Skip to main content
SpringerLink
Log in

Interactions of Rhizobia with Nonleguminous Plants: A Molecular Ecology Perspective for Enhanced Plant Growth

  • Chapter
  • First Online:
Nitrogen Fixing Bacteria: Sustainable Growth of Non-legumes

Part of the book series: Microorganisms for Sustainability ((MICRO,volume 36))

Abstract

Rhizobia are known for its symbiotic association with the leguminous plants, which have role in biological nitrogen fixation in root nodules. However, its association with nonlegumes has received relatively lesser attention. With the progress in technology and research strategies, the molecular ecological perspective of rhizobial interaction with nonlegumes has recently gained much progress. Rhizobia are now known to form symbiosis with nonlegumes without forming true nodules, and yet promote the growth of nonlegumes through direct and indirect mechanisms. Plant growth-promoting traits such as production of phytohormones, siderophore, ACC deaminase activity, phosphate solubilization, and improving the nutrient uptake by modulating the root structure are the PGPR mechanisms described for rhizobia. Recently, rhizobia have also been reported to modulate the rhizospheric bacterial community structure that helps plants to adapt to a new or hostile environment. The rhizobia can also mediate biocontrol through antibiosis, parasitism, or competition which inhibits plant pathogens, induces systemic resistance in the host plant, and also releases exopolysaccharides for improving root adhering soil in the plants. The research on cell-to-cell communication for this unique synergistic interaction with nonlegumes, such as rice and wheat plants, has revealed interesting facts, which may be used for better plant growth. Therefore, the application of rhizobia as PGPR and further use as a biofertilizer, stress regulators, and biocontrol agents for nonleguminous plants need more intervention from the perspective of its interaction with nonlegumes, which has been addressed in this article. Also, the importance of rhizobia with the perspective of molecular ecology, genomics attributes of rhizobia colonizing nonlegumes, and possible rhizobial engineering have been included.

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

Access this chapter

Log in via an institution
eBook
USD 16.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
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

  • Abd-Alla MH (1994) Use of organic phosphorus by Rhizobium leguminosarum biovarviceae phosphatases. Biol Fertil Soil 18(3):216–218

    Article  CAS  Google Scholar 

  • Abdel-Aziz RA, Radwan SMA, Abdel-Kader MM, Barakat MIA (1996) Biocontrol of faba bean root-rot using VA mycorrhizae and its effect on biological nitrogen fixation. Egypt J Microbiol (Egypt)

    Google Scholar 

  • Abou-Shanab RA, Angle JS, Delorme TA, Chaney RL, Van Berkum P, Moawad H et al (2003) Rhizobacterial effects on nickel extraction from soil and uptake by Alyssum murale. New Phytol 158(1):219–224

    Article  CAS  Google Scholar 

  • Afzal A, Bano A (2008) Rhizobium and phosphate-solubilizing bacteria improve the yield and phosphorus uptake in wheat (Triticum aestivum). Int J Agric Biol 10(1):85–88

    CAS  Google Scholar 

  • Ahmad E, Khan M, Zaidi A (2013) ACC deaminase producing Pseudomonas putida strain PSE3 and Rhizobium leguminosarum strain RP2 in synergism improves growth, nodulation and yield of pea grown in alluvial soils. Symbiosis 61(2):93–104

    Article  CAS  Google Scholar 

  • Akintokun AK, Taiwo MO (2016) Comparison of single culture and the consortium of growth-promoting rhizobacteria from three tomato (Lycopersicon esculentum Mill) varieties. Adv Plants Agric Res 5(1):00167

    Google Scholar 

  • Alagawadi AR, Gaur AC (1988) Associative effect of Rhizobium and phosphate-solubilizing bacteria on the yield and nutrient uptake of chickpea. Plant Soil 105(2):241–246

    Article  Google Scholar 

  • Alami Y, Achouak W, Marol C, Heulin T (2000) Rhizosphere soil aggregation and plant growth promotion of sunflowers by an exopolysaccharide-producing Rhizobium sp. strain isolated from sunflower roots. Appl Environ Microbiol 66(8):3393–3398

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alexandre A, Oliveira S (2013) Response to temperature stress in rhizobia. Crit Rev Microbiol 39(3):219–228

    Article  CAS  PubMed  Google Scholar 

  • Ali SZ, Sandhya V, Grover M, Kishore N, Rao LV, Venkateswarlu B (2009) Pseudomonas sp. strain AKM-P6 enhances tolerance of sorghum seedlings to elevated temperatures. Biol Fertil Soil 46(1):45–55

    Article  CAS  Google Scholar 

  • Alikhani HA, Saleh-Rastin N, Antoun H (2007) Phosphate solubilization activity of rhizobia native to Iranian soils. In: Velázquez E, Rodríguez-Barrueco C (eds) First international meeting on microbial phosphate solubilization. Developments in plant and soil sciences, vol 102. Springer, Dordrecht, pp 35–41

    Chapter  Google Scholar 

  • Al-Mallah MK, Davey MR, Cocking EC (1989) Formation of nodular structures on rice seedlings by rhizobia. J Exp Bot 40(4):473–478

    Article  Google Scholar 

  • Al-Mallah MK, Davey MR, Cocking EC (1990) Enzyme treatment, PEG, biotin and mannitol, stimulate nodulation of white clover by Rhizobium trifolii. J Plant Physiol 137(1):15–19

    Article  CAS  Google Scholar 

  • Alström S (1991) Induction of disease resistance in common bean susceptible to halo blight bacterial pathogen after seed bacterization with rhizosphere pseudomonads. J Gen Appl Microbiol 37(6):495–501

    Article  Google Scholar 

  • Alström S, Burns RG (1989) Cyanide production by rhizobacteria as a possible mechanism of plant growth inhibition. Biol Fertil Soil 7(3):232–238

    Article  Google Scholar 

  • Altúzar-Molina A, Lozano L, Ortíz-Berrocal M, Ramírez M, Martínez L, de Lourdes Velázquez-Hernández M et al (2020) Expression of the legume-specific nod factor receptor proteins alters developmental and immune responses in rice. Plant Mol Biol Reporter 38(2):262–281

    Article  Google Scholar 

  • Amara MA, Dahdoh MSA (1995) Effect of inoculation with plant-growth promoting rhizobacteria, PGPR on yield and uptake of nutrients by wheat grown on sandy soil. In: 5th. National Congress on Bio-Agriculture in Relation to Environment, Cairo (Egypt) 20–21 Nov 1995

    Google Scholar 

  • Antoun H, Kloepper JW (2001) Plant growth-promoting rhizobacteria (PGPR). In: Brenner S, Miller JH (eds) Encyclopedia of genetics. Academic Press, New York, pp 1477–1480

    Chapter  Google Scholar 

  • Antoun H, Prevost D (2000) PGPR activity of Rhizobium with non-leguminous plants. In: Proceedings of the 5th international PGPR workshop. Villa Carlos Paz, Córdoba, Argentina, p 62

    Google Scholar 

  • Antoun H, Bordeleau LM, Gagnon C (1978) Antagonisme entre Rhizobium meliloti et Fusarium oxysporum en relation avec l’efficacité symbiotique. Can J Plant Sci 58(1):75–78

    Article  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.). In: Hardarson G, Broughton WJ (eds) Molecular microbial ecology of the soil. Developments in plant and soil sciences, vol 83. Springer, Dordrecht, pp 57–67

    Chapter  Google Scholar 

  • Anyia AO, Archambault DJ, Slaski JJ (2004) Growth promoting effects of the diazotroph Azorhizobium caulinodans on Canadian wheat cultivars. In: Proceedings of the 4th International Crop Science Congress, Brisbane, Australia, pp 201–202

    Google Scholar 

  • 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

    Google Scholar 

  • Arora NK, Verma M, Mishra J (2017) Rhizobial bioformulations: past, present and future. In: Mehnaz S (ed) Rhizotrophs: plant growth promotion to bioremediation. Microorganisms for sustainability, vol 2. Springer, Singapore, pp 69–99

    Chapter  Google Scholar 

  • Arshad M, Shaharoona B, Mahmood T (2008) Inoculation with Pseudomonas spp. containing ACC-deaminase partially eliminates the effects of drought stress on growth, yield, and ripening of pea (Pisum sativum L.). Pedosphere 18(5):611–620

    Article  Google Scholar 

  • Atzorn R, Crozier A, Wheeler CT, Sandberg G (1988) Production of gibberellins and indole-3-acetic acid by Rhizobium phaseoli in relation to nodulation of Phaseolus vulgaris roots. Planta 175(4):532–538

    Article  CAS  PubMed  Google Scholar 

  • Bahulikar RA, Torres-Jerez I, Worley E, Craven K, Udvardi MK (2014) Diversity of nitrogen-fixing bacteria associated with switchgrass in the native tallgrass prairie of Northern Oklahoma. Appl Environ Microbiol 80(18):5636–5643

    Article  PubMed  PubMed Central  Google Scholar 

  • Baier R, Schiene K, Kohring B, Flaschel E, Niehaus K (1999) Alfalfa and tobacco cells react differently to chitin oligosaccharides and Sinorhizobium meliloti nodulation factors. Planta 210(1):157–164

    Article  CAS  PubMed  Google Scholar 

  • Banerjee S, Schlaeppi K, van der Heijden MG (2018) Keystone taxa as drivers of microbiome structure and functioning. Nat Rev Microbiol 16(9):567–576

    Article  CAS  PubMed  Google Scholar 

  • Bao Z, Okubo T, Kubota K, Kasahara Y, Tsurumaru H, Anda M et al (2014) Metaproteomic identification of diazotrophic methanotrophs and their localization in root tissues of field-grown rice plants. Appl Environ Microbiol 80(16):5043–5052

    Article  PubMed  PubMed Central  Google Scholar 

  • Bardin SD, Huang HC, 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 Bot 82(3):291–296

    Article  Google Scholar 

  • Belimov AA, Kojemiakov AP, Chuvarliyeva CN (1995) Interaction between barley and mixed cultures of nitrogen fixing and phosphate-solubilizing bacteria. Plant Soil 173(1):29–37

    Article  CAS  Google Scholar 

  • Belimov AA, Safronova VI, Sergeyeva TA, Egorova TN, Matveyeva VA, Tsyganov VE et al (2001) Characterization of plant growth-promoting rhizobacteria isolated from polluted soils and containing 1-aminocyclopropane-1-carboxylate deaminase. Can J Microbiol 47(7):642–652

    Article  CAS  PubMed  Google Scholar 

  • Belimov AA, Hontzeas N, Safronova VI, Demchinskaya SV, Piluzza G, Bullitta S, Glick BR (2005) Cadmium-tolerant plant growth-promoting bacteria associated with the roots of Indian mustard (Brassica juncea L. Czern.). Soil Biol Biochem 37(2):241–250

    Article  CAS  Google Scholar 

  • Bender GL, Preston L, Barnard D, Rolfe BG (1990) Formation of nodule-like structures on the roots of the non-legumes rice and wheat. In: Nitrogen fixation: Achievements and objectives. Chapman and Hall, New York, p 825

