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An Insight into the Legume–Rhizobium Interaction

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Abstract

Active forms of nitrogen are limiting in soil, but the legume–Rhizobium interaction overcomes this barrier by biological nitrogen fixation and lessens the usage of fertilizers. An understanding exists between the two partners for symbiotic association to share their resources without either one becoming dominant. Certain compounds released by the host legume plants into the rhizosphere attract the rhizobia and activate the expression of rhizobial nod genes that in turn leads to the production and secretion of strain-specific NFs. NF signalling cascade and events of cell divisions in cortex and pericycle and bacterial infection occur in an orchestrated manner and give rise to a nodule. The nodule organogenesis can be studied under nodule formation and bacterial invasion. Depending on the persistence of meristem, nodules formed can be determinate or indeterminate, but ultimately it is the host plant species that determine the type of nodule formed. More than 90 % of arable land experience one or other kind of stress. Stress conditions affect the host plant, rhizobium and also the interaction between the two.

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References

  • Aarons SR, Graham PH (1991) Response of Rhizobium leguminosarum bv phaseoli to acidity. Plant Soil 134:145–151

    CAS  Google Scholar 

  • Andrés JA, Rovera M, Guiñazú LB, Pastor NA, Rosas SB (2012) Interactions between legumes and rhizobia under stress conditions. In: Maheshwari DK (ed) Bacteria in agrobiology: stress management. Springer, Berlin

    Google Scholar 

  • Andriankaja A, Boisson-Dernier A, Frances L, Sauviac L, Jauneau A, Barker DG, de Carvalho-Niebel F (2007) AP2-ERF transcription factors mediate nod factor-dependent MtENOD11 activation in root hairs via a novel cis-regulatory motif. Plant Cell 19:2866–2885

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ané JM, Kiss GB, Riely BK, Penmetsa RV, Oldroyd GE, Ayax C, Lévy J, Debellé F, Baek JM, Kalo P, Rosenberg C, Roe BA, Long SR, Dénarié J, Cook DR (2004) Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science 303:1364–1367

    Article  PubMed  CAS  Google Scholar 

  • Aranjuelo I, Irigoyen JJ, Sánchez-Díaz, M (2007). Effect of elevated temperature and water availability on CO2 exchange and nitrogen fixation of nodulated alfalfa plants. Environ Exp Bot 59(2):99–108

    Google Scholar 

  • Arrighi JF, Barre A, Ben Amor B, Bersoult A, Soriano LC, Mirabella R, de Carvalho-Niebel F, Journet EP, Ghérardi M, Huguet T, Geurts R, Dénarié J, Rougé P, Gough C (2006) The Medicago truncatula Lysine motif-receptor-like kinase gene family includes NFP and new nodule-expressed genes. Plant Physiol 142(1):265–279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Azooz MM, Ahmad P (eds) (2015) Legumes under environmental stress: yield, improvement and adaptations. John Wiley & Sons, Hoboken

    Google Scholar 

  • Bederska M, Borucki W, Znojek E (2012) Movement of fluorescent dyes Lucifer Yellow (LYCH) and carboxyfluorescein (CF) in Medicago truncatula Gaertn. roots and root nodules. Symbiosis 58:183–190

    Article  PubMed  CAS  Google Scholar 

  • Bhalerao SA, Prabhu DV (2013) Aluminium toxicity in plants: a review. J Appl Chem 2:447–474

    CAS  Google Scholar 

  • Bhat UR, Carlson RW (1992) Chemical characterization of pH-dependent structural epitopes of lipopolysaccharides from Rhizobium leguminosarum biovar phaseoli. J Bacteriol 174(7):2230–2235

    CAS  PubMed  PubMed Central  Google Scholar 

  • Biswas B, Chan PK, Gresshoff PM (2009) A novel ABA insensitive mutant of Lotus japonicus with a wilty phenotype displays unaltered nodulation regulation. Mol Plant 2:487–499

    Article  CAS  PubMed  Google Scholar 

  • Bond L (1948) Origin and developmental morphology of root nodules of Pisum sativum. Bot Gaz 109(4):411–434

    Article  Google Scholar 

  • Bordeleau LM, Prevost D (1994) Nodulation and nitrogen fixation in extreme environments. Plant Soil 161:115–125

    Article  CAS  Google Scholar 

  • Borisov AY, Madsen LH, Tsyganov VE, Umehara Y, Voroshilova VA, Batagov AO, Sandal N, Mortensen A, Schauser L, Ellis N, Tikhonovich IA, Stougaard J (2003) The sym35 gene required for root nodule development in pea is an ortholog of NIN from Lotus japonicus. Plant Physiol 131:1009–1017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Botsford JL, Lewis TA (1990) Osmoregulation in Rhizobium meliloti: production of glutamic acid in response to osmotic stress. Appl Environ Microbiol 56(2):488–494

