Skip to main content

A Deeper Insight into the Symbiotic Mechanism of Rhizobium spp. from the Perspective of Secondary Metabolism

  • Chapter
  • First Online:
Secondary Metabolites of Plant Growth Promoting Rhizomicroorganisms

Abstract

Rhizobia are group of organism, known globally for their nitrogen-fixing ability. In addition to nitrogen fixation, they significantly contribute to plant growth promotion and disease control. Rhizobial aptness for plant growth promotion and antagonism against a wide range of pathogens is due to its ability to produce a wide range of secondary metabolites such as HCN, siderophore, antibiotics, rhizobitoxin, lytic enzymes, IAA, phosphate solubilization and induced systemic resistance. Rhizobial inoculants, ascribed with multiple roles of nitrogen fixation, growth promotion and disease suppression, have strengthened crop productivity. This compilation urges the need to recognize and exploit the potential multifaceted secondary metabolites of rhizobia for biological control and growth promotion.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Al-Ani RA, Adhab MA, Mahdi MH, Abood HM (2012) Rhizobium japonicum as a biocontrol agent of soybean root rot disease caused by Fusarium solani and Macrophomina phaseolina. Plant Prot Sci 48:149–155

    Google Scholar 

  • Albareda M, Rodríguez-Navarro DN, Camacho M, Temprano FJ (2008) Alternatives to peat as a carrier for rhizobia inoculants: solid and liquid formulations. Soil Biol Biochem 40:2771–2779. https://doi.org/10.1016/j.soilbio.2008.07.0210067-y

    Article  CAS  Google Scholar 

  • Amadou C, Pascal G, Mangenot S, Glew M, Bontemps C, Capela D, Carrère S, Cruveiller S, Dossat C, Lajus A, Marchetti M (2008) Genome sequence of the β-rhizobium Cupriavidus taiwanensis and comparative genomics of rhizobia. Genome Res 18(9):1472–1483

    CAS  PubMed  PubMed Central  Google Scholar 

  • Andrews SC, Robinson AK, Rodriguez-Quinones F (2003) Bacterial iron homeostasis. FEMS Microbiol Rev 27(2–3):215–237

    CAS  PubMed  Google Scholar 

  • Antoun H, Bordeleau LM, Gagnon C (1978) Antagonisme entre Rhizobium meliloti at Fusarium oxysporum en relation avec lefficacite symbiotique. Can J Plant Sci 58:75–78

    Google Scholar 

  • Antoun H, Beauchamp CJ, Goussard N, Chabot R, Lalande R (1998) Potential of Rhizobium and Bradyrhizobium species as plant growth promoting rhizobacteria on non-legumes: effect on radishes (Raphanus Sativus L.). Plant Soil 204:57–67

    CAS  Google Scholar 

  • Appleby CA (1984) Leghemoglobin and Rhizobium respiration. Annu Rev Plant Physiol 35(1):443–478

    CAS  Google Scholar 

  • Arfaoui A, Sifi B, El Hassni M, El Hadrami I, Boudabbous A, Chérif M (2005) Biochemical analysis of chickpea protection against Fusarium wilt afforded by two Rhizobium isolates. Plant Pathol J 4:35–42

    Google Scholar 

  • Arfaoui A, Sifi B, Boudabous A, El Hadrami I, Cherif M (2006) Identification of Rhizobium isolates possessing antagonistic activity against Fusarium oxysporum f.sp ciceris, the causal agent of Fusarium wilt of chickpea. J Plant Pathol 88:67–75

    CAS  Google Scholar 

  • Arora N, Kang S, Maheshwari D (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

    Google Scholar 

  • Barber MS, Giesecke U, Reichert A, Minas W (2004) Industrial enzymatic production of cephalosporin-based b-lactams. Adv Biochem Engin/Biotechnol 88:179–216

    CAS  Google Scholar 

  • Bardin SD, Huang H-C, Pinto J, Amundsen EJ, Erickson RS (2004) Biological control of Pythium damping-off of pea and sugar beet by Rhizobium leguminosarum bv. viceae. Can J Botany 82:291–296

    Google Scholar 

  • Bashan Y (1986) Alginate beads as synthetic inoculant carriers for slow release of bacteria that affect plant growth. Appl Environ Microbiol 51(5):1089–1098

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bashan Y (1998) Inoculants of plant growth-promoting bacteria for use in agriculture. Biotech adv 16(4):729–770

    CAS  Google Scholar 

  • Beauchamp CJ, Dion P, Kloepper JW, Antoun H (1991) Physiological characterization of opine-utilizing rhizobacteria for traits related to plant growth-promoting activity. Plant Soil 132:273–279. https://doi.org/10.1007/bf00010408

    Article  CAS  Google Scholar 

  • Beck DP (1991) Suitability of charcoal-amended mineral soil as carrier for Rhizobium inoculants. Soil Biol Biochem 23:41–44

    Google Scholar 

  • Beijerinck MW (1888) Cultur des Bacillus radicicola aus den Kno¨llchen. Bot Ztg 46:740–750

    Google Scholar 

  • Benson DR, Clawson ML (2000) Evolution of the actinorhizal plant nitrogen-fixing symbiosis. In: Triplett E (ed) Prokaryotic nitrogen fixation: a model system for the analysis of a biological process. Horizon Scientific Press, Wymondham, pp 207–224

    Google Scholar 

  • Berdy J (2005) Bioactive microbial metabolites a personal view. J Antibiot 58:1–26

