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The Rhizobium–Plant Symbiosis: State of the Art

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Plant Microbe Symbiosis

Abstract

Nitrogen is a vital element necessary for all living organisms (plants, microbes, and animals) for the production of nucleic acids, proteins, and other biomolecules in which nitrogen is needed. Nitrogen is the most abundant gas in the atmosphere of planet Earth, almost 79%. Even in its highest availability, living organisms cannot utilize this gaseous form, unless and until it is in fixed form, which is the reduced form, where it combines with hydrogen and forms ammonia. Photosynthetic plants use this fixed nitrogen to make organic matter, and the phytoproteins that are produced enter into the food chain. On death or during decomposition, microorganisms catabolize the proteins present in the body of dead organisms, fecal wastes, and other organic matter, releasing ammonium ions and forming the primary mechanism of the nitrogen cycle. Microbes exist everywhere, in soil, air, water, and even in extreme conditions, and they also need nutrients for their survival. Of all types of bacteria, some form the complex association known as symbiosis with other living organisms, which can be commensalism, parasitism, mutualism, predation, amensalism, or competition, proto-cooperation between bacteria and other organisms. Bacteria from the family Rhizobiaceae survive even nitrogen-limiting condition by symbiotic association with plants of the leguminous family. This chapter discusses the whole mechanism involved in the symbiotic association between rhizobia and legumes.

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References

  • Ahemad M, Kibret M (2014) Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. J King Saud Univ Sci 26(1):1–20

    Article  Google Scholar 

  • Al-Falih AMK (2002) Factors affecting the efficiency of symbiotic nitrogen fixation by Rhizobium. Pak J Biol Sci 5(11):1277–1293

    Article  Google Scholar 

  • Bertrand A, Dhont C, Bipfubusa M, Chalifour FP, Drouin P, Beauchamp CJ (2015) Improving salt stress responses of the symbiosis in alfalfa using salt-tolerant cultivar and rhizobial strain. Appl Soil Ecol 87:108–117

    Article  Google Scholar 

  • Bielach A, Podlešáková K, Marhavý P, Duclercq J, Cuesta C, Müller B et al (2012) Spatiotemporal regulation of lateral root organogenesis in Arabidopsis by cytokinin. Plant Cell 24:3967–3981

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bloemberg GV, Lugtenberg BJ (2001) Molecular basis of plant growth promotion and biocontrol by rhizobacteria. Curr Opin Plant Biol 4:343–350

    Article  CAS  PubMed  Google Scholar 

  • Breakspear A, Liu C, Roy S, Stacey N, Rogers C, Trick M et al (2014) The root hair “infectome” of Medicago truncatula uncovers changes in cell cycle genes and reveals a requirement for auxin signaling in rhizobial infection. Plant Cell 26:4680–4701

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Broughton WJ, Hernandez G, Blair M, Beebe S, Gepts P, Vanderleyden J (2003) Beans (Phaseolus spp.)–model food legumes. Plant Soil 252:55–128

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Cesco S, Neumann G, Tomasi N, Pinton R, Weisskopf L (2010) Release of plant-borne flavonoids into the rhizosphere and their role in plant nutrition. Plant Soil 329:1–25

    Article  CAS  Google Scholar 

  • Crespi M, Gálvez S (2000) Molecular mechanisms in root nodule development. J Plant Growth Regul 19:155–166

    Article  CAS  PubMed  Google Scholar 

  • Davison J (1988) Plant beneficial bacteria. Biotechnology 6:282–286

    CAS  Google Scholar 

  • De Meyer SE, De Beuf K, Vekeman B, Willems A (2015) A large diversity of non-rhizobial endophytes found in legume root nodules in Flanders (Belgium). Soil Biol Biochem 83:1–11

    Article  CAS  Google Scholar 

  • Desbrosses GJ, Stougaard J (2011) Root nodulation: a paradigm for how plant–microbe symbiosis influences host developmental pathways. Cell Host Microbe 10:348–358

    Article  CAS  PubMed  Google Scholar 

  • Dunn MF (2015) Key roles of microsymbiont amino acid metabolism in rhizobia–legume interactions. Crit Rev Microbiol 41:411–451

    Article  CAS  PubMed  Google Scholar 

  • Durbak A, Yao H, McSteen P (2012) Hormone signaling in plant development. Curr Opin Plant Biol 15:92–96

    Article  CAS  PubMed  Google Scholar 

  • Faucher C, Camut H, De’narié J, Truchet G (1989) The nodH and nodQ host range genes of Rhizobium meliloti behave as avirulence genes in R. leguminosarum bv. viciae and determine changes in the production of plant-specific extracellular signals. Mol Plant-Microbe Interact 2:291–300

    Article  Google Scholar 

  • Foo E (2017) Role of plant hormones and small signalling molecules in nodulation under P stress. In: Legume nitrogen fixation in soils with low phosphorus availability. Springer, Cham, pp 153–167

    Google Scholar 

  • Gourion B, Berrabah F, Ratet P, Stacey G (2015) Rhizobium–legume symbioses: the crucial role of plant immunity. Trends Plant Sci 20:186–194