    Google Scholar 

  • Bera R, Seal A, Bhattacharyya P, Das TH, Sarkar D, Kangjoo K (2006) Targeted yield concept and a framework of fertilizer recommendation in irrigated rice domains of subtropical India. J Zhejiang Univ Sci B 7(12):963–968

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beveridge CA, Gresshoff PM, Rameau C, Turnbull CG (2003) Additional signalling compounds are required to orchestrate plant development. J Plant Growth Regul 22(1):15–24

    Article  CAS  Google Scholar 

  • Bhattacharjee RB, Singh A, Mukhopadhyay SN (2008) Use of nitrogen-fixing bacteria as biofertiliser for non-legumes: prospects and challenges. Appl Microbiol Biotechnol 80(2):199–209

    Article  CAS  PubMed  Google Scholar 

  • Bhattacharya C, Deshpande B, Pandey B (2013) Isolation and characterization of Rhizobium sp. form root of legume plant (Pisum sativum) and its antibacterial activity against different bacterial strains. Int J Agric Food Sci 3(4):138–141

    Google Scholar 

  • Biederbeck VO, Lupwayi NZ, Hanson KG, Rice WA, Zentner RP (2000) Effect of long-term rotation with lentils on rhizosphere ecology and on endophytic rhizobia in wheat. In: Book of abstracts, 17th North American Conference on Symbiotic Nitrogen Fixation 23:28–29

    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(5):1644–1650

    Article  CAS  Google Scholar 

  • Bodelier PL, Wijlhuizen AG, Blom CW, Laanbroek HJ (1997) Effects of photoperiod on growth of and denitrification by Pseudomonas chlororaphis in the root zone of Glyceria maxima, studied in a gnotobiotic microcosm. Plant Soil 190(1):91–103

    Article  CAS  Google Scholar 

  • Boiero L, Perrig D, Masciarelli O, Penna C, Cassán F, Luna V (2007) Phytohormone production by three strains of Bradyrhizobium japonicum and possible physiological and technological implications. Appl Microbiol Biotechnol 74(4):874–880

    Article  CAS  PubMed  Google Scholar 

  • Bolton GW, Nester EW, Gordon MP (1986) Plant phenolic compounds induce expression of the Agrobacterium tumefaciens loci needed for virulence. Science 232(4753):983–985

    Article  CAS  PubMed  Google Scholar 

  • Borges CS, de Sá ES, Muniz AW, Osorio Filho BD (2019) Potential use of Rhizobium for vegetable crops growth promotion. Afr J Agric Res 14(8):477–483

    Article  CAS  Google Scholar 

  • Bowen GD, Rovira AD (1999) The rhizosphere and its management to improve plant growth. Adv Agron 66:1–102

    Article  Google Scholar 

  • Breil BT, Ludden PW, Triplett EW (1993) DNA sequence and mutational analysis of genes involved in the production and resistance of the antibiotic peptide trifolitoxin. J Bacteriol 175(12):3693–3702

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buhian WP, Bensmihen S (2018) Mini-review: nod factor regulation of phytohormone signaling and homeostasis during rhizobia-legume symbiosis. Front Plant Sci 9:1247

    Article  PubMed  PubMed Central  Google Scholar 

  • Bulgarelli D, Garrido-Oter R, Münch PC, Weiman A, Dröge J, Pan Y et al (2015) Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host Microbe 17(3):392–403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burd GI, Dixon DG, Glick BR (2000) Plant growth-promoting bacteria that decrease heavy metal toxicity in plants. Can J Microbiol 46(3):237–245

    Article  CAS  PubMed  Google Scholar 

  • Carletti S, Caceres ER, Llorent B (1994) Growth promotion by PGPR on different plant species growing in hydroponic conditions. In: Improving plant productivity with rhizosphere bacteria. Proc. 3rd international workshop on plant growth-promoting rhizobacteria, Adelaide, Australia

    Google Scholar 

  • Carrillo GC, Vazquez MDRG (1992) Comparative study of siderophore-like activity of Rhizobium phaseoli and Pseudomonas fluorescens. J Plant Nutr 15(5):579–590

    Article  CAS  Google Scholar 

  • Carson KC, Holliday S, Glenn AR, Dilworth MJ (1992) Siderophore and organic acid production in root nodule bacteria. Arch Microbiol 157(3):264–271

    Article  CAS  PubMed  Google Scholar 

  • Carson KC, Meyer JM, Dilworth MJ (2000) Hydroxamate siderophores of root nodule bacteria. Soil Biol Biochem 32(1):11–21

    Article  CAS  Google Scholar 

  • Chabot R, Antoun H, Cescas MP (1993) Stimulation de la croissance du maïs et de la laitue romaine par des microorganismes dissolvant le phosphore inorganique. Can J Microbiol 39(10):941–947

    Article  Google Scholar 

  • Chabot R, Antoun H, Cescas MP (1996) Growth promotion of maize and lettuce by phosphate-solubilizing Rhizobium leguminosarum biovar. phaseoli. Plant Soil 184(2):311–321

    Article  CAS  Google Scholar 

  • Chabot R, Beauchamp CJ, Kloepper JW, Antoun H (1998) Effect of phosphorus on root colonization and growth promotion of maize by bioluminescent mutants of phosphate-solubilizing Rhizobium leguminosarum biovar phaseoli. Soil Biol Biochem 30(12):1615–1618

    Article  Google Scholar 

  • Chaintreuil C, Giraud E, Prin Y, Lorquin J, Bâ A, Gillis M et al (2000) Photosynthetic bradyrhizobia are natural endophytes of the African wild rice Oryza breviligulata. Appl Environ Microbiol 66(12):5437–5447

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chakraborty U, Purkayastha RP (1984) Role of rhizobitoxine in protecting soybean roots from Macrophomina phaseolina infection. Can J Microbiol 30(3):285–289

    Article  CAS  PubMed  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(1):124–130

    Article  Google Scholar 

  • Chapman JM, Muday GK (2021) Flavonols modulate lateral root emergence by scavenging reactive oxygen species in Arabidopsis thaliana. J Biol Chem 296

    Google Scholar 

  • Chen H, Richardson AE, Gartner E, Djordjevic MA, Roughley RJ, Rolfe BG (1991) Construction of an acid-tolerant Rhizobium leguminosarum biovar trifolii strain with enhanced capacity for nitrogen fixation. Appl Environ Microbiol 57(7):2005–2011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chi F, Shen SH, Cheng HP, Jing YX, Yanni YG, Dazzo FB (2005) Ascending migration of endophytic rhizobia, from roots to leaves, inside rice plants and assessment of benefits to rice growth physiology. Appl Environ Microbiol 71(11):7271–7278

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chi F, Yang P, Han F, Jing Y, Shen S (2010) Proteomic analysis of rice seedlings infected by Sinorhizobium meliloti 1021. Proteomics 10(9):1861–1874

    Article  CAS  PubMed  Google Scholar 

  • Chiwocha SD, Abrams SR, Ambrose SJ, Cutler AJ, Loewen M, Ross AR, Kermode AR (2003) A method for profiling classes of plant hormones and their metabolites using liquid chromatography-electrospray ionization tandem mass spectrometry: an analysis of hormone regulation of thermodormancy of lettuce (Lactuca sativa L.) seeds. Plant J 35(3):405–417

    Article  CAS  PubMed  Google Scholar 

  • Cocking EC (2003) Endophytic colonization of plant roots by nitrogen-fixing bacteria. Plant Soil 252(1):169–175

    Article  CAS  Google Scholar 

  • Cocking EC, Srivastava JS, Kothari SL, Davey M (1992) Invasion of nonlegume plants by diazotrophic bacteria. In: Khush G, Bennett J (eds) Nodulation and nitrogen fixation in rice: potentials and prospects, pp 119–121

    Google Scholar 

  • Cocking EC, Kothari SL, Batchelor CA, Jain S, Webster G, Jones J et al (1995) Interaction of rhizobia with non-legume crops for symbiotic nitrogen fixation nodulation. In: Fendrik I, del Gallo M, Vanderleyden J, de Zamaroczy M (eds) Azospirillum VI and related microorganisms. NATO ASI series, vol 37. Springer, Berlin, pp 197–205

    Chapter  Google Scholar 

  • Cook RL, Hesterberg D (2013) Comparison of trees and grasses for rhizoremediation of petroleum hydrocarbons. Int J Phytoremediation 15(9):844–860

    Article  CAS  PubMed  Google Scholar 

  • Dakora FD (2003) Defining new roles for plant and rhizobial molecules in sole and mixed plant cultures involving symbiotic legumes. New Phytol 158(1):39–49

    Article  CAS  Google Scholar 

  • Dakora FD, Phillips DA (2002) Root exudates as mediators of mineral acquisition in low-nutrient environments. In: Food security in nutrient-stressed environments: exploiting plants’ genetic capabilities, pp 201–213

    Chapter  Google Scholar 

  • Dardanelli MS, de Cordoba FJF, Espuny MR, Carvajal MAR, Díaz MES, Serrano AMG et al (2008) Effect of Azospirillum brasilense coinoculated with Rhizobium on Phaseolus vulgaris flavonoids and Nod factor production under salt stress. Soil Biol Biochem 40(11):2713–2721

    Article  CAS  Google Scholar 

  • Dardanelli MS, Manyani H, González-Barroso S, Rodríguez-Carvajal MA, Gil-Serrano AM, Espuny MR et al (2010) Effect of the presence of the plant growth-promoting rhizobacterium (PGPR) Chryseobacterium balustinum Aur9 and salt stress in the pattern of flavonoids exuded by soybean roots. Plant Soil 328(1):483–493

    Article  CAS  Google Scholar 

  • Date RA (2001) Advances in inoculant technology: a brief review. Aust J Exp Agric 41(3):321–325

    Article  CAS  Google Scholar 

  • Dazzo FB, Yanni YG, Rizk R, de Bruijn FJ, Rademaker J, Squartini A, Corich V, Mateos P, Martínez-Molina E, Velázquez E, Biswas JC, Hernandez RJ, Ladha JK, Hill J, Weinman J, Rolfe BG, Vega-Hernández M, Bradford JJ, Hollingsworth RI, Ostrom P, Marshall E, Jain T, Orgambide G, Philip-Hollingsworth S, Triplett E, Malik KA, Maya-Flores J, Hartmann A, Umali-Garcia M, Izaguirre-Mayoral ML (2000) Progress in multinational collaborative studies on the beneficial association between Rhizobium leguminosarum bv. trifolii and rice. In: Ladha JK, Reddy PM (eds) The quest for nitrogen fixation in rice. Los Baños, The Philippines, IRRI Press, pp 167–189

    Google Scholar 

  • De Bruijn FJ, Jing Y, Dazzo FB (1995) Potential and pitfalls of trying to extend symbiotic interactions of nitrogen-fixing organisms to presently non-nodulated plants, such as rice. In: Management of biological nitrogen fixation for the development of more productive and sustainable agricultural systems. Springer, Dordrecht, pp 225–240