    CAS  PubMed  Google Scholar 

  • Bergman K, Gulash-Hofee M, Hovestadt RE, Larosiliere RC, Ronco PG, Su L (1988) Physiology of behavioral mutants of Rhizobium meliloti: evidence for a dual chemotaxis pathway. J Bacteriol 170:3249–3254

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bibb MJ (2005) Regulation of secondary metabolism in streptomycetes. Curr Opin Microbiol 8:208–215

    CAS  PubMed  Google Scholar 

  • Biswas JC, Ladha JK, Dazzo FB (2000) Rhizobia inoculation improves nutrient uptake and growth of lowland rice. Soil Sci Soc Am J 64:1644–1650. https://doi.org/10.2136/sssaj2000.6451644x

    Article  CAS  Google Scholar 

  • Brockwell J, Bottomley PJ (1995) Recent advances in inoculant technology and prospects for the future. Soil Biol Biochem 27:683–697. https://doi.org/10.1016/0038-0717(95)98649-9

    Article  CAS  Google Scholar 

  • Brockwell J, Gault RR, Chase DL, Hely FW, Zorin M, Corbin EJ (1980) An appraisal of practical alternatives to legume seed inoculation: field experiments on seed bed inoculation with solid and liquid inoculants. Aust J Agri Res 31(1):47–60

    Google Scholar 

  • Buonassisi AJ, Copeman RJ, Pepin HS, Eaton GW (1986) Effect of Rhizobium spp. on Fusarium solani f. sp. phaseoli. Can J Plant Pathol 8:140–146

    Google Scholar 

  • Caetano-Anolles G, Crist-Estes DK, Bauer WD (1988) Chemotaxis of Rhizobium meliloti to the plant flavone luteolin requires functional nodulation genes. J Bacterial 170:3164–3169

    CAS  Google Scholar 

  • Callaham DA, Torrey JG (1981) The structural basis for infection of root hairs of Trifolium repens by Rhizobium. Can J Bot 59:1647–1664

    Google Scholar 

  • Carson KC, Holliday S, Glenn AR, Dilworth MJ (1992) Siderophore and organic acid production in root nodule bacteria. Arch Microbiol 157:264–271

    CAS  PubMed  Google Scholar 

  • Carson KC, Meyer J-M, Dilworth MJ (2000) Hydroxamate siderophores of root nodule bacteria. Soil Biol Biochem 32:11–21. https://doi.org/10.1016/S0038-0717(99)00107-8

    Article  CAS  Google Scholar 

  • Chakraborty U, Purkayastha RP (1984) Role of rhizobitoxine in protecting soybean roots from Macrophomina phaseolina. Can J Microbiol 30:285–289

    CAS  PubMed  Google Scholar 

  • Chamber MA (1983) Influence of several methods for rhizobial inoculation on nodulation and yield of soybeans. Plant Soi1 74:203–209

    Google Scholar 

  • Chandra S, Choure K, Dubey RC, Maheshwari DK (2007) Rhizosphere competent Mesorhizobium loti MP6 induces root hair curling, inhibits Sclerotinia sclerotiorum and enhances growth of Indian mustard (Brassica campestris). Braz J Microbiol 38:124–130

    Google Scholar 

  • Chao WL, Alexander M (1984) Mineral soils as carriers for Rhizobium inoculants. Appl Environ Microbiol 47:94–97

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chatterjee A, Cui Y, Liu Y, Dumenyo CK, Chatterjee AK (1995) Inactivation of rsmA leads to overproduction of extracellular pectinases, cellulases, and proteases in Erwinia carotovora subsp. carotovora in the absence of the starvation/cell density-sensing signal, N-(3-oxohexanoyl)-L-homoserine lactone. Appl Environ Microbiol 61:1959–1967

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen WX, Yan GH, Li JL (1988) Numerical taxonomic study of fast-growing soybean rhizobia and a proposal that Rhizobium fredii be assigned to Sinorhizobium gen. nov. Int J Syst Bacteriol 38(4):392–397

    Google Scholar 

  • Chernin L, Ismailov Z, Haran S, Chet I (1955) Chitinolytic Enterobacter agglomerans antagonistic to fungal plant pathogens. Appl Environ Microbiol 61(5):1720–1726

    Google Scholar 

  • Corbett JR (1974) Pesticide design. In: The biochemical mode of action of pesticides. Academic, London, pp 44–86

    Google Scholar 

  • Crowley DE, Gries D (1994) Modeling of iron availability in the plant rhizosphere. In: Biochemistry of metal micronutrients in the rhizosphere. Lewis Publishers, Boca Raton, pp 199–224

    Google Scholar 

  • Das K, Prasanna R, Saxena AK (2017) Rhizobia: a potential biocontrol agent for soilborne fungal pathogens. Folia Microbiol 62(5):425–435

    CAS  Google Scholar 

  • Date R, Roughley R (1977) Preparation of legume seed inoculants a treatise on dinitrogen fixation section IV agronomy and ecology. Wiley, New York, pp 243–275

    Google Scholar 

  • Demain AL (1998) Induction of microbial secondary metabolism. Int Microbiol 1:259–264

    CAS  PubMed  Google Scholar 

  • Demain AL, Fang A (2000) The natural functions of secondary metabolites. In: Fietcher AI (ed) Advances in biochemical engineering/biotechnology: history of modern biotechnology, vol 2. Springer, Berlin, p 39

    Google Scholar 

  • Demain AL, Sanchez S (2009) Microbial drug discovery: 80 years of progress. J Antibiot 62:5–16

    CAS  PubMed  Google Scholar 

  • Dénarié J, Cullimore J (1993) Lipo-oligosaccharide nodulation factors: a new class of signalling molecules mediating recognition and morphogenesis. Cell 74:951–954

