .Types, amounts, and possible functions of compounds released into the rhizosphere by soil-grown plants. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere: biochemistry and organic substances at the soil–plant interface. CRC Press, Boca Rato´n, pp 1–22
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
Verma JP, Yadav J, Tiwari KN, Jaiswal DK (2014) Evaluation of plant growth promoting activities of microbial strains and their effect on growth and yield of chickpea (Cicer arietinum L.) in India. Soil Biol Biochem 70:33–37
Vessey KJ (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586
Villacieros M, Power B, Sanchez-Contreras M, Lloret J, Oruezabal RI, Martin M, Fernandez-Pinas F, Bonilla I, Whelan C, Dowling DN, Rivilla R (2003) Colonization behaviour of Pseudomonas fluorescens and Sinorhizobium meliloti in the alfalfa (Medicago sativa) rhizosphere. Plant Soil 251:47–54
Walton DC, Li Y (1995) Abscisic acid biosynthesis and metabolism. Plant hormones: physiology, biochemistry and molecular biology. Kluwer, Dordrecht, pp 140–157
Watkin ELJ, O’Hara GW, Glenn AR (1997) Calcium and acid stress interact to affect the growth of Rhizobium leguminosarum bv. trifolii. Soil Biol Biochem 29:1427–1432
Watkin ELJ, O’Hara GW, Glenn AR (2003) Physiological responses to acid stress of an acid-soil tolerant and an acid-soil sensitive strain of Rhizobium leguminosarum biovar trifolii. Soil Biol Biochem 35:621–624
Whipps JM (2001). Microbial interactions and biocontrol in the rhizosphere. J. Experiment. Bot., 52: 487-511.
Wilson PW, Burris RH (1947). The mechanism of biological nitrogen fixation. Bacteriol Rev 11(1):41–73
Wright GD (2007) The antibiotic resistome: the nexus of chemical and genetic diversity. Nat Rev Microbiol 5:175–186
Xavier G, Martins L, Neves M, Rumjanek N (1998) Edaphic factors as determinants for the distribution of intrinsic antibiotic resistance in a cowpea rhizobia population. Biol Fertil Soils 27:386–392.
Yelton MM, Yang SS, Edie SA, Lim ST (1983) Characterization of an effective salt-tolerant fast-growing strain of Rhizobium japonicum. J Gen Microbiol 129:1537–1547
Zahran HH (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an aird climate. Microbiol Mol Biol Rev 63(4):968–989
Zafar-ul-Hye M, Ahmad M, Shahzad SM (2013) Synergistic effect of rhizobia and plant growth promoting rhizobacteria on the growth and nodulation of lentil seedlings under axenic conditions. Soil Environ 32:79–86
Zaidi A, Khan MS, Ahemad M and Oves M, (2009) Plant growth promotion by phosphate solubilizing bacteria. Acta Microbiol Immunol Hung 56:263–284.
Zhan HJ, Lee CC, Leigh JA (1991) Induction of the second exopolysaccharide (EPS) in Rhizobium meliloti SU47 by low phosphate concentrations. J Bacteriol 173:7391–7394
Zhang XP, Karsisto M, Harper R, LindstroE`m K (1991) Diversity of Rhizobium bacteria isolated from the root nodules of leguminous trees. Int J Syst Evol Bacteriol 41:104–113
--0--
Downloads
Published
Issue
Section
License
ABC Research Alert is an Open Access journal. Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal the right of first publication with the work simultaneously licensed under a CC BY-NC 4.0 International License that allows others to share the work with an acknowledgment of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of their work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgment of its initial publication in this journal. We require authors to inform us of any instances of re-publication.