    Google Scholar 

  • De Jong AJ, Heidstra R, Spaink HP, Hartog MV, Meijer EA, Hendriks T et al (1993) Rhizobium lipooligosaccharides rescue a carrot somatic embryo mutant. Plant Cell 5(6):615–620

    Article  PubMed  PubMed Central  Google Scholar 

  • Depret G, Houot S, Allard MR, Breuil MC, Nouaïm R, Laguerre G (2004) Long-term effects of crop management on Rhizobium leguminosarum biovar viciae populations. FEMS Microbiol Ecol 51(1):87–97

    Article  CAS  PubMed  Google Scholar 

  • Deryło M, Choma A, Puchalski B, Suchanek W (1994) Siderophore activity in Rhizobium species isolated from different legumes. Acta Biochim Pol 41(1):7–11

    Article  PubMed  Google Scholar 

  • Deshwal VK, Dubey RC, Maheshwari DK (2003) Isolation of plant growth-promoting strains of Bradyrhizobium (Arachis) sp. with biocontrol potential against Macrophomina phaseolina causing charcoal rot of peanut. Curr Sci:443–448

    Google Scholar 

  • de Souza R, Sant’Anna FH, Ambrosini A, Tadra-Sfeir M, Faoro H, Pedrosa FO, Souza EM, Passaglia LM (2015) Genome of Rhizobium sp. UR51a, isolated from rice cropped in Southern Brazilian fields. Genome Announc 3(2):e00249-15

    Article  PubMed  PubMed Central  Google Scholar 

  • DiCenzo GC, Zamani M, Milunovic B, Finan TM (2016) Genomic resources for identification of the minimal N2‐fixing symbiotic genome. Environ Microbiol 18(8):2534–2547

    Article  CAS  PubMed  Google Scholar 

  • Dobbelaere S, Vanderleyden J, Okon Y (2003) Plant growth-promoting effects of diazotrophs in the rhizosphere. Crit Rev Plant Sci 22(2):107–149

    Article  CAS  Google Scholar 

  • Dolan L (2001) The role of ethylene in root hair growth in Arabidopsis. J Plant Nutr Soil Sci 164(2):141–145

    Article  CAS  Google Scholar 

  • Dudeja SS, Suneja S, Khurana AL (1997) Iron acquisition system and its role in legume-Rhizobium symbiosis. Indian J Microbiol 37:1–12

    Google Scholar 

  • Dupin SE, Geurts R, Kiers ET (2020) The non-legume Parasponia andersonii mediates the fitness of nitrogen-fixing rhizobial symbionts under high nitrogen conditions. Front Plant Sci 10:1779

    Article  PubMed  PubMed Central  Google Scholar 

  • Dyachok JV, Tobin AE, Price NPJ, Von Arnold S (2000) Rhizobial Nod factors stimulate somatic embryo development in Picea abies. Plant Cell Rep 19(3):290–297

    Article  CAS  PubMed  Google Scholar 

  • Ehteshamul-Haque S, Ghaffar A (1992) Use of Bradyrhizobium japonicaum and fungicides in the control of root rot disease of sun flower. In: Proceedings of Status of Plant Pathology in Pakistan, Department of Botany, University of Karachi, Karachi, pp 261–266

    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(2):157–163

    Article  Google Scholar 

  • Ehteshamul-Haque S, Abid M, Sultana V, Ara J, Ghaffar A (1996) Use of organic amendments on the efficacy of biocontrol agents in the control of root rot and root knot disease complex of okra. Nematol Mediterr 24(1):13–16

    Google Scholar 

  • El-Tarabily KA, Soaud AA, Saleh ME, Matsumoto S (2006) Isolation and characterisation of sulfur-oxidising bacteria, including strains of Rhizobium, from calcareous sandy soils and their effects on nutrient uptake and growth of maize (Zea mays L.). Aust J Agric Res 57(1):101–111

    Article  CAS  Google Scholar 

  • Essel E, Xie J, Deng C, Peng Z, Wang J, Shen J et al (2019) Bacterial and fungal diversity in rhizosphere and bulk soil under different long-term tillage and cereal/legume rotation. Soil Till Res 194:104302

    Article  Google Scholar 

  • Etesami H, Alikhani HA, Jadidi M, Aliakbari A (2009) Effect of superior IAA producing rhizobia on N, P, K uptake by wheat grown under greenhouse condition. World Appl Sci J 6:1629–1633

    CAS  Google Scholar 

  • Fagorzi C, Checcucci A, DiCenzo GC, Debiec-Andrzejewska K, Dziewit L, Pini F et al (2018) Harnessing rhizobia to improve heavy-metal phytoremediation by legumes. Genes 9(11):542

    Article  PubMed Central  Google Scholar 

  • Fernández LA, Zalba P, Gómez MA, Sagardoy MA (2007) Phosphate-solubilization activity of bacterial strains in soil and their effect on soybean growth under greenhouse conditions. Biol Fertil Soil 43(6):805–809

    Article  Google Scholar 

  • Figueiredo MVB, Vilar JJ, Burity HA (1999) Alleviation of water stress effects in cowpea by Bradyrhizobium spp. inoculation. Plant Soil 207(1):67–75

    Article  Google Scholar 

  • Flores-Félix JD, Velázquez E, Martínez-Molina E, González-Andrés F, Squartini A, Rivas R (2021) Connecting the lab and the field: Genome analysis of phyllobacterium and Rhizobium strains and field performance on two vegetable crops. Agronomy 11(6):1124

    Article  Google Scholar 

  • Franche C, Lindström K, Elmerich C (2009) Nitrogen-fixing bacteria associated with leguminous and non-leguminous plants. Plant Soil 321(1):35–59

    Article  CAS  Google Scholar 

  • Gaby JC, Rishishwar L, Valderrama-Aguirre LC, Green SJ, Valderrama-Aguirre A, Jordan IK, Kostka JE (2018) Diazotroph community characterization via a high-throughput nifH amplicon sequencing and analysis pipeline. Appl Environ Microbiol 84(4):e01512–e01517

    Article  PubMed  PubMed Central  Google Scholar 

  • Galal YGM (2003) Assessment of nitrogen availability to wheat (Triticum aestivum L.) from inorganic and organic N sources as affected by Azospirillum brasilense and Rhizobium leguminosarum inoculation. Egypt J Microbiol 38:57–73

    Google Scholar 

  • García JE, Maroniche G, Creus C, Suárez-Rodríguez R, Ramirez-Trujillo JA, Groppa MD (2017) In vitro PGPR properties and osmotic tolerance of different Azospirillum native strains and their effects on growth of maize under drought stress. Microbiol Res 202:21–29

    Article  PubMed  Google Scholar 

  • García-Fraile P, Carro L, Robledo M, Ramírez-Bahena MH, Flores-Félix JD, Fernández MT, Mateos PF, Rivas R, Igual JM, Martínez-Molina E, Peix A, Velázquez E (2012) Rhizobium promotes non-legumes growth and quality in. PLoS One 7:38122

    Article  Google Scholar 

  • Gardener BBM, Fravel DR (2002) Biological control of plant pathogens: research, commercialization, and application in the USA. Plant Health Prog 3(1):17

    Article  Google Scholar 

  • Geddes BA, Kearsley J, Morton R, Finan TM (2020) The genomes of rhizobia. Adv Bot Res 94:2013–2249

    Google Scholar 

  • Geetha SJ, Joshi SJ (2013) Engineering rhizobial bioinoculants: a strategy to improve iron nutrition. Sci World J

    Google Scholar 

  • Geetha R, Desai AJ, Archana G (2009) Effect of the expression of Escherichia coli fhuA gene in Rhizobium sp. IC3123 and ST1 in planta: its role in increased nodule occupancy and function in pigeon pea. Appl Soil Ecol 43(2–3):185–190

    Article  Google Scholar 

  • Glick BR (2010) Using soil bacteria to facilitate phytoremediation. Biotechnol Adv 28(3):367–374

    Article  CAS  PubMed  Google Scholar 

  • Glick BR, Jacobson CB, Schwarze MM, Pasternak JJ (1994) 1-Aminocyclopropane-1-carboxylic acid deaminase mutants of the plant growth-promoting rhizobacterium Pseudomonas putida GR12-2 do not stimulate canola root elongation. Can J Microbiol 40(11):911–915

    Article  CAS  Google Scholar 

  • Glick BR, Karaturovíc DM, Newell PC (1995) A novel procedure for rapid isolation of plant growth-promoting pseudomonads. Can J Microbiol 41(6):533–536

    Article  CAS  Google Scholar 

  • Glick BR, Holguin G, Patten CL, Penrose DM (1999) Biochemical and genetic mechanisms used by plant growth-promoting bacteria. World Scientific

    Book  Google Scholar 

  • Gómez-Godínez LJ, Fernandez-Valverde SL, Romero JCM, Martínez-Romero E (2019) Metatranscriptomics and nitrogen fixation from the rhizoplane of maize plantlets inoculated with a group of PGPRs. Syst Appl Microbiol 42(4):517–525

    Article  PubMed  Google Scholar 

  • González V, Santamaría RI, Bustos P, Pérez-Carrascal OM, Vinuesa P, Juárez S et al (2019) Phylogenomic Rhizobium species are structured by a continuum of diversity and genomic clusters. Front Microbiol 10:910

    Article  PubMed  PubMed Central  Google Scholar 

  • Gopalakrishnan S, Sathya A, Vijayabharathi R, Varshney RK, Gowda CL, Krishnamurthy L (2015) Plant growth-promoting rhizobia: challenges and opportunities. 3 Biotech 5(4):355–377

    Article  PubMed  Google Scholar 

  • Goyal RK, Schmidt MA, Hynes MF (2021) Molecular biology in the improvement of biological nitrogen fixation by rhizobia and extending the scope to cereals. Microorganisms 9(1):125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Greetatorn T, Hashimoto S, Sarapat S, Tittabutr P, Boonkerd N, Uchiumi T, Teaumroong N (2019) Empowering rice seedling growth by endophytic Bradyrhizobium sp. SUTN 9-2. Lett Appl Microbiol 68(3):258–266

    CAS  PubMed  Google Scholar 

  • Greetatorn T, Hashimoto S, Maeda T, Fukudome M, Piromyou P, Teamtisong K et al (2020) Mechanisms of rice endophytic Bradyrhizobial cell differentiation and its role in nitrogen fixation. Microb Environ 35(3):ME20049

    Article  Google Scholar 

  • Grichko VP, Glick BR (2001) Amelioration of flooding stress by ACC deaminase-containing plant growth-promoting bacteria. Plant Physiol Biochem 39(1):11–17

    Article  CAS  Google Scholar 

  • Guerinot ML (1991) Iron uptake and metabolism in the rhizobia/legume symbioses. In: Iron nutrition and interactions in plants. Springer, Dordrecht, pp 239–249