    PubMed  Google Scholar 

  • Denison RF, Kiers ET (2004) Why are most rhizobia beneficial to their plant hosts, rather than parasitic? Microbes Infect 6(13):1235–1239

    CAS  PubMed  Google Scholar 

  • Deshwal VK, Pandey P, Kang SC, Maheshwari DK (2003) Rhizobia as a biological control agent against soil borne plant pathogenic fungi. Ind J Exp Biol 41:1160–1164

    CAS  Google Scholar 

  • Diby P, Anandaraj M, Kumar A, Sarma YR (2005) Antagonistic mechanisms of fluorescent pseudomonads against Phytophthora capsici in black pepper (Piper nigrum L.). J Spices Aromatic Crops 14(2):122–129

    Google Scholar 

  • Dihazi A, Jaiti F, Zouine J, Hassni ME, Hadrami IE (2003) Effect of salicylic acid on phenolic compounds related to date palm resistance to Fusarium oxysporum f. sp. albedinis. Phytopathol Mediterr 42:9–16

    CAS  Google Scholar 

  • Dixon ROD, Wheeler CT (1986) Nitrogen fixation in plants. Blackie and Son, Glasgow. https://doi.org/10.1111/j.1439-0434.1997.tb00355.x

    Book  Google Scholar 

  • Dubey RC, Maheshwari DK (2011) Role of PGPR in integrated nutrient management of oil seed crops. In: Bacteria in agrobiology: plant nutrient management. Springer, Berlin/Heidelberg, pp 1–15

    Google Scholar 

  • Dutta S, Mishra A, Kumar BD (2008) Induction of systemic resistance against fusarial wilt in pigeon pea through interaction of plant growth promoting rhizobacteria and rhizobia. Soil Biol Biochem 40:452–461

    CAS  Google Scholar 

  • Ehteshamul-Haque S, Ghaffar A (1993) Use of rhizobia in the control of root rot diseases of sunflower, okra, soybean and mungbean. J Phytopathol 138:157–163

    Google Scholar 

  • Essalmani H, Lahlou H (2002) In vitro antagonistic activity of some microorganisms towards Fusarium oxysporum f. sp. lentis (french). Crypto Mycol 23:221–234

    Google Scholar 

  • Estevez de Jensen C, Percich JA, Graham PH (2002) Integrated management strategies of bean root rot with Bacillus subtilis and Rhizobium in Minnesota. Field Crops Res 74:107–115. https://doi.org/10.1016/S0378-4290(01)00200-3

    Article  Google Scholar 

  • Fisher RF, Long SR (1992) Rhizobium-plmt signal exchange. Nature 357:655–660

    CAS  PubMed  Google Scholar 

  • Fouilleux G, Revellin C, Hartmann A, Catroux G (1996) Increase of Bradyrhizobium japonicum numbers in soils and enhanced nodulation of soybean (Glycine max (L) merr.) using granular inoculants amended with nutrients. FEMS Microbiol Ecol 20(3):173–183

    CAS  Google Scholar 

  • Frank B (1889) Ueber die Pilzsymbiose der Leguminosen. Ber Deut Bot Ges 7:332–346

    Google Scholar 

  • Gage DJ (2004) Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol Mol Biol Rev 68(2):280–300

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ganesan S, Kuppusamy RG, Sekar R (2007) Integrated management of stem rot disease (Sclerotium rolfsii) of groundnut (Arachis hypogaea L.) using Rhizobium and Trichoderma harzianum (ITCC-4572). Turk J Agric For 31:103–108

    Google Scholar 

  • Gao X, Lu X, Wu M, Zang H, Pan R, Tian J, Li S, Liao H (2012) Coinoculation with rhizobia and AMF inhibited soybean red crown rot: from field study to plant defense-related gene expression analysis. PLoS One 7:e33977

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gehring PJ, Mohan RJ, Watamare PG (1993) Solvents, fumigants and related compounds. In: Hayes WJ, Laws ER (eds) Handbook of pesticide toxiocology, vol 2. Academic, San Diego, pp 646–649

    Google Scholar 

  • Gonzalez JB, Fernandez FJ, Tomasini A (2003) Microbial secondary metabolites production and strain improvement. Indian J Biotechnol 2:322–333

    Google Scholar 

  • González V, Santamaría RI, Bustos P, Hernández-González I, Medrano-Soto A, Moreno-Hagelsieb G, Dávila G (2006) The partitioned Rhizobium etli genome: genetic and metabolic redundancy in seven interacting replicons. Proc Natl Acad Sci USA 103(10):3834–3839

    PubMed  Google Scholar 

  • Gopalakrishnan S, Sathya A, Vijayabharathi R, Varshney RK, Gowda CLL, Krishnamurthy L (2015) Plant growth promoting rhizobia: challenges and opportunities. Biotech 5:355–377. https://doi.org/10.1007/s13205-014-0241-x

    Article  Google Scholar 

  • Graham-Weis L, Bennet ML, Paau AS (1987) Production of bacterial inoculants by direct fermentation on nutrient-supplemented vermiculite. Appl Environ Microbiol 53:2138–2140

    Google Scholar 

  • Guan C, Pawlowski K, Bisseling T (1995) Nodulation in legumes and Actinorhizal plants. In: Tikhonovich IA, Provorov NA, Romanov VI, Newton WE (eds) Nitrogen fixation: fundamentals and applications. Current plant science and biotechnology in agriculture. Springer, Dordrecht, pp 49–59

