Submitted Successfully!
Thank you for your contribution! You can also upload a video entry or images related to this topic.
Ver. Summary Created by Modification Content Size Created at Operation
1 + 2074 word(s) 2074 2021-09-30 05:47:44 |
2 format correct Meta information modification 2074 2021-10-08 05:42:15 |

Video Upload Options

Do you have a full video?


Are you sure to Delete?
If you have any further questions, please contact Encyclopedia Editorial Office.
Missaoui, A. Biological Nitrogen Fixation. Encyclopedia. Available online: (accessed on 11 December 2023).
Missaoui A. Biological Nitrogen Fixation. Encyclopedia. Available at: Accessed December 11, 2023.
Missaoui, Ali. "Biological Nitrogen Fixation" Encyclopedia, (accessed December 11, 2023).
Missaoui, A.(2021, October 04). Biological Nitrogen Fixation. In Encyclopedia.
Missaoui, Ali. "Biological Nitrogen Fixation." Encyclopedia. Web. 04 October, 2021.
Biological Nitrogen Fixation

In agroecosystems, nitrogen is one of the major nutrients limiting plant growth. To meet the increased nitrogen demand in agriculture, synthetic fertilizers have been used extensively in the latter part of the twentieth century, which have led to environmental challenges such as nitrate pollution. Biological nitrogen fixation (BNF) in plants is an essential mechanism for sustainable agricultural production and healthy ecosystem functioning. BNF by legumes and associative, endosymbiotic, and endophytic nitrogen fixation in non-legumes play major roles in reducing the use of synthetic nitrogen fertilizer in agriculture, increased plant nutrient content, and soil health reclamation. 

biological nitrogen fixation nitrogenase nif genes legumes and nodules associative nitrogen fixation soil microbiome rhizosphere

1. Introduction

A healthy, functioning soil ensures nutrient cycling for optimum plant growth for agricultural production [1]. However, agricultural productivity is often limited by available soil nutrients, especially nitrogen [2]. Nitrogen is not present in soil parent material despite the fact that nitrogen content in the atmosphere is highest among all the atmospheric gases [3]. Hence, soil nitrogen input for plant nutrition and crop productivity largely depends on organic matter degradation, synthetic fertilizer applications, and biological nitrogen fixation (BNF) via nitrogenase enzyme activity [4][5]. This limited bio-availability of N and the escalating reliance of crop growth on N have created a colossal N-based fertilizer industry worldwide [6][7]. Nitrogenous fertilizer production currently represents a significant expense for the efficient growth of various crops in the developed world. Synthetic N fertilizers are currently used in grain, grass, and fruit productions (about 60% for cereals and 10% with irrigated rice production) [8]. More than 50% of the applied N-based fertilizer is used by the plants and the remaining can be subjected to losses like surface runoff and leaching leading to nitrate contamination of soils and groundwater. In terms of energy efficiency, moreover, manufacturing nitrogen-based fertilizers requires six times more energy than that needed to produce either phosphorous or potassium-based fertilizers [9]. Therefore, reducing dependence on nitrogenous fertilizers in agriculture in the developed world and developing countries may lead to potential gains in an agricultural setting. Biological nitrogen fixation (BNF) in economically important food and forage crops [10] has drawn attention to achieve sustainable agricultural goals in both hemispheres of the world [11]. In livestock production systems in the southeastern USA, strategically planting nitrogen-fixing legumes in cattle pastures has shown to increase the available soil nitrogen [12], thereby reducing the need to apply synthetic nitrogen sources. The diazotrophic microorganisms from bacteria or archaea domains are responsible for BNF and only some prokaryotes are able to use atmospheric nitrogen through BNF by encoding nitrogenase, an enzyme that catalyzes the conversion of N2 gas to ammonia (NH3) [8][13][14]. Despite the phylogenic and ecological diversity among diazotrophic bacteria and their hosts, a synchronized interaction is always a prerequisite between the microbial entities and the host plant to achieve a successful nitrogen fixation system. The importance of this process is enormous as it reduces the dependence on nitrogen fertilizers for plants and thus, for agriculture overall. It has been estimated that worldwide, biological nitrogen fixation produces roughly 200 million tons of nitrogen annually [15][16]. In fact, nearly 50% of the total nitrogen in crop fields is the contribution of BNF by diazotrophic bacteria of the total biosphere nitrogen [17]. Moreover, fixed nitrogen can also be transferred to intercropped non-legumes in the case of mixed cropping systems, such as the soybean–wheat system, or the next season crops in crop rotation [18]