    Chapter  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hafeez FY, Safdar ME, Chaudhry AU, Malik KA (2004) Rhizobial inoculation improves seedling emergence, nutrient uptake and growth of cotton. Aust J Exp Agric 44(6):617–622

    Article  Google Scholar 

  • Haggag WM, Wafaa MH (2002) Sustainable agriculture management of plant diseases. J Biol Sci 2(4):280–284

    Article  Google Scholar 

  • Han HS, Lee KD (2005) Plant growth-promoting rhizobacteria effect on antioxidant status, photosynthesis, mineral uptake and growth of lettuce under soil salinity. Res J Agric Biol Sci 1(3):210–215

    Google Scholar 

  • Hara S, Morikawa T, Wasai S, Kasahara Y, Koshiba T, Yamazaki K, Fujiwara T, Tokunaga T, Minamisawa K (2019) Identification of nitrogen-fixing Bradyrhizobium associated with roots of field-grown sorghum by metagenome and proteome analyses. Front Microbiol 10:407

    Article  PubMed  PubMed Central  Google Scholar 

  • Hilali A, Prévost D, Broughton WJ, Antoun H (2001) Effets de l’inoculation avec des souches de Rhizobium leguminosarum biovar trifolii sur la croissance du blé dans deux sols du Maroc. Can J Microbiol 47(6):590–593

    Article  CAS  PubMed  Google Scholar 

  • Hiltner L (1904) Uber nevere erfahrungen und probleme auf dem gebiet der boden bakteriologie und unter besonderer beurchsichtigung der grundungung und broche. Arbeit Deut Landw Ges Berlin 98:59–78

    Google Scholar 

  • Hirsch AM, Fang Y, Asad S, Kapulnik Y (1997) The role of phytohormones in plant-microbe symbioses. Plant Soil 194(1):171–184

    Article  CAS  Google Scholar 

  • Höflich G (2000) Colonization and growth promotion of non-legumes by Rhizobium bacteria. In: Bell CR, Brylinsky M, Johnson-Green P (eds) Microbial biosystems: new frontiers. Proceedings of the 8th international symposium on microbial ecology. Atlantic Canada Society for Microbial Ecology, Halifax, pp 827–830

    Google Scholar 

  • Höflich G, Wiehe W, Kühn G (1994) Plant growth stimulation by inoculation with symbiotic and associative rhizosphere microorganisms. Experientia 50(10):897–905

    Article  Google Scholar 

  • Honma M, Shimomura T (1978) Metabolism of 1-aminocyclopropane-1-carboxylic acid. Agric Biol Chem 42(10):1825–1831

    CAS  Google Scholar 

  • Hume DJ, Shelp BJ (1990) Superior performance of the hup−Bradyrhizobium japonicum strain 532C in Ontario soybean field trials. Can J Plant Sci 70(3):661–666

    Article  Google Scholar 

  • Humphry DR, Andrews M, Santos SR, James EK, Vinogradova LV, Perin L et al (2007) Phylogenetic assignment and mechanism of action of a crop growth-promoting Rhizobium radiobacter strain used as a biofertiliser on graminaceous crops in Russia. Antonie van Leeuwenhoek 91(2):105–113

    Article  PubMed  Google Scholar 

  • Hussain MB, Mehboob I, Zahir ZA, Naveed M, Asghar HN (2009) Potential of Rhizobium spp. for improving growth and yield of rice (Oryza sativa L.). Soil Environ 28(1):49–55

    Google Scholar 

  • Irar S, González EM, Arrese-Igor C, Marino D (2014) A proteomic approach reveals new actors of nodule response to drought in split-root grown pea plants. Physiol Plant 152(4):634–645

    Article  CAS  PubMed  Google Scholar 

  • Irshad A, Rehman RNU, Abrar MM, Saeed Q, Sharif R, Hu T (2021) Contribution of Rhizobium–legume symbiosis in salt stress tolerance in Medicago truncatula evaluated through photosynthesis, antioxidant enzymes, and compatible solutes accumulation. Sustainability 13(6):3369

    Article  CAS  Google Scholar 

  • Jadhav RS, Thaker NV, Desai A (1994) Involvement of the siderophore of cowpea Rhizobium in the iron nutrition of the peanut. World J Microbiol Biotechnol 10(3):360–361

    Article  CAS  PubMed  Google Scholar 

  • Janczarek M, Jaroszuk-Ściseł J, Skorupska A (2009) Multiple copies of rosR and pssA genes enhance exopolysaccharide production, symbiotic competitiveness and clover nodulation in Rhizobium leguminosarum bv. trifolii. Antonie Van Leeuwenhoek 96(4):471–486

    Article  CAS  PubMed  Google Scholar 

  • Jha PN, Gomaa AB, Yanni YG, El-Saadany AEY, Stedtfeld TM, Stedtfeld RD et al (2020) Alterations in the endophyte-enriched root-associated microbiome of rice receiving growth-promoting treatments of urea fertilizer and Rhizobium biofertilizer. Microb Ecol 79(2):367–382

    Article  CAS  PubMed  Google Scholar 

  • Jia HT, Liu JY, Shi YJ, Li DL, Wu FZ, Zhou XG (2019) Characterization of cucumber rhizosphere bacterial community with high-throughput amplicon sequencing. Allelopathy J 47(1):103–112

    Article  Google Scholar 

  • Jiménez-Gómez A, Flores-Félix JD, García-Fraile P, Mateos PF, Menéndez E, Velázquez E, Rivas R (2018) Probiotic activities of Rhizobium laguerreae on growth and quality of spinach. Sci Rep 8(1):1–10

    Article  Google Scholar 

  • Jing Y, Li G, Jin G, Shan X, Zhang B, Guan C, Li J (1990) Rice root nodules with acetylene reduction activity. In: Gresshoff PM, Roth LE, Stacey G, Newton WE (eds) Nitrogen fixation achievements and objectives, p 829

    Google Scholar 

  • Jing Y, Li G, Shan X (1992) Development of nodule-like structure on rice roots. In: Khush GS, Bennett J (eds) Nodulation and nitrogen fixation in rice, pp 123–126

    Google Scholar 

  • Joshi F, Chaudhari A, Joglekar P, Archana G, Desai A (2008) Effect of expression of Bradyrhizobium japonicum 61A152 fegA gene in Mesorhizobium sp., on its competitive survival and nodule occupancy on Arachis hypogea. Appl Soil Ecol 40(2):338–347

    Article  Google Scholar 

  • Joshi FR, Desai DK, Archana G, Desai AJ (2009) Enhanced survival and nodule occupancy of pigeon pea nodulating Rhizobium sp. ST1 expressing fegA gene of Bradyrhizobium japonicum 61A152. J Biol Sci 9:40–51

    CAS  Google Scholar 

  • Joshi AU, Andharia KN, Patel PA, Kotadiya RJ, Kothari RK (2019) Plant growth-promoting rhizobacteria: mechanism, application, advantages and disadvantages. In: Green biotechnology. Day Publishing House: Division of Astral International Pvt. Ltd., New Delhi, pp 13–40

    Google Scholar 

  • Kaci Y, Heyraud A, Barakat M, Heulin T (2005) Isolation and identification of an EPS-producing Rhizobium strain from arid soil (Algeria): characterization of its EPS and the effect of inoculation on wheat rhizosphere soil structure. Res Microbiol 156(4):522–531

    Article  CAS  PubMed  Google Scholar 

  • Kanade SN, Shaikh SM, Ade AB, Khilare VC (2010) Degradation of Malathion by Rhizobium isolated from fenugreek (Trigonella foenumgraecum). J Biotechnol Bioinform 1:240–242

    Google Scholar 

  • Khaitov B, Kurbonov A, Abdiev A, Adilov M (2016) Effect of chickpea in association with Rhizobium to crop productivity and soil fertility. Eurasian J Soil Sci 5(2):105–112

    Google Scholar 

  • Khalid A, Arshad M, Zahir ZA (2006) Phytohormones: microbial production and applications. In: Biological approaches to sustainable soil system, pp 207–220

    Chapter  Google Scholar 

  • Khan MS, Zaidi A, Wani PA, Oves M (2009) Role of plant growth-promoting rhizobacteria in the remediation of metal contaminated soils. Environ Chem Lett 7(1):1–19

    Article  Google Scholar 

  • Khan N, Zandi P, Ali S, Mehmood A, Adnan Shahid M, Yang J (2018) Impact of salicylic acid and PGPR on the drought tolerance and phytoremediation potential of Helianthus annus. Front Microbiol 2507

    Google Scholar 

  • Khokhar SN, Qureshi A (1998) Interaction of Azorhizobium caulinodans with different rice cultivars for increased N2-fixation. In: Nitrogen fixation with non-legumes. Springer, Dordrecht, pp 91–93

    Chapter  Google Scholar 

  • Klee HJ, Hayford MB, Kretzmer KA, Barry GF, Kishore GM (1991) Control of ethylene synthesis by expression of a bacterial enzyme in transgenic tomato plants. Plant Cell 3(11):1187–1193

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kloepper JW (1978) Plant growth-promoting rhizobacteria on radishes. In: Proceedings of the 4th international conference on plant pathogenic bacteria, Station de Pathologie Vegetale et Phytobacteriologie, INRA, Angers, France, 2, pp 879–882

    Google Scholar 

  • Kumar A, Patel JS, Meena VS, Srivastava R (2019) Recent advances of PGPR-based approaches for stress tolerance in plants for sustainable agriculture. Biocatal Agric Biotechnol 20:101271

    Article  Google Scholar 

  • Kumari B, Mallick MA, Solanki MK, Solanki AC, Hora A, Guo W (2019) Plant growth-promoting rhizobacteria (PGPR): modern prospects for sustainable agriculture. In: Plant health under biotic stress. Springer, Singapore, pp 109–127

    Chapter  Google Scholar 

  • Lagier JC, Dubourg G, Million M, Cadoret F, Bilen M, Fenollar F et al (2018) Culturing the human microbiota and culturomics. Nat Rev Microbiol 16(9):540–550

    Article  CAS  PubMed  Google Scholar 

  • Law IJ, Strijdom BW (1988) Inoculation of cowpea and wheat with strains of Bradyrhizobium sp. that differ in their production of indole acetic acid. S Afr J Plant Soil 6(3):161–166

    Article  Google Scholar 

  • Lay CY, Bell TH, Hamel C, Harker KN, Mohr R, Greer CW et al (2018) Canola root–associated microbiomes in the Canadian Prairies. Front Microbiol 9:1188

    Article  PubMed  PubMed Central  Google Scholar 

  • LeBlanc N, Crouch JA (2019) Prokaryotic taxa play keystone roles in the soil microbiome associated with woody perennial plants in the genus Buxus. Ecol Evol 9:11102–11111

    Article  PubMed  PubMed Central  Google Scholar 

  • Lemanceau P (1992) Effets bénéfiques de rhizobactéries sur les plantes: exemple des Pseudomonas spp fluorescents. Agronomie 12(6):413–437