    Google Scholar 

  • Guerinot ML (1994) Microbial iron transport. Annu Rev Microbiol 48(1):743–772

    CAS  PubMed  Google Scholar 

  • Guerinot ML, Meidl EJ, Plessner O (1990) Citrate as a siderophore in Bradyrhizobium japonicum. J Bacteriol 172:3298–3303

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gupta CP, Kumar B, Dubey RC, Maheshwari DK (2006) Chitinase mediated destructive antagonistic potential of Pseudomonas aeruginosa GRC1 against Sclerotinia sclerotiorum causing charcoal rot of peanut. BioControl 51:821–835

    CAS  Google Scholar 

  • Gyaneshwar P, Kumar GN, Parekh LJ, Poole PS (2002) Role of soil microorganisms in improving P nutrition of plants. Plant Soil 245:83–93

    CAS  Google Scholar 

  • Hafeez FY, Naeem FI, Naeem R, Zaidi AH, Malik KA (2005) Symbiotic effectiveness and bacteriocin production by Rhizobium leguminosarum bv. viciae isolated from agriculture soils in Faisalabad. Environ Exp Bot 54:142–147. https://doi.org/10.1016/j.envexpbot.2004.06.008

    Article  CAS  Google Scholar 

  • Handberg K, Stougaard JS (1992) Lotus japonicus, an autogamous, diploid legume species for classical and molecular genetics. Plant J 2:487–496

    Google Scholar 

  • Hegde SV, Brahmaprakash GP (1992) A dry granular inoculant of Rhizobium for soil application. Plant Soil 144(2):309–311

    Google Scholar 

  • Hemissi I, Mabrouk Y, Abdi N, Bouraoui M, Saidi M, Sifi B (2011) Effects of some Rhizobium strains on chickpea growth and biological control of Rhizoctonia solani. Afr J Microbiol Res 5:4080–4090

    CAS  Google Scholar 

  • Hirsch PR (1979) Plasmid-determined bacteriocin production by Rhizobium leguminosarum. Microbiology 113:219–228. https://doi.org/10.1099/00221287-113-2-219

    Article  CAS  Google Scholar 

  • Hirsch PR, Van Montagu M, Johnston AWB, Brewin NJ, Schell J (1980) Physical identification of bacteriocinogenic, nodulation and other plasmids in strains of Rhizobium leguminosarum. Microbiology 120:403–412. https://doi.org/10.1099/00221287-120-2-403

    Article  Google Scholar 

  • Howieson JG, Brockwell J (2005) Nomenclature of legume root nodule bacteria in 2005 and implications for collection of strains from the field. In: Brockwell J (ed) 14th Australian nitrogen fixation conference. The Australian Society for Nitrogen Fixation, Katoomba, pp 17–23

    Google Scholar 

  • Huang HC, Erickson RS (2007) Effect of seed treatment with Rhizobium leguminosarum on Pythium damping-off, seedling height, root nodulation, root biomass, shoot biomass, and seed yield of pea and lentil. J Phytopathol 155:31–37. https://doi.org/10.1111/j.1439-0434.2006.01189.x

    Article  Google Scholar 

  • Jarvis BDW, van Berkum P, Chen WX, Nour SM, Fernandez MP, Cleyet-Marel JC, Gillis M (1997) Transfer of Rhizobium loti, Rhizobium huakuii, Rhizobium ciceri, Rhizobium mediterraneum, and Rhizobium tianshanense to Mesorhizobium gen. nov. Int J Syst Evo microbiol 47(3):895–898

    Google Scholar 

  • Jayasinghearachchi HS, Seneviratne G (2004) A bradyrhizobial-Penicillium spp. biofilm with nitrogenase activity improves N2 fixing symbiosis of soybean. Biol Fert Soils 40:432–434. https://doi.org/10.1007/s00374-004-0796-5

    Article  CAS  Google Scholar 

  • Jordan DC (1982) Transfer of Rhizobium japonicum Buchanan 1980 to Bradyrhizobium gen. nov., a genus of slow-growing, root nodule bacteria from leguminous plants. Int J Syst Bacteriol 32(1):136–139

    Google Scholar 

  • Kacem M, Kazouz F, Merabet C, Rezki M, de Lajudie P, Bekki A (2009) Antimicrobial activity of Rhizobium sp. strains against Pseudomonas savastanoi, the agent responsible for the olive knot disease in Algeria. Grasas Aceites 60(2):139–146

    Google Scholar 

  • Kannenberg EL, Brewin NJ (1989) Expression of a cell surface antigen from Rhizobium leguminosarum 3841 is regulated by oxygen and pH. J Bacteriol 171(9):4543–4548

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kawaguchi T, Azuma M, Horinouchi S, Beppu T (1988) Effect of B-factor and its analogues on rifamycin biosynthesis in Nocardia sp. J Antibiot 41:360–365

    CAS  PubMed  Google Scholar 

  • Khavazi K, Rejali F, Seguin P, Miransari M (2007) Effects of carrier, sterilisation method, and incubation on survival of Bradyrhizobium japonicum in soybean (Glycine max L.) inoculants. Enzym Microb Technol 41:780–784

    CAS  Google Scholar 

  • Knowles CJ, Bunch AW (1986) Microbial cyanide metabolism. Adv Microbiol Physiol 27:73–111

    CAS  Google Scholar 

  • Kostov O, Lynch JM (1998) Composted sawdust as a carrier for Bradyrhizobium, Rhizobium and Azospirillum in crop inoculation. World J Microbiol Biotechnol 14(3):389–397