2. Biological Nitrogen Fixation (BNF)

Nitrogen fixation is a dynamic and high-energy demanding process [19]. The pathway for the biological reduction of inert N2 into the reactive compound NH3 (ammonia) under micro-aerobic conditions is as follows:
N2 + 8H+ + 8e + 16Mg-ATP → 2NH3 + H2 + 16Mg-ADP + 16 P 
Free-living diazotrophs correspond to a small fraction of the plant rhizospheres ecosystem, and they belong to alphaproteobacteria (RhizobiaBradyrhizobiaRhodobacteria), betaproteobacteria (BurkholderiaNitrosospira), gammaproteobacteria (PseudomonasXanthomonas), firmicutes, and cyanobacteria [20]. However, their presence, function, and importance can be explained by the “black queen” hypothesis which predicts that in free-living microbial communities, only a few “helpers” that carry the heaviest weight in terms of functions, such as high energy-requiring nitrogen fixation, support the rest of the flora and fauna population or the “beneficiaries” that rely on the “helpers” or the “beneficial” for nitrogen needs [21].
The symbiotic relationship between soil bacteria, collectively known as rhizobia (which includes the genera RhizobiumBradyrhizobiumMesorhizobium, and Sinorhizobium), and legume roots generates nodules (a new differentiated special organ) that fix atmospheric nitrogen through the action of the nitrogenase enzyme [22]. BNF by plants and its bacterial associations represent an important natural system for capturing atmospheric N and processing it into a reactive form of nitrogen through enzymatic reduction. BNF is considered an extremely sensitive process influenced by nutrient and environmental conditions and enables a plant to supply all or part of its requirements through interactions with endo-symbiotic, associative, and endophytic symbionts, thus offering a competitive advantage over any non-nitrogen-fixing plants [15][23][24][25][26]. The highly conserved nitrogenase complex in free-living and symbiotic diazotrophs enables them to participate in various types of associations/interactions with their host plants. BNF by plant–rhizobia symbiotic systems is mediated by endosymbiotic interaction when plants develop root nodules; in legumes and rhizobia, gram-negative alpha proteobacteria are the most common microbial species that associate (endo-symbiotic interaction) with legumes of the Fabaceae (Papilionaceae) family [27][28][29]. Actinomycetes such as the Parasponia species (family Cannabaceae) and Frankia sp. that associate with a broad spectrum of actinorhizal plants are well documented in nitrogen fixation as well [8]. Cyanobacteria (mainly Nostoc sp.) have also been found to colonize different plant organs, either intracellularly in the family Gunneraceae or extracellularly in AzollaCycadaceae, liverworts, and hornworts. Associative nitrogen fixation (ANF) and/or endophytic symbioses are often observed among diazotrophs, such as Azospirillum spp., Azoarcus spp. and Herbaspirillum, with a wide variety of plant roots including cereals. The nitrogenase protein, as well as the associated proteins and non-proteins forming nitrogenase enzyme, are sensitive to the presence of oxygen [30]. For this extreme sensitivity to oxygen, obligate anaerobes such as Clostridium pasteurianum are ideal candidates for nitrogen fixation; however, facultative anaerobes such as Klebsiella oxytoca are also capable of fixing nitrogen but only when the oxygen is absent in the system [31]. Obligate aerobes, such as Azotobacter vinelandii can also shield nitrogenase from oxygen and perform nitrogen fixation by consuming oxygen via cytochrome oxidases [31][32].

2.1. The Nitrogenase Protein and Nodule Formation

As mentioned earlier, a protein complex called nitrogenase (composed of enzymes with metal co-factors) makes nitrogen fixation possible in plants. The first one is dinitrogenase and the second one is dinitrogenase reductase [33]. According to the active site co-factor binding metal, there exist three types of dinitrogenase in nature. (a) Molybdenum (Mo) nitrogenase; it is most abundant and carries the most significance in the nitrogen-fixing bacterial and archaeal niche and the alternative vanadium (V) and iron-only (Fe) nitrogenases [34]. The molybdenum-dependent dinitrogenase is formed by nifD and nifK gene products and dinitrogenase reductase is a homodimer of the nifH gene product [30][35]. It is well documented that molybdenum nitrogenase is produced in all diazotrophs in nature, while some produce vanadium or iron nitrogenase in addition to Mo-nitrogenase [36][37]. The rhizobium bacteria residing in nodules fix atmospheric nitrogen gas to NH3, which plants can assimilate via glutamine synthase to form glutamine. In response, the bacteria derive plant carbohydrates, mainly as malate for food and an energy source for nitrogen fixation. Nodules are very complex structures, containing several processes which operate and interact at distinct levels. The process of nodule formation requires a coordinated exchange of signals between the two symbiotic partners [38]. Bacteria had their symbiotic genes first characterized by transposon mutagenesis; this achieved the definition of over 50 nodulation genes (Nod and Nol) in bacteria, and about the same number controlling nitrogen fixation; thus many nod- and fix-bacterial strains exist in many species of rhizobia. Legume–rhizobium symbiosis starts with molecular signaling between the two partners. Early nodulation gene cascades in legumes. Plants release signals such as flavonoids (e.g., the flavone 7,4 dihydroxyflavone and the isoflavone genistein) which are picked up by compatible bacteria in the rhizosphere [39][40] leading to the production of Nod factors (NF) which trigger early events in the nodulation process [41][42]. This triggers the downstream gene cascade including those involved in nucleoporin, cation channels, calcium spiking, early nodule expression, and cytokine signaling leading to cortical and pericyclic cell divisions, and concomitant bacterial infection. Rhizobia are entrapped by root hair curling after the Nod factor has been perceived, which results in initiating the formation of an infection thread (a tubular structure). This infection thread facilitates the penetration of root hair cells and adjacent cortical cells [43]. Cell divisions in cortical and pericycle occur simultaneously resulting in the formation of the nodule primordium. Bacterial cell division facilitates the rhizobial traveling through the infection thread and is eventually freed into the induced nodule primordium cells [44][45]. As nodules mature with time, bacteria are enclosed within the symbiosome membrane, resultant from an inverted plasma membrane of plant origin. In this encapsulated chamber, the bacteria experience a micro-aerobic environment (lower oxygen concentration) and differentiate into bacteroids, fixing diffused nitrogen gas using their nitrogenase enzyme complex [46][47]. Depending on whether or not the meristem remains active for the life of the nodule, two main types of nodules are formed on the various legume species, (i) indeterminate or (ii) determinate. In the case of determinate nodules, nodular meristematic activity is terminated early and is usually initiated sub-epidermally in the outer cortex, thus giving rise to spherical nodules [48]. In indeterminate nodules, the inner cortex undergoes cell division (anticlinally) followed by periclinal divisions in the pericycle. Here, cylindrical nodules are formed due to more persistent meristems [49][50].