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brown SM, Walsh KB (1994) Anatomy of the legume nodule cortex with respect to nodule permeability. Aust J Plant Physiol 21:49–68

    Article  Google Scholar 

  • Cannon SB et al (2006) Legume genome evolution viewed through the Medicago truncatula and Lotus japonicus genomes. Proc Natl Acad Sci U S A 103(40):14959–14964

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cardenas L, Vidali L, Dominguez J, Perez H, Sanchez F, Hepler PK, Quinto C (1998) Rearrangement of actin microfilaments in plant root hairs responding to Rhizobium etli nodulation signals. Plant Physiol 116(3):871–877

    Article  CAS  PubMed Central  Google Scholar 

  • Catoira R, Galera C, de Billy F, Penmetsa RV, Journet EP, Maillet F, Rosenberg C, Cook D, Gough C, Denarie J (2000) Four genes of Medicago truncatula controlling components of a nod factor transduction pathway. Plant Cell 12:1647–1665

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cook D (2000) Medicago truncatula—a model in the making! Curr Opin Plant Biol 2:301–304

    Article  Google Scholar 

  • Cooper JE (2007) Early interactions between legumes and rhizobia: disclosing complexity in a molecular dialogue. J Appl Microbiol 103:1355–1365

    Article  CAS  PubMed  Google Scholar 

  • Csonka LN, Hanson AD (1991) Prokaryotic osmoregulation: genetics and physiology. Annu Rev Microbiol 45:569–606

    Article  CAS  PubMed  Google Scholar 

  • D’Souza-Ault MR, Smith LT, Smith GM (1993) Roles of N-acetylglutaminylglutamine amide and glycine betaine in adaptation of Pseudomonas aeruginosa to osmotic stress. Appl Environ Microbiol 59(2):473–478

    PubMed  PubMed Central  Google Scholar 

  • de Ruijter N, Rook M, Bisseling T, Emons A (1998) Lipochitooligosaccharides re-initiate root hair tip growth in Vicia sativa with high calcium and spectrin-like antigen at the tip. Plant J 13:341–350

    Article  Google Scholar 

  • Ding YL, Oldroyd GE (2009) Positioning the nodule, the hormone dictum. Plant Signal Behav 4:89–93

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ding YL, Kalo P, Yendrek C, Sun J, Liang Y, Marsh JF, Harris JM, Oldroyd GE (2008) Abscisic acid coordinates Nod factor and cytokinin signaling during the regulation of nodulation in Medicago truncatula. Plant Cell 20:2681–2695

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dixon R, Kahn D (2004) Genetic regulation of biological nitrogen fixation. Nat Rev Microbiol 2:621–631

    Article  CAS  PubMed  Google Scholar 

  • Dogra T, Priyadarshini A, Kumar A, Singh NK (2013) Identification of genes involved in salt tolerance and symbiotic nitrogen fixation in chickpea rhizobium Mesorhizobium ciceri Ca181. Symbiosis 61(3):135–143

    Article  CAS  Google Scholar 

  • Felle HH, Kondorosi E, Kondorosi A, Schultze M (1999) Elevation of the cytosolic free [Ca2+] is indispensable for the transduction of the nod factor signal in alfalfa. Plant Physiol 121:273–279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferguson BJ, Indrasumunar A, Hayashi S, Lin MH, Lin YH, Reid DE, Gresshoff PM (2010) Molecular analysis of legume nodule development and autoregulation. J Integr Plant Biol 52(1):61–76

    Article  CAS  PubMed  Google Scholar 

  • Ferreira PAA, Bomfeti CA, Soares BL, de Souza Moreira FM (2012). Efficient nitrogen-fixing Rhizobium strains isolated from amazonian soils are highly tolerant to acidity and aluminium. World J Microbiol Biotechnol 28: 1947–1959.

    Article  CAS  Google Scholar 

  • Fischer H-M (1994) Genetic regulation of nitrogen fixation in Rhizobia. Microbiol Rev 58:352–386

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fliegmann J, Bono J (2015) Lipo-chitooligosaccharidic nodulation factors and their perception by plant receptors. Glycoconj J 32:455–464

    Article  CAS  PubMed  Google Scholar 

  • Ford CW (1984) Accumulation of low molecular weight solutes in water stressed tropical legumes. Phytochemistry 23:1007–1015

    Article  CAS  Google Scholar 

  • Fougère F, Le-Rudulier D, Streeter JG (1991) Effects of salt stress on amino acid, organic acid, and carbohydrate composition of roots, bacteroids and cytosol of alfalfa (Medicago sativa L.). Plant Physiol 96:1228–1236

    Article  PubMed  PubMed Central  Google Scholar 

  • Franssen HJ, Vijn I, Yang WC, Bisseling T (1992) Developmental aspects of the Rhizobium-legume symbiosis. Plant Mol Biol 19(1):89–107