    Google Scholar 

  • Kumar H, Bajpai VK, Dubey RC, Maheshwari DK, Kang SC (2010) Wilt disease management and enhancement of growth and yield of Cajanus cajan (L) var. Manak by bacterial combinations amended with chemical fertilizer. Crop Prot 29:591–598. https://doi.org/10.1016/j.cropro.2010.01.002

    Article  Google Scholar 

  • Kumar H, Dubey RC, Maheshwari DK (2011) Effect of plant growth promoting rhizobia on seed germination, growth promotion and suppression of Fusarium wilt of fenugreek (Trigonella foenumgraecum L.). Crop Prot 30:1396–1403. https://doi.org/10.1016/j.cropro.2011.05.001

    Article  Google Scholar 

  • Kumari S, Khanna V (2014) Effect of antagonistic Rhizobacteria coinoculated with Mesorhizobium ciceris on control of fusarium wilt in chickpea (Cicer arietinum L.). Afr J Microbiol Res 8:1255–1265

    Google Scholar 

  • Kurrey D, Lakpale R, Rajput RS (2016) Growth behavior, nodulation and Rhizobium population, as affected by combined application of herbicide and insecticide in soybean (Glycine max L.). J Pure Appl Microbio 10(4):2931–2936

    CAS  Google Scholar 

  • Laranjo M, Alexandre A, Oliveira S (2014) Legume growth-promoting rhizobia: an overview on the Mesorhizobium genus. Microbiol Res 169(1):2–17

    PubMed  Google Scholar 

  • Libbenga KR, Harkes PAA (1973) Initial proliferation of cortical cells in the formation of root nodules in Pisum sativum L. Planta 114:17–28

    CAS  PubMed  Google Scholar 

  • Ligon JM, Hill DS, Hammer PE, Torkewitz NR, Hofmann D, Kempf HJ, Pée KHV (2000) Natural products with antifungal activity from pseudomonas biocontrol bacteria. Pest Manag Sci 56:688–695

    CAS  Google Scholar 

  • Lloyd CW, Pearce KJ, Rawlins DJ, Ridge RW, Shaw PJ (1987) Endoplasmic microtubules connect the advancing nucleus to the tip of legume root hairs, but F-actin is involved in basipetal migration. CellMot Cytoskel 8:27–36

    Google Scholar 

  • Lodwig EM, Poole PS (2003) Metabolism of Rhizobium bacteroids. Crit Rev Plant Sci 22(1):37–38

    CAS  Google Scholar 

  • MacLean AM, Finan TM, Sadowsky MJ (2007) Genomes of the symbiotic nitrogen-fixing bacteria of legumes. Plant Physiol 144(2):615–622

    CAS  PubMed  PubMed Central  Google Scholar 

  • Makoi JHJR, Bambara S, Ndakidemi PA (2010) Rhizosphere phosphatase enzyme activities and secondary metabolites in plants as affected by the supply of Rhizobium, lime and molybdenum in Phaseolus vulgaris L. Aust J Crop Sci 4(8):590–597

    CAS  Google Scholar 

  • Malajczuk N, Pearce M, Litchfield RT (1984) Interactions between Phytophthora cinnamomi and Rhizobium isolates. Trans Br Mycol Soc 82:491–500. https://doi.org/10.1016/S00071536(84)80014-5

    Article  Google Scholar 

  • Martínez-Viveros O, Jorquera MA, Crowley DE, Gajardo G, Mora ML (2010) Mechanisms and practical considerations involved in plant growth promotion by rhizobacteria. J Soil Sci Plant Nutr 10:293–319

    Google Scholar 

  • Matzanke BF (1991) Structures, coordination chemistry and functions of microbial iron chelates. In: Winkelmann G (ed) Handbook of microbial iron chelates. CRC Press, Boca Raton, pp 15–64

    Google Scholar 

  • Mavrodi DV, Bonsall RF, Delaney SM, Soule MJ, Phillips G, Thomashow LS (2001) Functional analysis of genes for biosynthesis of Pyocyanin and phenazine-1-Carboxamide from Pseudomonas aeruginosa PAO1. J Bacteriol 183:6454–6465. https://doi.org/10.1128/jb.183.21.6454-6465.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mazen MM, El-Batanony NH, Abd El-Monium MM, Massoud ON (2008) Cultural filtrate of Rhizobium spp. and arbuscular mycorrhiza are potential biological control agents against root rot fungal diseases of Faba bean. Global J Biotechnol Biochem 3(1):32–41

    Google Scholar 

  • Mehta S, Nautiyal SC (2001) An efficient method for qualitative screening of phosphate solubilizing bacteria. Curr Microbiol 43:51–56

    CAS  PubMed  Google Scholar 

  • Mishra RP, 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

    CAS  PubMed  Google Scholar 

  • Modi M, Shah KS, Modi VV (1985) Isolation and characterisation of catechol-like siderophore from cowpea Rhizobium RA-1. Arch Microbiol 141:156–158. https://doi.org/10.1007/bf00423277

    Article  CAS  Google Scholar 

  • Mourad K, Fadhila K, Chahinez M, Meriem R, Philippe DL, Abdelkader B (2009) Antimicrobial activities of Rhizobium sp. strains against Pseudomonas savastanoi, the agent responsible for the olive knot disease in Algeria. Grasas Aceites 60(2):139–146

    Google Scholar 

  • Mylona P, Pawlowski K, Bisseling T (1995) Symbiotic nitrogen fixation. Plant Cell 7:869–885

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nadia H, Massoud O, Mazen M, El-Monium MA (2007) The inhibitory effects of cultural filtrates of some wild Rhizobium spp. on some faba bean root rot pathogens and their antimicrobial synergetic effect when combined with Arbuscular mycorrhiza (AM). World J Agric Sci 3:721–730