    Article  CAS  PubMed  Google Scholar 

  • Griesmann M, Chang Y, Liu X, Song Y, Haberer G, Crook MB, Billault-Penneteau B et al (2018) Phylogenomics reveals multiple losses of nitrogen-fixing root nodule symbiosis. Science:eaat1743. https://doi.org/10.1126/science.aat1743

  • Guinel FC (2015) Ethylene, a hormone at the center-stage of nodulation. Front Plant Sci 6:1121

    Article  PubMed  PubMed Central  Google Scholar 

  • Guinel FC, Geil RD (2002) A model for the development of the rhizobial and arbuscular mycorrhizal symbioses in legumes and its use to understand the roles of ethylene in the establishment of these two symbioses. Can J Bot 80:695–720

    Article  CAS  Google Scholar 

  • Haney CH, Long SR (2010) Plant flotillins are required for infection by nitrogen-fixing bacteria. Proc Natl Acad Sci USA 107:478–483

    Article  PubMed  Google Scholar 

  • Hirsch AM, Lum MR, Downie JA (2001) What makes the rhizobia–legume symbiosis so special? Plant Physiol 127:1484–1492

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Irmer S, Podzun N, Langel D, Heidemann F, Kaltenegger E, Schemmerling B, Geilfus C-M, Zörb C, Ober D (2015) New aspect of plant–rhizobia interaction: alkaloid biosynthesis in Crotolaria depends on nodulation. PNAS 112:4164–4169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jeffries P, Gianinazzi S, Perotto S, Turnau K, Barea JM (2003) The contribution of arbuscular mycorrhizal fungi in sustainable maintenance of plant health and soil fertility. Biol Fertil Soils 37:1–16

    Article  Google Scholar 

  • Jordan DC (1984) Bradyrhizobium. In: Bergey’s manual of systematic bacteriology, vol 1. Williams & Wilkins, Baltimore, pp 242–244

    Google Scholar 

  • Kawaharada Y, Kelly S, Wibroe Nielsen M, Hjuler CT, Gysel K, Muszyñki A et al (2015) Receptor-mediated exopolysaccharide perception controls bacterial infection. Nature (Lond) 523:308–312

    Article  CAS  Google Scholar 

  • Khalid A, Arshad M, Shaharoona B et al (2009) Plant growth promoting Rhizobacteria and sustainable agriculture. In: Microbial strategies for crop improvement. Springer, Berlin, pp 133–160

    Chapter  Google Scholar 

  • Kong Z, Deng Z, Glick BR, Wei G, Chou M (2017) A nodule endophytic plant growth-promoting Pseudomonas and its effects on growth, nodulation and metal uptake in Medicago lupulina under copper stress. Ann Microbiol 67:49–58

    Article  CAS  Google Scholar 

  • Lefebvre B, Timmers T, Mbengue M, Moreau S, Hervé C, Tóth K et al (2010) A remorin protein interacts with symbiotic receptors and regulates bacterial infection. Proc Natl Acad Sci USA 107:2343–2348

    Article  PubMed  PubMed Central  Google Scholar 

  • Levy A, Gonzalez IS, Mittelviefhaus M, Clingenpeel S, Paredes SH, Miao J, Alvarez BR (2018) Genomic features of bacterial adaptation to plants. Nat Genet 50:138

    Article  CAS  Google Scholar 

  • Lewin A, Rosenberg C, Meyer ZAH, Wong CH, Nelson L, Manen JF, Stanley J, Downing DN, De’narié J, Broughton WJ (1987) Multiple host-specificity loci of the broad host-range Rhizobium sp. NGR234 selected using the widely compatible legume Vigna unguiculata. Plant Mol Biol 8:447–459

    Article  CAS  PubMed  Google Scholar 

  • Limpens E, van Zeijl A, Geurts R (2015) Lipochitoologosaccharides modulate plant host immunity to enable endosymbiosis. Annu Rev Phytopathol 53:15.1–15.24. https://doi.org/10.1146/annurev-phyto-080614-120149

    Article  CAS  Google Scholar 

  • Long SR (1984) Nodulation genetics. In: Kosuge T, Nester EW (eds) Plant–microbe interactions. Macmillan, New York, pp 265–306

    Google Scholar 

  • Mahdi SS, Hassan GI, Samoon SA et al (2010) Bio-fertilizers in organic agriculture. J Phytol 2:42–54

    Google Scholar 

  • Manoj KR, Kalia RK, Singh R, Gangola MP, Dhawan AK (2011) Developing stress tolerant plants through in vitro selection: an overview of the recent progress. Environ Exp Bot 71:89–98

    Article  Google Scholar 

  • Marhavý P, Vanstraelen M, De Rybel B, Zhaojun D, Bennett MJ, Beeckman T et al (2013) Auxin reflux between the endodermis and pericycle promotes lateral root initiation. EMBO J 32:149–158

    Article  CAS  PubMed  Google Scholar 

  • McCully ME (2001) Niches for bacterial endophytes in crop plants: a plant biologist’s review. Aust J Plant Physiol 28:983–990