    Article  CAS  PubMed  Google Scholar 

  • Frazer HL (1942) The occurrence of endodermis in leguminous root nodules and its effect on nodule function. Proc R Soc Edinb B 61:328–343

    Google Scholar 

  • Fujihara S, Yoneyama T (1993) Effects of pH and osmotic stress on cellular polyamine contents in the soybean rhizobia Rhizobium fredii P220 and Bradyrhizobium japonicum A1017. Appl Environ Microbiol 59:1104–1109

    CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ghittoni NE, Bueno MA (1995) Peanut rhizobia under salt stress: role of trehalose accumulation in strain ATCC 514466. Can J Microbiol 41:1021–1030

    Article  CAS  Google Scholar 

  • Gibson KE, Kobayashi H, Walker GC (2008) Molecular determinants of a symbiotic chronic infection. Annu Rev Genet 42:413–441

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gleason C, Chaudhuri S, Yang TB, Munoz A, Poovaiah BW, Oldroyd GE (2006) Nodulation independent of rhizobia induced by a calcium-activated kinase lacking autoinhibition. Nature 441:1149–1152

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez-Rizzo S, Crespi M, Frugier F (2006) The Medicago truncatula CRE1 cytokinin receptor regulates lateral root development and early symbiotic interaction with Sinorhizobium meliloti. Plant Cell 18:2680–2693

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gordon AJ, Thomas BJ, Reynolds PHS (1992) Localization of sucrose synthase in soybean root nodules. New Phytol 122:35–44

    Article  CAS  Google Scholar 

  • Gouffi K, Pica N, Pichereau V, Blanco C (1999). Disaccharides as a new class of nonaccumulated osmoprotectants for Sinorhizobium meliloti. Appl Environ Microbiol 65:1491–1500.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Graham PH, Vance CP (2003) Legumes: Importance and constraints to greater use. Plant Physiol 131:872–877

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Graham PH, Draeger K, Ferrey ML, Conroy MJ, Hammer BE, Martinez E, Naarons SR, Quinto C (1994) Acid pH tolerance in strains of Rhizobium and Bradyrhizobium tolerance of Rhizobium tropici UMR1899. Can J Microbiol 40:198–207

    Article  CAS  Google Scholar 

  • Gust AA, Willmann R, Desaki Y, Grabherr HM (2012) Plant LysM proteins: modules mediating symbiosis and immunity. Trends Plant Sci 17(8):495–502

    Article  CAS  PubMed  Google Scholar 

  • Haeze WD, Holsters M (2002) Nod factor structures, responses, and perception during initiation of nodule development. Glycobiology 12(6):9R–105R

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Heckmann AB, Lombardo F, Miwa H, Perry JA, Bunnewell S, Parniske M, Wang TL, Downie JA (2006) Lotus japonicus nodulation requires two GRAS domain regulators, one of which is functionally conserved in a non-legume. Plant Physiol 142:1739–1750

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hepler PK, Vidali L, Cheung AY (2001) Polarized cell growth in higher plants. Annu Rev Cell Dev Biol 17:159–187

    Article  CAS  PubMed  Google Scholar 

  • Hirsch AM (1992) Developmental biology of legume nodulation. New Phytol 122:211–237

    Article  Google Scholar 

  • Hirsch AM (1999) Role of lectins (and rhizobial exopolysaccharides) in legume nodulation. Curr Opin Plant Biol 2:320–326

    Article  CAS  PubMed  Google Scholar 

  • Hirsch S, Kim J, Munoz A, Heckmann AB, Downie JA, Oldroyd GE (2009) GRAS proteins form a DNA binding complex to induce gene expression during nodulation signaling in Medicago truncatula. Plant Cell 21:545–557

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hungria M, Franco AA (1993) Effects of high temperature on nodulation and nitrogen fixation by Phaseolus vulgaris L. Plant Soil 149(1):95–102

    Article  CAS  Google Scholar 

  • Imaizumi-Anraku H, Takeda N, Kawaguchi M, Parniske M, Hayashi M, Kawasaki S (2005) Host genes involved in activation and perception of calcium spiking. Plant Cell Physiol 46:S5–S5

    Google Scholar 

  • Iwanami Y (1956) Protoplasmic movement in pollen grains and pollen tubes. Phytomorphology 6:288–295

    Google Scholar 

  • Jenkins MB, Virginia RA, Jarrell WM (1989) Ecology of fast-growing and slow-growing mesquite-nodulating rhizobia in Chihuahuan and Sonoron Desert ecosystems. Soil Sci Soc Am J 53(2):543–549

    Article  Google Scholar 

  • Jjemba PK (2001) The interaction of protozoa with their potential prey bacteria in the rhizosphere. J Eukaryot Microbiol 48:320–324