    Article  Google Scholar 

  • Li WX, Kodama O, Akatsuka T (1991) Role of oxygenated fatty acids in rice phytoalexin production. Agric Biol Chem 55(4):1041–1047

    CAS  Google Scholar 

  • Li W, Nishiyama R, Watanabe Y, Van Ha C, Kojima M, An P, Tian L, Tian C, Sakakibara H, Tran LS (2018) Effects of overproduced ethylene on the contents of other phytohormones and expression of their key biosynthetic genes. Plant Physiol Biochem 128:170–177

    Article  CAS  PubMed  Google Scholar 

  • Lynch J (1990a) Substrate flow in the rhizosphere. Plant Soil 129:1–10

    Article  CAS  Google Scholar 

  • Lynch JM (1990b) The rhizosphere. Wiley Interscience, Chichester

    Google Scholar 

  • Lynch JM, Whipps JM (1990) Substrate flows in the rhizosphere. Plant Soil 129:1–10

    Article  CAS  Google Scholar 

  • Ma W, Sebestianova SB, Sebestian J, Burd GI, Guinel FC, Glick BR (2003) Prevalence of 1-aminocyclopropane-1-carboxylate deaminase in Rhizobium spp. Antonie Van Leeuwenhoek 83(3):285–291

    Article  CAS  PubMed  Google Scholar 

  • Ma W, Charles TC, Glick BR (2004) Expression of an exogenous 1-aminocyclopropane-1-carboxylate deaminase gene in Sinorhizobium meliloti increases its ability to nodulate alfalfa. Appl Environ Microbiol 70(10):5891–5897

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Machado RG, de Sá ELS, Hahn L, Oldra S, Mangrich dos Passos JF, Osorio Filho BD et al (2016) Rhizobia symbionts of legume forages native to south brazil as promoters of cultivated grass growing. Int J Agric Biol 18(5)

    Google Scholar 

  • Maillet F, Poinsot V, André O, Puech-Pagès V, Haouy A, Gueunier M et al (2011) Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469(7328):58–63

    Article  CAS  PubMed  Google Scholar 

  • Mansouri H, Petit A, Oger P, Dessaux Y (2002) Engineered rhizosphere: the trophic bias generated by opine-producing plants is independent of the opine type, the soil origin, and the plant species. Appl Environ Microbiol 68(5):2562–2566

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marasco R, Rolli E, Vigani G, Borin S, Sorlini C, Ouzari H et al (2013) Are drought-resistance promoting bacteria cross-compatible with different plant models? Plant Signal Behav 8(10):e26741

    Article  PubMed  PubMed Central  Google Scholar 

  • Martens DA, Frankenberger WT (1993) Soil saccharide extraction and detection. Plant Soil 149(1):145–147

    Article  CAS  Google Scholar 

  • Martínez-Romero E, Wang ET, López-Merino A, Caballero-Mellado J, Rogel MA, Gándara B et al (2000) Ribosomal gene-based phylogenies on trial: the case of Rhizobium and related genera. Biol Plant Microb Interact 2:59–64

    Google Scholar 

  • Martiny AC (2019) High proportions of bacteria are culturable across major biomes. ISME J 13(8):2125–2128

    Article  PubMed  PubMed Central  Google Scholar 

  • Masalha J, Kosegarten H, Elmaci Ö, Mengel K (2000) The central role of microbial activity for iron acquisition in maize and sunflower. Biol Fertil Soil 30(5):433–439

    Article  CAS  Google Scholar 

  • Matiru VN, Dakora FD (2004) Potential use of rhizobial bacteria as promoters of plant growth for increased yield in landraces of African cereal crops. Afr J Biotechnol 3(1):1–7

    Article  CAS  Google Scholar 

  • Matiru VN, Dakora FD (2005a) Xylem transport and shoot accumulation of lumichrome, a newly recognized rhizobial signal, alters root respiration, stomatal conductance, leaf transpiration and photosynthetic rates in legumes and cereals. New Phytol 165(3):847–855

    Article  CAS  PubMed  Google Scholar 

  • Matiru VN, Dakora FD (2005b) The rhizosphere signal molecule lumichrome alters seedling development in both legumes and cereals. New Phytol 166(2):439–444

    Article  CAS  PubMed  Google Scholar 

  • Matiru VN, Jaffer MA, Dakora FD (2005) Rhizobial infection of African landraces of sorghum (Sorghum bicolor L.) and finger millet (Eleucine coracana L.) promotes plant growth and alters tissue nutrient concentration under axenic conditions. Symbiosis

    Google Scholar 

  • Mayak S, Tirosh T, Glick BR (2004) Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant physiol Biochem 42(6):565–572

    Article  CAS  PubMed  Google Scholar 

  • McCormick DB (1989) Two interconnected B vitamins: riboflavin and pyridoxine. Physiol Rev 69(4):1170–1198

    Article  CAS  PubMed  Google Scholar 

  • Mehboob I, Zahir ZA, Mahboob A, Shahzad SM, Jawad A, Arshad M (2008) Preliminary screening of Rhizobium isolates for improving growth of maize seedlings under axenic conditions. Soil Environ 27:64–71

    Google Scholar 

  • Mehboob I, Naveed M, Zahir ZA, Ashraf M (2012) Potential of rhizobia for sustainable production of non-legumes. In: Crop production for agricultural improvement. Springer, Dordrecht, pp 659–704

    Chapter  Google Scholar 

  • Menéndez E, Paço A (2020) Is the application of plant probiotic bacterial consortia always beneficial for plants? Exploring synergies between rhizobial and non-rhizobial bacteria and their effects on agro-economically valuable crops. Life 10(3):24

    Article  PubMed Central  Google Scholar 

  • Mia MAB, Shamsuddin ZH (2009) Enhanced emergence and vigor seedling production of rice through growth-promoting bacterial inoculation. Res J Seed Sci 2(4):96–104

    Article  Google Scholar 

  • Minamisawa K, Ogawa KI, Fukuhara H, Koga J (1996) Indolepyruvate pathway for indole-3-acetic acid biosynthesis in Bradyrhizobium elkanii. Plant Cell Physiol 37(4):449–453

    Article  CAS  Google Scholar 

  • Miransari M, Smith D (2009) Rhizobial lipo-chitooligosaccharides and gibberellins enhance barley (Hordeum vulgare L.) seed germination. Biotechnology 8(2):270–275

    Article  CAS  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(5):383–389

    Article  CAS  PubMed  Google Scholar 

  • Mongiardini EJ, Pérez-Giménez J, Althabegoiti MJ, Covelli J, Quelas JI, López-García SL, Lodeiro AR (2009) Overproduction of the rhizobial adhesin RapA1 increases competitiveness for nodulation. Soil Biol Biochem 41(9):2017–2020

    Article  CAS  Google Scholar 

  • Montecillo AD, Raymundo AK, Papa IA, Aquino GMB, Rosana ARR (2018) Complete genome sequence of Rhizobium sp. strain 11515TR, isolated from tomato rhizosphere in the Philippines. Microbiol Resour Announ 7(7):e00903–e00918

    Article  Google Scholar 

  • Montes-Grajales D, Esturau-Escofet N, Esquivel B, Martinez-Romero E (2019) Exo-metabolites of Phaseolus vulgaris-nodulating rhizobial strains. Metabolites 9(6):105

    Article  CAS  PubMed Central  Google Scholar 

  • Muthamilarasan M, Singh NK, Prasad M (2019) Multi-omics approaches for strategic improvement of stress tolerance in underutilized crop species: a climate change perspective. Adv Genet 103:1–38

    Article  CAS  PubMed  Google Scholar 

  • Nadeem SM, Zahir ZA, Naveed M, Arshad M (2007) Preliminary investigations on inducing salt tolerance in maize through inoculation with rhizobacteria containing ACC deaminase activity. Can J Microbiol 53(10):1141–1149

    Article  CAS  PubMed  Google Scholar 

  • Naidu VSGR, Panwar JDS, Annapurna K (2004) Effect of synthetic auxins and Azorhizobium caulinodans on growth and yield of rice. Indian J Microbiol 44:211–213

    CAS  Google Scholar 

  • Nautiyal CS (1997) A method for selection and characterization of rhizosphere-competent bacteria of chickpea. Curr Microbiol 34(1):12–17

    Article  CAS  PubMed  Google Scholar 

  • Neilands JB (1993) Siderophores. Arch Biochem Biophys 302(1):1–3

    Article  CAS  PubMed  Google Scholar 

  • Noel TC, Sheng C, Yost CK, Pharis RP, Hynes MF (1996) Rhizobium leguminosarum as a plant growth-promoting rhizobacterium: direct growth promotion of canola and lettuce. Can J Microbiol 42(3):279–283

    Article  CAS  PubMed  Google Scholar 

  • Nosheen S, Ajmal I, Song Y (2021) Microbes as biofertilizers, a potential approach for sustainable crop production. Sustainability 13(4):1868

    Article  Google Scholar 

  • O’Sullivan DJ, O’Gara F (1992) Traits of fluorescent Pseudomonas spp. involved in suppression of plant root pathogens. Microbiol Rev 56(4):662–676

    Article  PubMed  PubMed Central  Google Scholar 

  • Oberholster T, Vikram S, Cowan D, Valverde A (2018) Key microbial taxa in the rhizosphere of sorghum and sunflower grown in crop rotation. Sci Total Environ 624:530–539

    Article  CAS  PubMed  Google Scholar 

  • Op den Camp R, Streng A, De Mita S, Cao Q, Polone E, Liu W, Ammiraju JS, Kudrna D, Wing R, Untergasser A, Bisseling T (2011) LysM-type mycorrhizal receptor recruited for rhizobium symbiosis in nonlegume Parasponia. Science 331(6019):909–912

    Article  Google Scholar 

  • Op den Camp RH, Polone E, Fedorova E, Roelofsen W, Squartini A, Op den Camp HJ et al (2012) Nonlegume Parasponia andersonii deploys a broad Rhizobium host range strategy resulting in largely variable symbiotic effectiveness. Mol Plant Microbe Interact 25(7):954–963

    Article  Google Scholar 

  • Ormeno-Orrillo E, Servín-Garcidueñas LE, Rogel MA, González V, Peralta H, Mora J et al (2015) Taxonomy of rhizobia and agrobacteria from the Rhizobiaceae family in light of genomics. Syst Appl Microbiol 38(4):287–291

    Article  PubMed  Google Scholar 

  • Özkoç İ, Deliveli MH (2001) In vitro inhibition of the mycelial growth of some root rot fungi by Rhizobium leguminosarum biovar phaseoli isolates. Turkish J Biol 25(4):435–445

    Google Scholar 

  • Pandey P, Maheshwari DK (2007) Two-species microbial consortium for growth promotion of Cajanus cajan. Curr Sci 25:1137–1142

    Google Scholar 

  • Parveen S, Ghaffar A (1991) Effect of microbial antagonists in the control of root-rot of tomato. Pak J Bot 23(2):179–182