    Google Scholar 

  • Nap JP, Bisseling T (1990) Nodulin function and nodulin gene regulation in root nodule development. In: Gresshoff PM (ed) The molecular biology of symbiotic nitrogen fixation. CRC Press, Boca Raton, pp 181–229. ISBN 0-8493-6188-5

    Google Scholar 

  • Nautiyal CS (1997) Rhizosphere competence of Pseudomonas sp. NBRI9926 and Rhizobium sp. NBRI9513 involved in the suppression of chickpea (Cicer arietinum L.) pathogenic fungi. FEMS Microbiol Ecol 23:145–158. https://doi.org/10.1111/j.1574-6941.1997.tb00398.x

    Article  CAS  Google Scholar 

  • Newcomb W (1981a) Nodule morphogenesis and differentiation [Rhizobium]. Int Rev Cytol Suppl 13:247–298

    Google Scholar 

  • Newcomb W (1981b) Nodule morphogenesis. In Bourne GH, Danielli JF (eds) Int Rev Cytology, Supplement 13. Academic, New York pp 246–298

    Google Scholar 

  • Nobbe F, Hiltner L (1896) Inoculation of the soil for cultivating leguminous plants. US patent 570:813

    Google Scholar 

  • O’Brien J, Wright GD (2011) An ecological perspective of microbial secondary metabolism. Curr Opin Biotechnol 22(4):552–558

    PubMed  Google Scholar 

  • O’Gara F, Shanmugam KT (1976) Regulation of nitrogen fixation by Rhizobia. Export of fixed N2 as NH4 +. Biochim Biophys Acta 437(2):313–321

    PubMed  Google Scholar 

  • Omar SA, Abd-Alla MH (1998) Biocontrol of fungal root rot diseases of crop plants by the use of rhizobia and bradyrhizobia. Folia Microbiol 43:431–437. https://doi.org/10.1007/bf02818587

    Article  CAS  Google Scholar 

  • Pandey P, Maheshwari DK (2007) Two-species microbial consortium for growth promotion of Cajanus cajan. Curr Sci 92:1137–1142

    CAS  Google Scholar 

  • Patel HN, Chakraborty RN, Desai SB (1988) Isolation and partial characterization of phenolate siderophore from Rhizobium leguminosarum IARI 102. FEMS Microbiol Let 56(2):131–134

    CAS  Google Scholar 

  • Pawlowski K, Bisseling T (1997) Legume and actinorhizal root nodule formation. In: Plant roots-from cells to systems. Springer, Dordrecht, pp 137–142

    Google Scholar 

  • Perret X, Staehelin C, Broughton WJ (2000) Molecular basis of symbiotic promiscuity. Microbiol Mol Biol Rev 64:180–201

    CAS  PubMed  PubMed Central  Google Scholar 

  • Persmark M, Pittman P, Buyer JS, Schwyn B, Gill PR, Neilands JB (1993) J Am Chem Soc 115:3950–3956

    CAS  Google Scholar 

  • Phillips DA, Kapulnik Y (1995) Plant isoflavonoids, pathogens and symbionts. Trends Microbiol 3(2):58–66

    CAS  PubMed  Google Scholar 

  • Postgate JR (1982) The fundamentals of nitrogen fixation. Cambridge University Press, Cambridge/New York

    Google Scholar 

  • Prasanna R, Kumar A, Babu S, Chawla G, Chaudhary V, Singh S, Gupta V, Nain L, Saxena AK (2013) Deciphering the biochemical spectrum of novel cyanobacterium-based biofilms for use as inoculants. Biol Agric Hortic 29:145–158. https://doi.org/10.1080/01448765.2013.790303

    Article  Google Scholar 

  • Raaijmakers JM, Vlami M, de Souza JT (2002) Antibiotic production by bacterial biocontrol agents. Anton van Leeuwen 81:537–547. https://doi.org/10.1023/a:1020501420831

    Article  CAS  Google Scholar 

  • Ramos T, Bellaj ME, Idrissi-Tourane AE, Daayf F, Hadrami IE (1997) Les Phénolamides des Rachis de Palmes, Composants de la Réaction de Défense du Palmier Dattier vis-à-vis de Fusarium oxysporum f.sp. albedinis, Agent Causal du Bayoud. J Phytopathol 145:487–493

    CAS  Google Scholar 

  • Rezzonico F, Zala M, Keel C, Duffy B, Moënne-Loccoz Y, Défago G (2007) Is the ability of biocontrol fluorescent pseudomonads to produce the antifungal metabolite 2,4-diacetylphloroglucinol really synonymous with higher plant protection? New Phytol 173:861–872

    CAS  PubMed  Google Scholar 

  • Ridge RW (1988) Investigation of the cytoskeleton of freeze substituted root hairs. 6ot. Mag Tokyo 101:427–441

    Google Scholar 

  • Rioux CR, Jordan DC, Rattray JBM (1986) Iron requirement of Rhizobium leguminosarum and secretion of anthranilic acid during growth on an iron-deficient medium. Arch Biochem 248:175–182

    CAS  PubMed  Google Scholar 

  • Robertson JG, Lyttleton P, Bullivant S, Grayston GF (1978) Membranes in lupin root nodules. I. The role of Golgi bodies in the biogenesis of Infection threads and peribacteroid membranes. J Cell Sci 30:129–149

    CAS  PubMed  Google Scholar 

  • Rodriguez H, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17:319–339

    CAS  PubMed  Google Scholar 

  • Ronchi AL, Grassano A, Balatti AP (1997) Perlite as a carrier for legume inoculants. Agrochimica 41:186–195