    Article  CAS  PubMed  Google Scholar 

  • Jousset A, Lara E, Wall LG, Valverde C (2006) Secondary metabolites help biocontrol strain Pseudomonas fluorescens CHA0 to escape protozoan grazing. Appl Environ Microbiol 72:7083–90

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaló P, Gleason C, Edwards A, Marsh J, Mitra RM, Hirsch S, Jakab J, Sims S, Long SR, Rogers J, Kiss GB, Downie JA, Oldroyd GE (2005) Nodulation signaling in legumes requires NSP2, a MEMBER of the GRAS family of transcriptional regulators. Science 308:1786–1789

    Article  PubMed  CAS  Google Scholar 

  • Kanamori N, Madsen LH, Radutoiu S, Frantescu M, Quistgaard EM, Miwa H, Downie JA, James EK, Felle HH, Haaning LL, Jensen TH, Sato S, Nakamura Y, Tabata S, Sandal N, Stougaard J (2006) A nucleoporin is required for induction of Ca2+ spiking in legume nodule development and essential for rhizobial and fungal symbiosis. Proc Natl Acad Sci U S A 103:359–364

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kapuya JA, Barendse GWM, Linskens HF (1985) Water stress tolerance and proline accumulation in Phaseolus vulgaris. Acta Bot Neerl 34:295–300

    Article  Google Scholar 

  • Ketelaar T, Emons AMC (2001) The cytoskeleton in plant cell growth: lessons from root hairs. New Phytol 152:409–418

    Article  CAS  Google Scholar 

  • Kochian LV, Piñeros MA, Hoekenga OA (2005) The physiology, genetics and molecular biology of plant aluminum resistance and toxicity. Plant Soil 274:175–195

    Article  CAS  Google Scholar 

  • Kropf DL, Bisgrovet SR, Hable WE (1998). Cytoskeletal control of polar growth in plant cells. Curr Opin Cell Biol 10:117–122.

    Article  CAS  PubMed  Google Scholar 

  • Latef AAHA, Ahmad P (2015) Legumes and breeding under abiotic stress: an overview. In: Azooz MM, Ahmad P (eds) Legumes under environmental stress: yield, improvement and adaptations. John Wiley & Sons, Hoboken

    Google Scholar 

  • Latrach L, Farissi M, Mouradi M, Makoudi B, Bouizgaren A, Ghoulam C (2014) Growth and nodulation of alfalfa-rhizobia symbiosis under salinity: electrolyte leakage, stomatal conductance, and chlorophyll fluorescence. Turk J Agric For 38(3):320–326

    Article  Google Scholar 

  • Lavin M, Herendeen PS, Wojciechowski MF (2005) Evolutionary rates analysis of Leguminosae implicates a rapid diversification of lineages during the tertiary. Syst Biol 54:574–594

    Article  Google Scholar 

  • Lévy J, Bres C, Geurts R, Chalhoub B, Kulikova O, Duc G, Journet EP, Ané JM, Lauber E, Bisseling T, Dénarié J, Rosenberg C, Debellé F (2004) A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303:1361–1364

    Article  PubMed  CAS  Google Scholar 

  • Lhuissier FGP, De Ruijter NCA, Sieberer BJ, Esseling JJ, Emons AMC (2001) Time course of cell biological events evoked in legume root hairs by Rhizobium Nod factors: state of the art. Ann Bot 87:289–302

    Article  CAS  Google Scholar 

  • Limpens E, Franken C, Smit P, Willemse J, Bisseling T, Geurts R (2003) LysM domain receptor kinases regulating rhizobial nod factor-induced infection. Science 302:630–633

    Article  CAS  PubMed  Google Scholar 

  • Lloyd C, Pearce K, 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. Cell Motil Cytoskeleton 8:27–36

    Article  Google Scholar 

  • Lodwig EM et al (2003) Amino-acid cycling drives nitrogen fixation in the legume–Rhizobium symbiosis. Nature 422:722–726

    Article  CAS  PubMed  Google Scholar 

  • Long SR (1989) Rhizobium-legume nodulation: life together in the underground. Cell 56:203–214

    Article  CAS  PubMed  Google Scholar 

  • Long SR (2015) Receptive to infection. Nature 523:298–299

    Article  CAS  PubMed  Google Scholar 

  • Lopez M, Herrera-Cervera JA, Iribarne C, Tejera NA, Lluch C (2008) Growth and nitrogen fixation in Lotus japonicus and Medicago truncatula under NaCl stress: Nodule carbon metabolism. J Plant Physiol 165(6):641–650

    Article  CAS  PubMed  Google Scholar 

  • Lotocka B, Kopcinska J, Skalniak M (2012) Review article: the meristem in indeterminate root nodules of faboideae. Symbiosis 58:63–72