    Google Scholar 

  • Parveen S, Ehteshamul-Haque S, Ghaffar A (1993) Biological control of Meloidogyne javanica on tomato and okra in soil infested with Fusarium oxysporum. Pak J Nematol 11(2):151–156

    Google Scholar 

  • Paulitz TC, Bélanger RR (2001) Biological control in greenhouse systems. Annu Rev Phytopathol 39(1):103–133

    Article  CAS  PubMed  Google Scholar 

  • Peix A, Rivas-Boyero AA, Mateos PF, Rodriguez-Barrueco C, Martınez-Molina E, Velazquez E (2001) Growth promotion of chickpea and barley by a phosphate solubilizing strain of Mesorhizobium mediterraneum under growth chamber conditions. Soil Biol Biochem 33(1):103–110

    Article  CAS  Google Scholar 

  • Pena-Cabriales JJ, Alexander M (1983) Growth of Rhizobium in unamended soil. Soil Sci Soc Am J 47(1):81–84

    Article  Google Scholar 

  • Pena HB, Reyes I (2007) Nitrogen fixing bacteria and phosphate solubilizers isolated in lettuce (Lactuca sativa L.) and evaluated as plant growth promoters. Interciencia 32(8):560–565

    Google Scholar 

  • Peng S, Biswas JC, Ladha JK, Gyaneshwar P, Chen Y (2002) Influence of rhizobial inoculation on photosynthesis and grain yield of rice. Agron J 94(4):925–929

    Article  Google Scholar 

  • Peralta H, Mora Y, Salazar E, Encarnación S, Palacios R, Mora J (2004) Engineering the nifH promoter region and abolishing poly-β-hydroxybutyrate accumulation in Rhizobium etli enhance nitrogen fixation in symbiosis with Phaseolus vulgaris. Appl Environ Microbiol 70(6):3272–3281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pérez-Jaramillo JE, de Hollander M, Ramírez CA, Mendes R, Raaijmakers JM, Carrión VJ (2019) Deciphering rhizosphere microbiome assembly of wild and modern common bean (Phaseolus vulgaris) in native and agricultural soils from Colombia. Microbiome 7(1):1–16

    Article  Google Scholar 

  • Perrine FM, Prayitno J, Weinman JJ, Dazzo FB, Rolfe BG (2001) Rhizobium plasmids are involved in the inhibition or stimulation of rice growth and development. Funct Plant Biol 28(9):923–937

    Article  CAS  Google Scholar 

  • Perrine FM, Hocart CH, Hynes MF, Rolfe BG (2005) Plasmid-associated genes in the model micro-symbiont Sinorhizobium meliloti 1021 affect the growth and development of young rice seedlings. Environ Microbiol 7(11):1826–1838

    Article  CAS  PubMed  Google Scholar 

  • Perrine-Walker FM, Prayitno J, Rolfe BG, Weinman JJ, Hocart CH (2007) Infection process and the interaction of rice roots with rhizobia. J Exp Bot 58(12):3343–3350

    Article  CAS  PubMed  Google Scholar 

  • Perrine-Walker FM, Hynes MF, Rolfe BG, Hocart CH (2009) Strain competition and agar affect the interaction of rhizobia with rice. Can J Microbiol 55(10):1217–1223

    Article  CAS  PubMed  Google Scholar 

  • Phillips DA, Torrey JG (1970) Cytokinin production by Rhizobium japonicum. Physiol Plant 23(6):1057–1063

    Article  CAS  Google Scholar 

  • Phillips DA, Joseph CM, Yang GP, Martínez-Romero E, Sanborn JR, Volpin H (1999) Identification of lumichrome as a Sinorhizobium enhancer of alfalfa root respiration and shoot growth. Proc Natl Acad Sci U S A 96(22):12275–12280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Piromyou P, Songwattana P, Greetatorn T, Okubo T, Kakizaki KC, Prakamhang J et al (2015) The type III secretion system (T3SS) is a determinant for rice-endophyte colonization by non-photosynthetic Bradyrhizobium. Microb Environ 30(4):291–300

    Article  Google Scholar 

  • Plessner O, Klapatch T, Guerinot ML (1993) Siderophore utilization by Bradyrhizobium japonicum. Appl Environ Microbiol 59(5):1688–1690

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prayitno J, Stefaniak J, McIver J, Weinman JJ, Dazzo FB, Ladha JK et al (1999) Interactions of rice seedlings with bacteria isolated from rice roots. Funct Plant Biol 26(6):521–535

    Article  Google Scholar 

  • Prévost D, Saddiki S, Antoun H (2000) Growth and mineral nutrition of corn inoculated with effective strains of Bradyrhizobium japonicum. In: Proceedings of the 5th international PGPR workshop. Villa Carlos Paz, Córdoba, Argentina

    Google Scholar 

  • Qureshi MA, Shahzad H, Saeed MS, Ullah S, Ali MA, Mujeeb F, Anjum MA (2019) Relative potential of Rhizobium species to enhance the growth and yield attributes of cotton (Gossypium hirsutum L.). Eurasian J Soil Sci 8(2):159–166

    CAS  Google Scholar 

  • Raaijmakers JM, Paulitz TC, Steinberg C, Alabouvette C, Moënne-Loccoz Y (2009) The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil 321(1):341–361

    Article  CAS  Google Scholar 

  • Rao D, Mohanty S, Acharya C, Atoliya N (2018) Rhizobial taxonomy-current status. IUNFC Newslett 3:1–3

    Google Scholar 

  • Ray PK, Jana AK, Maitra DN, Saha MN, Chaudhury J, Saha S, Saha AR (2000) Fertilizer prescriptions on soil test basis for jute, rice and wheat in a Typic Ustochrept. J Indian Soc Soil Sci 48(1):79–84

    Google Scholar 

  • Reddy PM, Ladha JK, So RB, Hernandez RJ, Ramos MC, Angeles OR et al (1997) Rhizobial communication with rice roots: induction of phenotypic changes, mode of invasion and extent of colonization. Plant Soil 194(1):81–98

    Article  CAS  Google Scholar 

  • Reigh G, O’Connell M (1993) Siderophore-mediated iron transport correlates with the presence of specific iron-regulated proteins in the outer membrane of Rhizobium meliloti. J Bacteriol 175(1):94–102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reiter B, Bürgmann H, Burg K, Sessitsch A (2003) Endophytic nifH gene diversity in African sweet potato. Can J Microbiol 49(9):549–555

    Article  CAS  PubMed  Google Scholar 

  • Reitz M, Rudolph K, Schroder I, Hoffmann-Hergarten S, Hallmann J, Sikora R (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(8):3515–3518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Requena N, Jimenez I, Toro M, Barea JM (1997) Interactions between plant-growth-promoting rhizobacteria (PGPR), arbuscular mycorrhizal fungi and Rhizobium spp. in the rhizosphere of Anthyllis cytisoides, a model legume for revegetation in mediterranean semi-arid ecosystems. New Phytol 136(4):667–677

    Article  CAS  PubMed  Google Scholar 

  • Reyes VG, Schmidt EL (1979) Population densities of Rhizobium japonicum strain 123 estimated directly in soil and rhizospheres. Appl Environ Microbiol 37(5):854–858

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ridge RW, Bender GL, Rolfe BG (1992) Nodule-like structures induced on the roots of wheat seedlings by the addition of the synthetic auxin 2, 4-dichlorophenoxyacetic acid and the effects of microorganisms. Funct Plant Biol 19(5):481–492

    Article  CAS  Google Scholar 

  • Rodrigues Coelho MR, De Vos M, Carneiro NP, Marriel IE, Paiva E, Seldin L (2008) Diversity of nifH gene pools in the rhizosphere of two cultivars of sorghum (Sorghum bicolor) treated with contrasting levels of nitrogen fertilizer. FEMS Microbiol Lett 279(1):15–22

    Article  Google Scholar 

  • Rodrı́guez H, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17(4-5):319–339

    Article  PubMed  Google Scholar 

  • Roesch LFW, Camargo FA, Bento FM, Triplett EW (2008) Biodiversity of diazotrophic bacteria within the soil, root and stem of field-grown maize. Plant Soil 302(1):91–104

    Article  CAS  Google Scholar 

  • Rogers C, Oldroyd GE (2014) Synthetic biology approaches to engineering the nitrogen symbiosis in cereals. J Exp Bot 65(8):1939–1946

    Article  CAS  PubMed  Google Scholar 

  • Rojas-Jiménez K, Sohlenkamp C, Geiger O, Martínez-Romero E, Werner D, Vinuesa P (2005) A ClC chloride channel homolog and ornithine-containing membrane lipids of Rhizobium tropici CIAT899 are involved in symbiotic efficiency and acid tolerance. Mol Plant Microbe Interact 18(11):1175–1185

    Article  PubMed  Google Scholar 

  • Rolfe BG, Bender GL (1990) Evolving a Rhizobium for non-legume nodulation. In: Nitrogen fixation. Springer, Boston, MA, pp 779–780

    Chapter  Google Scholar 

  • Rout GR, Sahoo S (2005) Role of iron in plant growth and metabolism. Rev Agric Sci 3:1–24

    Google Scholar 

  • Sabry SR, Saleh SA, Batchelor CA, Jones J, Jotham J, Webster G et al (1997) Endophytic establishment of Azorhizobium caulinodans in wheat. Proc R Soc Lond B: Biol Sci 264(1380):341–346

    Google Scholar 

  • Şahin F, Çakmakçi R, Kantar F (2004) Sugar beet and barley yields in relation to inoculation with N2-fixing and phosphate solubilizing bacteria. Plant Soil 265(1):123–129

    Article  Google Scholar 

  • Saikia SP, Jain V (2007) Biological nitrogen fixation with non-legumes: an achievable target or a dogma? Curr Sci:317–322

    Google Scholar 

  • Savka MA, Dessaux Y, Oger P, Rossbach S (2002) Engineering bacterial competitiveness and persistence in the phytosphere. Mol Plant Microbe Interact 15(9):866–874

    Article  CAS  PubMed  Google Scholar 

  • Schloter M, Wiehe W, Assmus B, Steindl H, Becke H, Höflich G, Hartmann A (1997) Root colonization of different plants by plant-growth-promoting Rhizobium leguminosarum bv. trifolii R39 studied with monospecific polyclonal antisera. Appl Environ Microbiol 63(5):2038–2046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schwinghamer EA, Belkengren RP (1968) Inhibition of rhizobia by a strain of Rhizobium trifolii: Some properties of the antibiotic and of the strain. Arch Mikrobiol 64(2):130–145

    Article  CAS  PubMed  Google Scholar 

  • Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160(1):47–56

    Article  CAS  PubMed  Google Scholar 

  • Senthilkumar M, Madhaiyan M, Sundaram SP, Sangeetha H, Kannaiyan S (2008) Induction of endophytic colonization in rice (Oryza sativa L.) tissue culture plants by Azorhizobium caulinodans. Biotechnol Lett 30(8):1477–1487

    Article  CAS  PubMed  Google Scholar 

  • 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. Cv CO-43). Microbiol Res 164(1):92–104