    Google Scholar 

  • Roth LE, Stacey G (1989) Bacterium release into host cells of nitrogen-fixing soybean nodules: the symbiosome membrane comes from three sources. Eur J Cell Biol 49(1):13–23

    CAS  PubMed  Google Scholar 

  • Roughley RJ, Vincent J (1967) Growth and survival of Rhizobium spp. in peat culture. J Appl Bacteriol 30:362–376

    Google Scholar 

  • Roy N, Bhattacharyya P, Chakrabartty PK (1994) Iron acquisition during growth in an iron deficient medium by Rhizobium sp. isolated from Cicer arietinum. Microbiology 140:2811–2820

    CAS  Google Scholar 

  • Rugheim AM, Abdelgani ME (2009) Effects of microbial and chemical fertilization on yield and seed quality of faba bean. 9th conference of the African crop science society: science and technology supporting food security in Africa. Cape Town, South Africa 28 September–1 October 2009

    Google Scholar 

  • Ruiz Duenas FJ, Martinez MJ (1996) Enzymatic activities of Trametes versicolor and Pleurotus eryngii, implicated in biocontrol of Fusarium oxysporum f. sp. lycopersici. Curr Microbiol 32:151–155

    CAS  Google Scholar 

  • Ruiz B, Chávez A, Forero A, García-Huante Y, Romero A, Sánchez M, Rocha D, Sánchez B, Rodríguez-Sanoja R, Sánchez S, Langley E (2010) Production of microbial secondary metabolites: regulation by the carbon source. Crit Rev Microbiol 36(2):146–167

    CAS  PubMed  Google Scholar 

  • Sagolshemcha R, Devi YN, Singh WR (2017) Plant growth promoting effect and biocontrol potential of Rhizobium spp. against Macrophomina phaseolina. Int J Curr Microbiol App Sci 6(6):2695–2701

    CAS  Google Scholar 

  • Sáncheza AC, Gutiérrezc RT, Santanab RC, Urrutiab AR, Fauvarta M, Michielsa J, Vanderleydena J (2014) Effects of co-inoculation of native Rhizobium and Pseudomonas strains on growth parameters and yield of two contrasting Phaseolus vulgaris L. genotypes under Cuban soil conditions. Eur J Soil Biol 62:105–112

    Google Scholar 

  • Seneviratne G (2003) Development of eco-friendly, beneficial microbial biofilms. Curr Sci 85:1395–1396

    Google Scholar 

  • Seneviratne G, Zavahir JS, Bandara WMMS, Weerasekara MLMAW (2008) Fungal-bacterial biofilms: their development for novel biotechnological applications. World J Microbiol Biotechnol 24:739–743. https://doi.org/10.1007/s11274-007-9539-8

    Article  CAS  Google Scholar 

  • Shaban W, El-Bramawy M (2011) Impact of dual inoculation with Rhizobium and Trichoderma on damping off, root rot diseases and plant growth parameters of some legumes field crop under greenhouse conditions. Intl Res J Agric Sci Soil Sci 1:98–108

    Google Scholar 

  • Siddiqui ZA (2006) PGPR: prospective biocontrol agents of plant pathogens. In: Siddiqui ZA (ed) PGPR: biocontrol and biofertilization. Springer, Dordrecht, pp 111–142. https://doi.org/10.1007/1-4020-4152-7_4

    Chapter  Google Scholar 

  • Siddiqui IA, Shaukat SS (2002) Mixtures of plant disease suppressive bacteria enhance biological control of multiple tomato pathogens. Biol Fert Soils 36:260–268

    Google Scholar 

  • Siddiqui IA, Ehteshamul-Haque S, Zaki MJ, Abdul G (2000) Effect of urea on the efficacy of Bradyrhizobium sp. and Trichoderma harzianum in the control of root infecting fungi in mungbean and sunflower. Sarhad J Agric 16:403–406

    Google Scholar 

  • Siddiqui IA, Shaukat SS, Hussain-Sheikh I, Khan A (2006) Role of cyanide production by Pseudomonas fluorescens CHA0 in the suppression of root-knot nematode, Meloidogyne javanica in tomato. World J Microbiol Biotechnol 22(6):641–650

    CAS  Google Scholar 

  • Singh PK, Singh M, Vyas D (2010) Biocontrol of fusarium wilt of chickpea using arbuscular mycorrhizal fungi and Rhizobium leguminosorum biovar. Caryologia 63:349–353

    Google Scholar 

  • Singh HB, Sarma BK, Keswani C (eds) (2016) Agriculturally important microorganisms: commercialization and regulatory requirements in Asia. Springer, Singapore

    Google Scholar 

  • Singh HB, Sarma BK, Keswani C (eds) (2017) Advances in PGPR. CABI, London

    Google Scholar 

  • Smith MJ, Shoolery JN, Schwyn B, Holden I, Neilands JB (1985) Rhizobactin, a structurally novel siderophore from Rhizobium meliloti. J Am Chem Soc 107:1739–1743. https://doi.org/10.1021/ja00292a047

    Article  CAS  Google Scholar 

  • Smitha M, Singh R (2014) Biocontrol of phytopathogenic fungi using mycolytic enzymes produced by rhizospheric bacteria of Cicer arietinum. Indian J Agric Biochem 27:215–218

    Google Scholar 

  • Spaink H (1992) Rhizobial lipopolysaccharides: answers and questions. Plant Mol Biol 20:977–986

    CAS  PubMed  Google Scholar 

  • Sparow SD, Ham GE (1983) Survival of Rhizobium phaseoli in six carrier materials. Agron J 75:181–184