    Article  PubMed  Google Scholar 

  • Madsen EB, Madsen LH, Radutoiu S, Olbryt M, Rakwalska M, Szczyglowski K, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J (2003) A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425:637–640

    Article  CAS  PubMed  Google Scholar 

  • Marsh JF, Rakocevic A, Mitra RM, Brocard L, Sun J, Eschstruth A, Long SR, Schultze M, Ratet P, Oldroyd GE (2007) Medicago truncatula NIN is essential for rhizobial-independent nodule organogenesis induced by autoactive calcium/calmodulin-dependent protein kinase. Plant Physiol 144:324–335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maunoury N, Kondorosi A, Kondorosi E, Mergaert P (2008) Cell biology of nodule infection and development. In: James EK, Sprent JI, Dilworth WE (eds) Nitrogen-fixing leguminous symbioses. Springer, The Netherlands

    Google Scholar 

  • Mergaert P, Uchiumi T, Alunni B, Evanno G, Cheron A, Catrice O, Mausset AE, Barloy-Hubler F, Galibert F, Kondorosi A, Kondorosi E (2006) Eukaryotic control on bacterial cell cycle and differentiation in the Rhizobium-legume symbiosis. Proc Natl Acad Sci U S A 103(13):5230–5235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Michiels J, Verreth C, Vanderleyden J (1994) Effects of temperature stress on bean-nodulating Rhizobium strains. Appl Environ Microbiol 60(4):1206–1212

    CAS  PubMed  PubMed Central  Google Scholar 

  • Middleton PH, Jakab J, Penmetsa RV, Starker CG, Doll J, Kaló P, Prabhu R, Marsh JF, Mitra RM, Kereszt A, Dudas B, VandenBosch K, Long SR, Cook DR, Kiss GB, Oldroyd GE (2007) An ERF transcription factor in Medicago truncatula that is essential for nod factor signal transduction. Plant Cell 19:1221–1234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miller DD, de Ruijter NCA, Emons AMC (1997) From signal to form: aspects of the cytoskeleton plasma membrane cell wall continuum in root hair tips. J Exp Bot 48:1881–1896

    CAS  Google Scholar 

  • Mitra RM, Gleason CA, Edwards A, Hadfield J, Downie JA, Oldroyd GE, Long SR (2004) A Ca2+/calmodulin-dependent protein kinase required for symbiotic nodule development: Gene identification by transcript-based cloning. Proc Natl Acad Sci U S A 101:4701–4705

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Ann Rev Plant Biol 59:651–681

    Article  CAS  Google Scholar 

  • Murray JD, Karas BJ, Sato S, Tabata S, Amyot L, Szczyglowski K (2007) A cytokinin perception mutant colonized by Rhizobium in the absence of nodule organogenesis. Science 315:101–104

    Article  CAS  PubMed  Google Scholar 

  • Muthukumar T, Priyadharsini P, Uma E, Jaison S, Pandey RR (2014) Role of arbuscular mycorrhizal fungi in alleviation of acidity stress on plant growth. In: Miransari M (ed) Use of microbes for the alleviation of soil stresses. Springer, New York

    Google Scholar 

  • Nap JP, Bisseling T (1990) Developmental biology of plant-prokaryote symbiosis: the legume root nodule. Science 250:948–954

    Article  CAS  PubMed  Google Scholar 

  • Newcomb W, Peterson RL (1979) The occurrence and ontogeny of transfer cells associated with lateral roots and root nodules in Leguminosae. Can J Bot 57:2583–2602

    Article  Google Scholar 

  • Oldroyd GED, Downie JA (2004) Calcium, kinases and nodulation signalling in legumes. Nat Rev Mol Cell Biol 5:566–576

    Article  CAS  PubMed  Google Scholar 

  • Oldroyd GED, Long SR (2003) Identification and characterization of nodulation-signaling pathway 2, a gene of Medicago truncatula involved in Nod factor signaling. Plant Physiol 131:1027–1032

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Orchard VA, Cook FG (1983) Relation between soil respiration and soil moisture. Soil Biol Biochem 15:447–453

    Article  Google Scholar 

  • Oufdou K, Benidire L, Lyubenova L, Daoui K, Fatemi ZEA, Schröder P (2014) Enzymes of the glutathione–ascorbate cycle in leaves and roots of rhizobia-inoculated faba bean plants (Vicia faba L.) under salinity stress. Eur J Soil Sci 60:98–103

    CAS  Google Scholar 

  • O’Brian MR, Kirshbom PM, Maier RJ. (1987). Bacterial heme synthesis is required for expression of the leghemoglobin holoprotein but not the apoprotein in soybean root nodules. Proc Nati Acad Sci U S A 84: 8390–8393.