    Article  CAS  PubMed  Google Scholar 

  • Servín-Garcidueñas LE, Guerrero G, Rogel-Hernández MA, Martínez-Romero E (2019) Genome sequence of Rhizobium jaguaris CCGE525T, a strain isolated from Calliandra grandiflora nodules from a rain forest in Mexico. Microbiol Resour Announ 8(9):e01584–e01518

    Article  Google Scholar 

  • Sessitsch A, Reiter B, Pfeifer U, Wilhelm E (2002) Cultivation-independent population analysis of bacterial endophytes in three potato varieties based on eubacterial and actinomycetes-specific PCR of 16S rRNA genes. FEMS Microbiol Ecol 39(1):23–32

    Article  CAS  PubMed  Google Scholar 

  • Shakhawat Hossain M, Mårtensson A (2008) Potential use of Rhizobium spp. to improve fitness of non-nitrogen-fixing plants. Acta Agric Scand Sect B Soil Plant Sci 58(4):352–358

    CAS  Google Scholar 

  • Shaukat SS, Siddiqui IA (2003) The influence of mineral and carbon sources on biological control of charcoal rot fungus, Macrophomina phaseolina by fluorescent pseudomonads in tomato. Lett Appl Microbiol 36(6):392–398

    Article  CAS  PubMed  Google Scholar 

  • Sheikh LI, Dawar S, Zaki MJ, Ghaffar A (2006) Efficacy of Bacillus thuringiensis and Rhizobium meliloti with nursery fertilizers in the control of root infecting fungi on mung bean and okra plants. Pak J Bot 38(2):465

    Google Scholar 

  • Shimshick EJ, Hebert RR (1979) Binding characteristics of N2-fixing bacteria to cereal roots. Appl Environ Microbiol 38(3):447–453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Siddiqui IA, Ehteshamul-Haq S, Zaki MJ, Ghaffar A (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 (Pak)

    Google Scholar 

  • Silva HSA, Romeiro RDS, Mounteer A (2003) Development of a root colonization bioassay for rapid screening of rhizobacteria for potential biocontrol agents. J Phytopathol 151(1):42–46

    Article  Google Scholar 

  • Silva FB, Winck B, Borges CS, Santos FL, Bataiolli RD, Backes T et al (2020) Native rhizobia from southern Brazilian grassland promote the growth of grasses. Rhizosphere 16:100240

    Article  Google Scholar 

  • Singh R, Kumar V, Sharma S, Behl RK, Singh BP, Narula N (2005) Performance and persistence of green fluorescent protein (gfp) marked Azotobacter chroococcum in sterilized and unsterilized wheat rhizospheric soil. J Appl Environ Biol 11:751–755

    CAS  Google Scholar 

  • Singh RK, Mishra RP, Jaiswal HK, Kumar V, Pandey SP, Rao SB, Annapurna K (2006) Isolation and identification of natural endophytic rhizobia from rice (Oryza sativa L.) through rDNA PCR-RFLP and sequence analysis. Curr Microbiol 52(5):345–349

    Article  CAS  PubMed  Google Scholar 

  • Singh A, Jain A, Sarma BK, Upadhyay RS, Singh HB (2014) Rhizosphere competent microbial consortium mediates rapid changes in phenolic profiles in chickpea during Sclerotium rolfsii infection. Microbiol Res 169(5-6):353–360

    Article  CAS  PubMed  Google Scholar 

  • Smith SE, Dickson S, Smith FA (2001) Nutrient transfer in arbuscular mycorrhizas: how are fungal and plant processes integrated? Funct Plant Biol 28(7):685–696

    Article  Google Scholar 

  • Smith DL, Prithiviraj B, Zhang F (2002) Rhizobial signals and control of plant growth. In: Nitrogen fixation: global perspectives. CABI Publishing, Wallingford, pp 327–330

    Google Scholar 

  • Somers E, Vanderleyden J, Srinivasan M (2004) Rhizosphere bacterial signalling: a love parade beneath our feet. Crit Rev Microbiol 30(4):205–240

    Article  CAS  PubMed  Google Scholar 

  • Spencer D, James EK, Ellis GJ, Shaw JE, Sprent JI (1994) Interaction between rhizobia and potato tissues. J Exp Bot 45(10):1475–1482

    Article  CAS  Google Scholar 

  • Staehelin C, Granado J, Müller J, Wiemken A, Mellor RB, Felix G, Boller T (1994) Perception of Rhizobium nodulation factors by tomato cells and inactivation by root chitinases. Proc Natl Acad Sci U S A 91(6):2196–2200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Steen AD, Crits-Christoph A, Carini P, DeAngelis KM, Fierer N, Lloyd KG, Cameron Thrash J (2019) High proportions of bacteria and archaea across most biomes remain uncultured. ISME J 12:3126–3130

    Article  Google Scholar 

  • Stevens JB, Carter RA, Hussain H, Carson KC, Dilworth MJ, Johnston AW (1999) The fhu genes of Rhizobium leguminosarum, specifying siderophore uptake proteins: fhuDCB are adjacent to a pseudogene version of fhuA. Microbiology 145(3):593–601

    Article  CAS  PubMed  Google Scholar 

  • Streeter JG (1994) Failure of inoculant rhizobia to overcome the dominance of indigenous strains for nodule formation. Can J Microbiol 40(7):513–522

    Article  Google Scholar 

  • Streng A, op den Camp R, Bisseling T, Geurts R (2011) Evolutionary origin of Rhizobium Nod factor signaling. Plant Signal Behav 6(10):1510–1514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suárez R, Wong A, Ramírez M, Barraza A, Orozco MDC, Cevallos MA et al (2008) Improvement of drought tolerance and grain yield in common bean by overexpressing trehalose-6-phosphate synthase in rhizobia. Mol Plant Microbe Interact 21(7):958–966

    Article  PubMed  Google Scholar 

  • Sullivan JT, Trzebiatowski JR, Cruickshank RW, Gouzy J, Brown SD, Elliot RM et al (2002) Comparative sequence analysis of the symbiosis island of Mesorhizobium loti strain R7A. J Bacteriol 184(11):3086–3095

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sytsma KJ, Morawetz J, Pires JC, Nepokroeff M, Conti E, Zjhra M et al (2002) Urticalean rosids: circumscription, rosid ancestry, and phylogenetics based on rbcL, trnL-F, and ndhF sequences. Am J Bot 89(9):1531–1546

    Article  CAS  PubMed  Google Scholar 

  • Terakado-Tonooka J, Ohwaki Y, Yamakawa H, Tanaka F, Yoneyama T, Fujihara S (2008) Expressed nifH genes of endophytic bacteria detected in field-grown sweet potatoes (Ipomoea batatas L.). Microb Environ 23(1):89–93

    Article  Google Scholar 

  • Thaweenut N, Hachisuka Y, Ando S, Yanagisawa S, Yoneyama T (2011) Two seasons’ study on nifH gene expression and nitrogen fixation by diazotrophic endophytes in sugarcane (Saccharum spp. hybrids): expression of nifH genes similar to those of rhizobia. Plant Soil 338(1):435–449

    Article  CAS  Google Scholar 

  • Thijs S, Sillen W, Weyens N, Vangronsveld J (2017) Phytoremediation: state-of-the-art and a key role for the plant microbiome in future trends and research prospects. Int J Phytoremed 19(1):23–38

    Article  CAS  Google Scholar 

  • Trinick MJ, Galbraith J (1980) The Rhizobium requirements of the non-legume Parasponia in relationship to the cross-inoculation group concept of legumes. New Phytol 86(1):17–26

    Article  Google Scholar 

  • Trinick MJ, Hadobas PA (1989) Biology of the Pavasponia-Bradyrhizobium symbiosis. In: Nitrogen fixation with non-legumes. Springer, Dordrecht, pp 25–33

    Chapter  Google Scholar 

  • Trinick MJ, Hadobas PA (1995) Formation of nodular structures on the non-legumes Brassica napus, B. campestris, B. juncea and Arabidopsis thaliana with Bradyrhizobium and Rhizobium isolated from Parasponia spp. or legumes grown in tropical soils. Plant Soil 172(2):207–219

    Article  CAS  Google Scholar 

  • Triplett EW, Breil BT, Splitter GA (1994) Expression of tfx and sensitivity to the rhizobial peptide antibiotic trifolitoxin in a taxonomically distinct group of alpha-proteobacteria including the animal pathogen Brucella abortus. Appl Environ Microbiol 60(11):4163–4166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tu JC (1978) Protection of soybean from severe Phytophthora root rot by Rhizobium. Physiol Plant Pathol 12(2):233–240

    Article  Google Scholar 

  • Tu JC (1979) Evidence of differential tolerance among some root rot fungi to rhizobial parasitism in vitro. Physiol Plant Pathol 14:171–177

    Article  Google Scholar 

  • Tulumello J, Chabert N, Rodriguez J, Long J, Nalin R, Achouak W, Heulin T (2021) Rhizobium alamii improves water stress tolerance in a non-legume. Sci Total Environ 797:148895

    Article  CAS  PubMed  Google Scholar 

  • Turner TR, James EK, Poole PS (2013) The plant microbiome. Genome Biol 14:209

    Article  PubMed  PubMed Central  Google Scholar 

  • Van Loon LC (2007) Plant responses to plant growth-promoting rhizobacteria. In: New perspectives and approaches in plant growth-promoting. Rhizobacteria research, pp 243–254

    Chapter  Google Scholar 

  • Van Dillewijn P, Soto MJ, Villadas PJ, Toro N (2001) Construction and environmental release of a Sinorhizobium meliloti strain genetically modified to be more competitive for alfalfa nodulation. Appl Environ Microbiol 67(9):3860–3865

    Article  PubMed  PubMed Central  Google Scholar 

  • van Velzen R, Holmer R, Bu F, Rutten L, van Zeijl A, Liu W et al (2018) Comparative genomics of the nonlegume Parasponia reveals insights into evolution of nitrogen-fixing Rhizobium symbioses. Proc Natl Acad Sci U S A 115(20):E4700–E4709

    PubMed  PubMed Central  Google Scholar 

  • Vargas LK, Lisboa BB, Schlindwein G, Granada CE, Giongo A, Beneduzi A, Passaglia LMP (2009) Occurrence of plant growth-promoting traits in clover-nodulating rhizobia strains isolated from different soils in Rio Grande do Sul state. Rev Brasil Ciên Solo 33(5):1227–1235

    Article  Google Scholar 

  • Velázquez E, Peix A, Zurdo-Piñiro JL, Palomo JL, Mateos PF, Rivas R et al (2005) The coexistence of symbiosis and pathogenicity-determining genes in Rhizobium rhizogenes strains enables them to induce nodules and tumors or hairy roots in plants. Mol Plant Microbe Interact 18(12):1325–1332

    Article  PubMed  Google Scholar 

  • Velázquez E, Carro L, Flores-Félix JD, Menéndez E, Ramírez-Bahena MH, Peix A (2019) Bacteria-inducing legume nodules involved in the improvement of plant growth, health and nutrition. In: Microbiome in plant health and disease. Springer, Singapore, pp 79–104