    Google Scholar 

  • Sridevi M, Mallaiah K (2008) Factors effecting chitinase activity of Rhizobium sp. from Sesbania sesban. Biologia 63:307–312

    CAS  Google Scholar 

  • Stephens JHG, Rask HM (2000) Inoculant production and formulation. Field Crops Res 65:249–258

    Google Scholar 

  • Stokkermans TJW, Peters NK (1994) Bradyrhizobium elkanii lipooligosaccharide signal induce complete nodule structures on Glycine soja Siebold et Zucc. Planta 193:413–420

    CAS  PubMed  Google Scholar 

  • Sutton WD, Pankhurst CE, Craig AS (1981) The rhizobium bacteroid state. In: Bourne GH, Danielli JF (eds) International review of cytology, supplement 13. Academic, New York, pp 149–177

    Google Scholar 

  • Szekeres A, Kredics L, Antal Z, Kevei F, Manczinger L (2004) Isolation and characterization of protease overproducing mutants of Trichoderma harzianum. FEMS Microbiol Lett 233:215–222

    CAS  PubMed  Google Scholar 

  • Temprano F, Albareda M, Camacho M, Daza A, Santamaría C, Rodríguez-Navarro ND (2002) Survival of several Rhizobium/Bradyrhizobium strains on different inoculant formulations and inoculated seeds. Int Microbiol 5:81–86. https://doi.org/10.1007/s10123-002-

    Article  CAS  PubMed  Google Scholar 

  • Triplett EW, Barta TM (1987) Trifolitoxin production and nodulation are necessary for the expression of superior nodulation competitiveness by Rhizobium leguminosarum bv. trifolii strain T24 on clover. Plant Physiol 85:335–342

    CAS  PubMed  PubMed Central  Google Scholar 

  • Triveni S, Prasanna R, Shukla L, Saxena AK (2013) Evaluating the biochemical traits of novel Trichoderma-based biofilms for use as plant growth-promoting inoculants. Ann Microbiol 63:1147–1156. https://doi.org/10.1007/s13213-012-0573-x

    Article  CAS  Google Scholar 

  • Van Kammen A (1984) Suggested nomenclature for plant genes involved in nodulation and symbiosis. Plant Mol Biol Rep 2:43–45

    Google Scholar 

  • van Rhijn P, Vanderleyden J (1995) The Rhizobium–plant symbiosis. Microb Rev 59(1):124–142

    Google Scholar 

  • VandenBosch KA, Bradley DJ, Knox JP, Perotto S, Butcher GW, Brewin NJ (1989) Common components of the infection thread matrix and the inter cellular space identified by immune cytochemical analysis of pea nodules and uninfected roots. EMBO J 8(2):335–341

    CAS  PubMed  PubMed Central  Google Scholar 

  • Verdine GL (1996) The combinatorial chemistry of nature. Nature 384:11–13

    CAS  PubMed  Google Scholar 

  • Verma DPS, Hong Z (1996) Biogenesis of the peribacteriod membrane in root nodules. Trends Microbiol 4(9):364–368

    CAS  PubMed  Google Scholar 

  • Verma D, Long S (1983) Molecular biology of Rhizobium plant symbiosis. In: Jeon K (ed) Intracellular symbiosis. Academic, New York, pp 211–245

    Google Scholar 

  • Vincent J (1974) Root nodule symbioses with Rhizobium. In: Quispel A (ed) Biology of nitrogen fixation. North Holland Press, Amsterdam, pp 265–341

    Google Scholar 

  • Vitousek PM, Aber JD, Howarth RW, Likens GE, Matson PA, Schindler DW, Schlesinger WH, Tilman DG (1997) Human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl 7:737–750

    Google Scholar 

  • Weidemann C, Tenhaken R, Höhl U, Barz W (1991) Medicarpin and maackiain 3-O-glucoside-6′-O-malonate conjugates are constitutive compounds in chickpea (Cicer arietinum L.) cell cultures. Plant Cell Rep 10:371–374. https://doi.org/10.1007/bf00193162

    Article  CAS  PubMed  Google Scholar 

  • Weigand F, Köster J, Weltzien H, Barz W (1986) Accumulation of phytoalexins and isoflavone glucosides in a resistant and a susceptible cultivar of Cicer arietinum during infection with Ascochyta rabiei. J Phytopathol 115:214–221

    CAS  Google Scholar 

  • Yu GY, Sinclair JB, Hartman GL, Bertagnolli BL (2002) Production of iturin a by Bacillus amyloliquefaciens suppressing Rhizoctonia solani. Soil Biol Biochem 34:955–963. https://doi.org/10.1016/S0038-0717(02)00027-5

    Article  CAS  Google Scholar 

  • Zahran HH (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63(4):968–989

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zakhia F, Jeder H, Domergue O, Willems A, Cleyet-Marel JC, Gillis M, Dreyfus B, de Lajudie P (2004) Characterisation of wild legume nodulating bacteria (LNB) in the infra-arid zone of Tunisia. Syst Appl Microbiol 27(3):380–395

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Singh, P., Rajput, R.S., Ram, R.M., Singh, H.B. (2019). A Deeper Insight into the Symbiotic Mechanism of Rhizobium spp. from the Perspective of Secondary Metabolism. In: Singh, H., Keswani, C., Reddy, M., Sansinenea, E., García-Estrada, C. (eds) Secondary Metabolites of Plant Growth Promoting Rhizomicroorganisms. Springer, Singapore. https://doi.org/10.1007/978-981-13-5862-3_14

Download citation

Publish with us

Policies and ethics