    Article  Google Scholar 

  • O’Hara GW, Howieson JG, Yates RJ, Real D, Revell C. (2008). BNF Applications for Poverty Alleviation. In: Dakora F, Chimphango SBM, Valentine AJ, Elmerich C, Newton WE (eds.) Biological Nitrogen Fixation: Towards Poverty Alleviation through Sustainable Agriculture. pp. 25–26. Springer Netherlands.

    Google Scholar 

  • Paau AS, Cowles JR, Raveed D (1978) Development of bacteroids in alfalfa (Medicago sativa) nodules. Plant Physiol 62:526–530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paau AS, Bloch CB, Brill WJ (1980) Developmental fate of Rhizobium meliloti bacteroids in alfalfa nodules. J Bacteriol 143:1480–1490

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pankhurst CE, Gibson AH (1973) Rhizobium strain influence on disruption of clover nodule development at high root temperature. J Gen Microbiol 74:219–231

    Article  CAS  Google Scholar 

  • Parsons R, Day DA (1990) Mechanism of soybean nodule adaptation to different oxygen pressure. Plant Cell Environ 13:501–512

    Article  Google Scholar 

  • Pena-Cabriales JJ, Castellanos JZ (1993) Effects of water stress on N2 fixation and grain yield of Phaseolus vulgaris L. Plant Soil 152(1):151–155

    Article  Google Scholar 

  • Peoples MB, Brockwell J, Herridge DF, Rochester IJ, Alves BJR, Urquiaga S, Boddey RM, Dakora FD, Bhattarai S, Maskey SL, Sampet C, Rerkasem B, Khan DF, Hauggaard-Nielsen H, Jensen ES (2009) The contributions of nitrogen-fixing crop legumes to the productivity of agricultural systems. Symbiosis 48:1–17

    Article  CAS  Google Scholar 

  • Pérez J, Jiménez-Zurdo JI, Martínez-Abarca F, Millán V, Shimkets LJ, Muñoz-Dorado J (2014) Rhizobial galactoglucan determines the predatory pattern of Myxococcus xanthus and protects Sinorhizobium meliloti from predation. Environ Microbiol 16:2341–2350

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pislariu CI, Sinharoy S, Wen J, Murray JD, Ratet P, Udvardi MK (2015) Retrotransposon (Tnt1)-Insertion mutagenesis in Medicago as a tool for genetic dissection of symbiosis in legumes. In: de Bruijn FJ (ed) Biological nitrogen fixation. John Wiley& Sons Inc, Hoboken, NJ

    Google Scholar 

  • Postma J, Hok-A-Hin CH, van Veen JA (1990) Role of microniches in protecting introduced Rhizobium leguminosarum biovar trifolii against competition and predation in soil. Appl Environ Microbiol 56:495–502

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pueppke SG, Broughton WJ (1999) Rhizobium sp. strain NGR234 and R. fredii USDA257 share exceptionally broad, nested host ranges. Mol Plant Microbe Interact 12(4):293–318

    Article  CAS  PubMed  Google Scholar 

  • Radutoiu S, Madsen LH, Madsen EB, Felle HH, Umehara Y, Grønlund M, Sato S, Nakamura Y, Tabata S, Sandal N, Stougaard J (2003) Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425:585–592

    Article  CAS  PubMed  Google Scholar 

  • Riely BK, Lougnon G, Ane JM, Cook DR (2007) The symbiotic ion channel homolog DMI1 is localized in the nuclear membrane of Medicago truncatula roots. Plant J 49:208–216

    Article  CAS  PubMed  Google Scholar 

  • Robbins NE, Trontin C, Duan L, Dinneny JR (2014) Beyond the barrier: communication in the root through the endodermis. Plant Physiol 166:551–559

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Roche P, Debelle F, Maillet F, Lerouge P, Faucher C, Truchet G, Denarib J, Prome JC (1991) Molecular basis of symbiotic host specificity in Rhizobium meliloti: nodH and nodPQ genes encode the sulfation of lipo-oligosaccharide signals. Cell 67:1131–1143

    Article  CAS  PubMed  Google Scholar 

  • Rønn R, Mccaig AE, Griffiths BS, Prosser JI (2002) Impact of protozoan grazing on bacterial community structure in soil microcosms. Appl Environ Microbiol 68:6094–6105

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Roughley RJ (1970) The influence of root temperature, Rhizobium strain and host selection on the structure and nitrogen-fixing efficiency of the root nodules of Trifolium subterraneum. Ann Bot 34:631–646

    Google Scholar 

  • Roughley RJ, Dart PJ (1970) Root temperature and root-hair infection of Trifolium subterraneum L. cv. Cranmore. Plant Soil 32:518–520

    Article  Google Scholar 

  • Rounds CM, Bezanilla M (2013) Growth Mechanisms in tip-growing plant cells. Annu Rev Plant Biol 64:243–265