    Google Scholar 

  • Moling S, Bisseling T (2015) Evolution of Rhizobium nodulation: from nodule-specific genes (nodulins) to recruitment of common processes. In: Biological nitrogen fixation, vol 2. Wiley, Hoboken, NJ, p 39

    Chapter  Google Scholar 

  • Mortier V, Wasson A, Jaworek P, De Keyser A, Decroos M, Holsters M et al (2014) Role of LONELY GUY genes in indeterminate nodulation on Medicago truncatula. New Phytol 202:582–593

    Article  CAS  PubMed  Google Scholar 

  • Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250

    Article  CAS  PubMed  Google Scholar 

  • Murray JD (2011) Invasion by invitation: rhizobial infection in legumes. Mol Plant-Microbe Interact 24:631–639

    Article  CAS  PubMed  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 

  • Nabizadeh E, Jalilnejad N, Armakani M (2011) Effect of salinity on growth and nitrogen fixation of alfalfa (Medicago sativa). World Appl Sci J 13:1895–1900

    CAS  Google Scholar 

  • Nakagawa S, Mino S (2018) Deep-sea vent extremophiles: cultivation, physiological characteristics, and ecological significance. In: Extremophiles. CRC, New York, pp 165–184

    Google Scholar 

  • Okazaki S et al (2013) Hijacking of leguminous nodulation signalling by the rhizobial type III secretion system. Proc Natl Acad Sci USA 110:17131–17136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oldroyd GED (2013) Speak, friend, and enter: signaling systems that promote beneficial associations in plants. Nat Rev 11:252–263

    CAS  Google Scholar 

  • Oldroyd GE, Murray JD, Poole PS, Downie JA (2011) The rules of engagement in the legume–rhizobial symbiosis. Annu Rev Genet 45:119–144

    Article  CAS  PubMed  Google Scholar 

  • Peck MC, Fisher RF, Long SR (2006) Diverse flavonoids stimulate NodD1 binding to nod gene promoters in Sinorhizobium meliloti. J Bacteriol 188:5417–5427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Requena N, Perez-Solis E, Azcón-Aguilar C, Jeffries P, Barea JM (2001) Management of indigenous plant–microbe symbioses aids restoration of desertified ecosystems. Appl Environ Microbiol 67:495–498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shiraishi A, Matsushita N, Hougetsu T (2010) Nodulation in black locust by the gamma proteobacteria Pseudomonas sp. and the beta proteobacteria Burkholderia sp. Syst Appl Microbiol 33:269–274

    Article  CAS  PubMed  Google Scholar 

  • Singleton PW, Bohlool BB (1984) Effect of salinity on nodule formation by soybean. Plant Physiol 74:72–76

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smit G, Swart S, Lugtenberg BJ, Kijne JW (1992) Molecular mechanisms of attachment of Rhizobium bacteria to plant roots. Mol Microbiol 6:2897–2903

    Article  CAS  PubMed  Google Scholar 

  • Spaink HP, Weinman J, Djordjevic MA, Wijfelman CA, Okker JH, Lugtenberg BJJ (1989) Genetic analysis and cellular localization of the Rhizobium host specificity-determining NodE protein. EMBO J 8:2811–2818

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzaki T, Ito M, Kawaguchi M (2013) Genetic basis of cytokinin and auxin functions during root nodule development. Front Plant Sci 4:42

    Article  PubMed  PubMed Central  Google Scholar 

  • Trinick MJ (1979) Structure of nitrogen-fixing nodules formed by Rhizobium on roots of Parasponia andersonii Planch. Can J Microbiol 25:565–578

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Vance CP (2001) Symbiotic nitrogen fixation and phosphorus acquisition. Plant nutrition in a world of declining renewable resources. Plant Physiol 127:390–397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Young JPW, Johnston AWB (1989) The evolution of specificity in the legume–Rhizobium symbiosis. Trends Ecol Evol 4:331–349

    Article  Google Scholar 

  • Young JPW, Downer HL, Eardly BD (1991) Phylogeny of the phototrophic Rhizobium strain Btail by polymerase chain reaction-based sequencing of the 16S rRNA gene segment. J Bacteriol 173:2271–2277

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zahran HH (2001) Rhizobia from wild legumes: diversity, taxonomy, ecology, nitrogen fixation and biotechnology. J Biotechnol 91(2-3):143–153

    Article  CAS  PubMed  Google Scholar 

  • Zaidi S, Usmani S, Singh BR, Musarrat J (2008) Significance of Bacillus subtilis strains SJ-101 as a bioinoculant for concurrent plant growth promotion and nickel accumulation in Brassica juncea. Chemosphere 64:991–997

    Article  CAS  Google Scholar 

  • Zhuang XL, Chen J, Shim H, Bai Z (2007) New advances in plant growth-promoting rhizobacteria for bioremediation. Environ Int 33:406–413

    Article  PubMed  Google Scholar 

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Kumar, N. et al. (2020). The Rhizobium–Plant Symbiosis: State of the Art. In: Varma, A., Tripathi, S., Prasad, R. (eds) Plant Microbe Symbiosis. Springer, Cham. https://doi.org/10.1007/978-3-030-36248-5_1

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