    Chapter  Google Scholar 

  • Vences-Guzmán MÁ, Guan Z, Ormeño-Orrillo E, González-Silva N, López-Lara IM, Martínez-Romero E et al (2011) Hydroxylated ornithine lipids increase stress tolerance in Rhizobium tropici CIAT899. Mol Microbiol 79(6):1496–1514

    Article  PubMed  PubMed Central  Google Scholar 

  • Venieraki A, Dimou M, Vezyri E, Kefalogianni I, Argyris N, Liara G, Pergalis P, Chatzipavlidis I, Katinakis P (2011) Characterization of nitrogen-fixing bacteria isolated from field-grown barley, oat, and wheat. J Microbiol 49(4):525–534

    Article  CAS  PubMed  Google Scholar 

  • Vergine M, Meyer JB, Cardinale M, Sabella E, Hartmann M, Cherubini P et al (2019) The Xylella fastidiosa-resistant olive cultivar “Leccino” has stable endophytic microbiota during the olive quick decline syndrome (OQDS). Pathogens 9(1):35

    Article  PubMed Central  Google Scholar 

  • Verma SC, Singh A, Chowdhury SP, Tripathi AK (2004) Endophytic colonization ability of two deep-water rice endophytes, Pantoea sp. and Ochrobactrum sp. using green fluorescent protein reporter. Biotechnol Lett 26(5):425–429

    Article  CAS  PubMed  Google Scholar 

  • Vessey JK (2003) Plant growth-promoting rhizobacteria as biofertilizers. Plant Soil 255(2):571–586

    Article  CAS  Google Scholar 

  • Volpiano CG, Lisboa BB, Granada CE, São José JFB, de Oliveira AMR, Beneduzi A (2019) Microbiome in plant health and disease

    Google Scholar 

  • Walsh C, Pascal RA Jr, Johnston M, Raines R, Dikshit D, Krantz A, Honma M (1981) Mechanistic studies on the pyridoxal phosphate enzyme 1-aminocyclopropane-1-carboxylate deaminase from Pseudomonas sp. Biochemistry 20(26):7509–7519

    Article  CAS  PubMed  Google Scholar 

  • Walters WA, Jin Z, Youngblut N, Wallace JG, Sutter J, Zhang W et al (2018) Large-scale replicated field study of maize rhizosphere identifies heritable microbes. Proc Natl Acad Sci U S A 115(28):7368–7373

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang C, Knill E, Glick BR, Défago G (2000) Effect of transferring 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase genes into Pseudomonas fluorescens strain CHA0 and its gacA derivative CHA96 on their growth-promoting and disease-suppressive capacities. Can J Microbiol 46(10):898–907

    Article  CAS  PubMed  Google Scholar 

  • Wang M, Eyre AW, Thon MR, Oh Y, Dean RA (2020) Dynamic changes in the microbiome of rice during shoot and root growth derived from seeds. Front Microbiol 2183

    Google Scholar 

  • Webster G, Gough C, Vasse J, Batchelor CA, O’callaghan KJ, Kothari SL et al (1997) Interactions of rhizobia with rice and wheat. In: Opportunities for biological nitrogen fixation in rice and other non-legumes. Springer, Dordrecht, pp 115–122

    Chapter  Google Scholar 

  • Weller DM, Raaijmakers JM, Gardener BBM, Thomashow LS (2002) Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annu Rev Phytopathol 40(1):309–348

    Article  CAS  PubMed  Google Scholar 

  • Werner D (1992) Symbiosis of plants and microbes (No. SB731 W49). Chapman & Hall, London

    Google Scholar 

  • Weyens N, van der Lelie D, Taghavi S, Vangronsveld J (2009) Phytoremediation: plant–endophyte partnerships take the challenge. Curr Opin Biotechnol 20(2):248–254

    Article  CAS  PubMed  Google Scholar 

  • Wiehe W, Höflich G (1995) Survival of plant growth-promoting rhizosphere bacteria in the rhizosphere of different crops and migration to non-inoculated plants under field conditions in north-east Germany. Microbiol Res 150(2):201–206

    Article  Google Scholar 

  • Wiehe W, Hecht-Buchholz CH, Hoflich G (1994) Electron microscopic investigations on root colonization of Lupinus albus and Pisum sativum with two associative plant growth-promoting rhizobacteria, Pseudomonas fluorescens and Rhizobium leguminosarum bv. trifolii. Symbiosis

    Google Scholar 

  • Wu Q, Peng X, Yang M, Zhang W, Dazzo FB, Uphoff N et al (2018) Rhizobia promote the growth of rice shoots by targeting cell signaling, division and expansion. Plant Mol Biol 97(6):507–523

    Article  CAS  PubMed  Google Scholar 

  • Xie ZP, Staehelin C, Vierheilig H, Wiemken A, Jabbouri S, Broughton WJ et al (1995) Rhizobial nodulation factors stimulate mycorrhizal colonization of nodulating and nonnodulating soybeans. Plant Physiol 108(4):1519–1525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu H, Yang Y, Tian Y, Xu R, Zhong Y, Liao H (2020) Rhizobium inoculation drives the shifting of rhizosphere fungal community in a host genotype-dependent manner. Front Microbiol 3135

    Google Scholar 

  • Yang SF, Hoffman NE (1984) Ethylene biosynthesis and its regulation in higher plants. Annu rev Plant Physiol 35(1):155–189

    Article  CAS  Google Scholar 

  • Yang G, Bhuvaneswari TV, Joseph CM, King MD, Phillips DA (2002) Roles for riboflavin in the Sinorhizobium-alfalfa association. Mol Plant Microbe Interact 15(5):456–462

    Article  CAS  PubMed  Google Scholar 

  • Yanni YG, Rizk RY, Corich V, Squartini A, Ninke K, Philip-Hollingsworth S et al (1997) Natural endophytic association between Rhizobium leguminosarum bv. trifolii and rice roots and assessment of its potential to promote rice growth. In: Opportunities for biological nitrogen fixation in rice and other non-legumes. Springer, Dordrecht, pp 99–114

    Chapter  Google Scholar 

  • Yanni YG, Rizk RY, Abd El-Fattah FK, Squartini A, Corich V, Giacomini A et al (2001) The beneficial plant growth-promoting association of Rhizobium leguminosarum bv. trifolii with rice roots. Funct Plant Biol 28(9):845–870

    Article  CAS  Google Scholar 

  • Yardin MR, Kennedy IR, Thies JE (2000) Development of high-quality carrier materials for field delivery of key microorganisms used as bio-fertilisers and bio-pesticides. Radiat Phys Chem 57(3–6):565–568

    Article  CAS  Google Scholar 

  • Yeoh YK, Dennis PG, Paungfoo-Lonhienne C, Weber L, Brackin R, Ragan MA et al (2017) Evolutionary conservation of a core root microbiome across plant phyla along a tropical soil chronosequence. Nat Commun 8(1):1–9

    Article  CAS  Google Scholar 

  • Yoneyama T, Terakado-Tonooka J, Minamisawa K (2017) Exploration of bacterial N2-fixation systems in association with soil-grown sugarcane, sweet potato, and paddy rice: a review and synthesis. Soil Sci Plant Nutr 63(6):578–590

    Article  CAS  Google Scholar 

  • Yoneyama T, Terakado-Tonooka J, Bao Z, Minamisawa K (2019) Molecular analyses of the distribution and function of diazotrophic rhizobia and methanotrophs in the tissues and rhizosphere of non-leguminous plants. Plants 8(10):408

    Article  CAS  PubMed Central  Google Scholar 

  • Yu D, Kennedy IR (1995) Nitrogenase activity (C2H2 reduction) of Azorhizobium in 2, 4-D-induced root structures of wheat. Soil Biol Biochem 27(4-5):459–462

    Article  Google Scholar 

  • Zahir ZA, Arshad M (2004) Perspectives in agriculture. Adv Agron 81:97–98

    Article  CAS  Google Scholar 

  • Zahir ZA, Munir A, Asghar HN, Shaharoona B, Arshad M (2008) Effectiveness of rhizobacteria containing ACC deaminase for growth promotion of peas (Pisum sativum) under drought conditions. J Microbiol Biotechnol 18(5):958–963

    CAS  PubMed  Google Scholar 

  • Zahir ZA, Ghani U, Naveed M, Nadeem SM, Asghar HN (2009) Comparative effectiveness of Pseudomonas and Serratia sp. containing ACC-deaminase for improving growth and yield of wheat (Triticum aestivum L.) under salt-stressed conditions. Arch Microbiol 191(5):415–424

    Article  CAS  PubMed  Google Scholar 

  • Zheng Y, Liang J, Zhao DL, Meng C, Xu ZC, Xie ZH, Zhang CS (2020) The root nodule microbiome of cultivated and wild halophytic legumes showed similar diversity but distinct community structure in Yellow River Delta saline soils. Microorganisms 8(2):207

    Article  CAS  PubMed Central  Google Scholar 

  • Ziaf K, Latif U, Amjad M, Shabir MZ, Asghar W, Ahmed S et al (2016) Combined use of microbial and synthetic amendments can improve radish (Raphanus sativus) yield. J Environ Agric Sci 6:10–15

    Google Scholar 

Download references

Acknowledgment

SD, ND and PP are grateful to Department of Biotechnology, Ministry of Science and Technology, Govt of India, for financial support. 

Conflict of interest

Author(s) declares no conflict of interest.

Author information

Authors and Affiliations

  1. Department of Microbiology, Assam University, Silchar, India

    Sourav Debnath, Nandita Das & Piyush Pandey

  2. Department of Botany and Microbiology, Gurukula Kangri (Deemed to be University), Haridwar, Uttarakhand, India

    Dinesh Kumar Maheshwari

Authors
  1. Sourav Debnath
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nandita Das
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dinesh Kumar Maheshwari
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Piyush Pandey
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Department of Botany and Microbiology, Gurukula Kangri (Deemed to be University), Haridwar, Uttarakhand, India

    Dinesh Kumar Maheshwari

  2. Uttarakhand State Council for Science and Technology (UCOST), Dehradun, Uttarakhand, India

    Rajendra Dobhal

  3. Department of Microbiology, School of Allied Health Sciences, MVN University, Palwal, Haryana, India

    Shrivardhan Dheeman

Rights and permissions

Reprints and permissions

Copyright information

© 2022 The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Debnath, S., Das, N., Maheshwari, D.K., Pandey, P. (2022). Interactions of Rhizobia with Nonleguminous Plants: A Molecular Ecology Perspective for Enhanced Plant Growth. In: Maheshwari, D.K., Dobhal, R., Dheeman, S. (eds) Nitrogen Fixing Bacteria: Sustainable Growth of Non-legumes. Microorganisms for Sustainability, vol 36. Springer, Singapore. https://doi.org/10.1007/978-981-19-4906-7_3

Download citation

Publish with us

Policies and ethics

Search

Navigation