    Article  CAS  PubMed  Google Scholar 

  • Saito K, Yoshikawa M, Yano K, Miwa H, Uchida H, Asamizu E, Sato S, Tabata S, Imaizumi-Anraku H, Umehara Y, Kouchi H, Murooka Y, Szczyglowski K, Downie JA, Parniske M, Hayashi M, Kawaguchi M (2007) NUCLEOPORIN85 is required for calcium spiking, fungal and bacterial symbioses, and seed production in Lotus japonicus. Plant Cell 19:610–624

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schauser L, RoussisA SJ, Stougaard J (1999) A plant regulator controlling development of symbiotic root nodules. Nature 402(6758):191–195

    Article  CAS  PubMed  Google Scholar 

  • Schmitz RA, Klopprogge K, Grabbe R (2002) Regulation of Nitrogen Fixation in Klebsiella pneumoniae and Azotobacter vinelandii: NifL, Transducing Two Environmental Signals to the nif Transcriptional Activator NifA. J Mol Microbiol Biotechnol 4(3): 235–242

    CAS  PubMed  Google Scholar 

  • Schulze J (2004) How are nitrogen fixation rates regulated in legumes? J Plant Nutr Soil Sci 167:125–137

    Article  CAS  Google Scholar 

  • Sharma SR, Rao NK, Gokhale TS, Ismail S (2013) Isolation and characterization of salt-tolerant rhizobia native to the desert soils of United Arab Emirates. Em J Food Agric 25(2):102–108

    Google Scholar 

  • Sieberer BJ, Timmers ACJ, Lhuissier FGP, Emons AMC (2002) Endoplasmic microtubules configure the subapical cytoplasm and are required for fast growth of Medicago truncatula root hairs. Plant Physiol 130:977–988

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simões-Araújo JL, Rodrigues, RL, Liliane BDA, Mondego, JM, Alves-Ferreira M, Rumjanek, NG, Margis-Pinheiro M. 2002. Identification of differentially expressed genes by cDNA-AFLP technique during heat stress in cowpea nodules. FEBS letters 515(1):44–50

    Article  PubMed  Google Scholar 

  • Smit P, Raedts J, Portyanko V, Debellé F, Gough C, Bisseling T, Geurts R (2005) NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription. Science 308:1789–1791

    Article  CAS  PubMed  Google Scholar 

  • Smith LG (2003) Cytoskeletal control of plant cell shape: getting the fine points. Curr Opin Plant Biol 6:63–73

    Article  PubMed  Google Scholar 

  • Smith LT, Smith GM, D’souza MR, Pocard JA, Rudulier DL, Madkour MA (1994) Osmoregulation in Rhizobium meliloti: mechanism and control by other environmental signals. J Exp Zool 268(2):162–165

    Article  CAS  Google Scholar 

  • Streeter G (1993) Translocation−A key factor limiting the efficiency of nitrogen fixation in legume nodules. Physiol Plant 87:616–623

    Article  CAS  Google Scholar 

  • Subramanian S (2013) Distinct hormone regulation of determinate and indeterminate nodule development in legumes. J Plant Biochem Physiol 1(110):2

    Google Scholar 

  • Sujkowska M, Górska-Czekaj M, Bederska M, Borucki W (2011) Vacuolar organization in the nodule parenchyma is important for the functioning of pea root nodules. Symbiosis 54:1–16

    Article  PubMed  PubMed Central  Google Scholar 

  • Sutton WD (1983) Nodule development and senescence. In: Broughton WJ (ed) Nitrogen Fixation, vol 3. Clarendon Press, Oxford

    Google Scholar 

  • Talbi C, Sánchez C, Hidalgo-Garcia A, González EM, Arrese-Igor C, Girard L, Bedmar EJ, Delgado MJ (2012) Enhanced expression of Rhizobium etli cbb 3 oxidase improves drought tolerance of common bean symbiotic nitrogen fixation. J Exp Bot 63(14):5035–5043

    Article  CAS  PubMed  Google Scholar 

  • Talibart R, Jebbar M, Gouesbet G, Himdi-Kabbab S, Wróblewski H, Blanco C, Bernard T (1994) Osmoregulation in rhizobia: ectoine-induced salt tolerance. J Bacteriol 176:5210–5217

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tang C, Thomson BD (1996) Effects of solution pH and bicarbonate on the growth and nodulation of a range of grain legumes. Plant Soil 186:321–330

    Article  CAS  Google Scholar 

  • Tate RL (1995) Soil microbiology (symbiotic nitrogen fixation). Wiley, New York

    Google Scholar 

  • Taylor RW, Williams ML, Sistani KR (1991) Nitrogen fixation by soybean-Bradyrhizobium combinations under acidity, low P and high Al stresses. Plant Soil 131:293–300

    Article  CAS  Google Scholar 

  • Timmers AC, Auriac MC, Truchet G (1999) Refined analysis of early symbiotic steps of the Rhizobium-Medicago interaction in relationship with microtubular cytoskeleton rearrangements. Development 126:3617–3628

    CAS  PubMed  Google Scholar 

  • Timmers AC, Soupene E, Auriac MC, de Billy F, Vasse J, Boistard P, Truchet G (2000) Saprophytic intracellular rhizobia in alfalfa nodules. Mol Plant Microbe Interact 13(11):1204–1213

    Article  CAS  PubMed  Google Scholar 

  • Tirichine L, Imaizumi-Anraku H, Yoshida S, Murakami Y, Madsen LH, Miwa H, Nakagawa T, Sandal N, Albrektsen AS, Kawaguchi M, Downie A, Sato S, Tabata S, Kouchi H, Parniske M, Kawasaki S, Stougaard J (2006) Deregulation of a Ca2+/calmodulin-dependent kinase leads to spontaneous nodule development. Nature 441:1153–1156

    Article  CAS  PubMed  Google Scholar 

  • Tirichine L, Sandal N, Madsen LH, Radutoiu S, Albrektsen AS, Sato S, Asamizu E, Tabata S, Stougaard J (2007) A gain-of-function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis. Science 315:104–107

    Article  CAS  PubMed  Google Scholar 

  • Tominaga MK, Sonobe MS, Yokota E, Shimmen T (1997) Microtubules regulate the organization of actin filaments at the cortical region in root hair cells of Hydrocharis. Protoplasma 199:83–92

    Article  CAS  Google Scholar 

  • Tu JC (1981) Effect of salinity on Rhizobium-root-hair interaction, nodulation and growth of soybean. Can J Plant Sci 61(2):231–239

    Article  Google Scholar 

  • Udvardi M, Day D (1997) Metabolite transport across symbiotic membranes of legume nodules. Annu Rev Plant Biol 48:493–523

    Article  CAS  Google Scholar 

  • Vasse J, de Billy F, Camut S, Truchet G (1990) Correlation between ultrastructural differentiation of bacteroids and nitrogen fixation in alfalfa nodules. J Bacteriol 172(8):4295–4306

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vassileva V, Milanov G, Ignatov G, Nikolov B (1997) Effect of low pH on nitrogen fixation of common bean grown at various calcium and nitrate levels. J Plant Nutr 20:279–94

    Article  CAS  Google Scholar 

  • Wagner SC (2011) Biological nitrogen fixation. Nat Educ Knowledge 3(10):15

    Google Scholar 

  • Wais RJ, Galera C, Oldroyd G, Catoira R, Penmetsa RV, Cook D, Gough C, Denarié J, Long SR (2000) Genetic analysis of calcium spiking responses in nodulation mutants of Medicago truncatula. Proc Natl Acad Sci U S A 97(24):13407–13412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Waldon HB, Jenkins MB, Virginia RA, Harding EE (1989) Characteristics of woodland rhizobial populations from surface-and deep-soil environments of the Sonoran Desert. Appl Environ Microbiol 55(12):3058–3064

    CAS  PubMed  PubMed Central  Google Scholar 

  • Walsh KB, McCully ME, Conny MJ (1989) Vascular transport and soybean nodule function: nodule xylem is a blind alley, not a throughway. Plant Cell Environ 12:395–405

    Article  Google Scholar 

  • Walsh KB, Atkins RS, Low CS (1992) Vascular anatomy of fabaceous nodules of determinate growth. Plant Cell Environ 15:849–854

    Article  Google Scholar 

  • Witty JF, Skot L, Revsbech NP (1987) Direct evidence for changes in the resistance of legume root nodules to O2 diffusion. J Exp Bot 38:1129–1140

    Article  Google Scholar 

  • Wood M, Cooper JE, Holding AJ (1984). Aluminium toxicity and nodulation of Trifofium repens. Plant and Soil 78: 381–391.

    Article  CAS  Google Scholar 

  • Wymer CL, Bibikova TN, Gilroy S (1997) Cytoplasmic free calcium distributions during the development of root hairs of Arabidopsis thaliana. Plant J 12(2):427–439

    Article  CAS  PubMed  Google Scholar 

  • Zahran HH (1991) Conditions for successful Rhizobium-legume symbiosis in saline environments. Biol Fertil Soils 12:73–80

    Article  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 

  • Zahran HH, Räsänen LA, Karsisto M, Lindström K (1994) Alteration of lipopolysaccharide and protein profiles in SDS-PAGE of rhizobia by osmotic and heat stress. World J Microbiol Biotechnol 10(1):100–105

    Article  CAS  PubMed  Google Scholar 

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Yamal, G., Bidalia, A., Vikram, K., Rao, K.S. (2016). An Insight into the Legume–Rhizobium Interaction. In: Hakeem, K., Akhtar, M. (eds) Plant, Soil and Microbes. Springer, Cham. https://doi.org/10.1007/978-3-319-29573-2_16

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