2.2. Genes Encoding Nitrogenase Enzyme

The understanding of the genetic basis of this relationship is of paramount importance and essential for the optimization of nitrogen acquisition rates in legumes themselves. Bacterial nif genes are well known to encode the components of the nitrogenase enzyme complex. nifHnifD, and nifK genes encode the structural subunit of di-nitrogenase reductase and the 2 subunits of di-nitrogenase, respectively. Many rhizobial genes have been fully sequenced, for instance, Mesorhizobium lotiSinorhizobium meliloti, and Bradyrhizobium japonicum [51][52][53]. These proteins have similar sequences and common structures and functions in many diazotrophs, for instance, Azotobacter vinelandiiHerbaspirillum seropedicaePseudomonas stutzeri, and Bradyrhizobium japonicum [54][55][56][57]. Furthermore, genetic and biochemical analyses revealed that many additional nif genes, including nifEnifNnifXnifQnif WnifVnifAnifBnifZ, and nifS, play roles in the regulation of nif genes and maturation processes of electron transport and FeMo-cofactor biosynthesis and assembly [58][59]. In addition, the fixABCX genes first identified in Rhizobium meliloti [60][61] and subsequently in other diazotrophs were reported to encode a membrane complex participating in electron transfer to nitrogenase [62]. The degree of specificity between legumes and rhizobia varies. The Nod factors produced by Rhizobium etli and Rhizobium loti produce identical Nod factors; however, they have distinct host ranges (Phaseolus spp. and Lotus spp., respectively) [63]. Moreover, different rhizobia nodulating the same plant may excrete completely different Nod factors. For instance, Rhizobium tropici and R. etli produce different Nod factors (sulfated and acetylfucosylated, respectively), but both are known to nodulate Proteus vulgaris [64]. More examples include Bradyrhizobium elkanii and Bradyrhizobium japonicum, which have a number of mutual hosts, but their Nod factors differ considerably [65].

2.3. Marker-Assisted Selection of Biological Nitrogen-Fixing Plants

Several studies have identified QTL associated with traits related to biological N fixation (Table 1 [66][67][68][69]). The QTL markers can be used in marker-assisted selection for breeding plants with better nitrogen fixation attributes. A QTL for the total ureides (acyl derivatives of urea) was identified on chromosome 17 in soybean which explained 13.26% phenotypic variation [70]. Li and the team [71] cloned a candidate gene associated with a major QTL in soybean for increasing nodule size and named it INCREASING NODULE SIZE1 (GmINS1). The overexpression of GmINS1 increased the N content and the biomass of the soybean plant due to an increase in number, biomass, the abundance of infection cells, and nitrogenase activity of large nodules [71]. The result was the opposite when GmINS1 was suppressed by RNA interference [71].
Table 1. Major genomic loci detected for BNF in different legume species [66][67][68][69].
Species Chromosome Number QTL or Marker Interval Plant Response QTL-Effect, R2 (%)
Common bean (Phaseolus vulgaris L.) 7 Ndfa7.1DB,SA N derived from atmosphere (Ndfa) 14.9
Soybean [Glycine max (L.) Merr.] 16 qBNF-16 Nodule size & number 15.9–59
Soybean [Glycine max (L.) Merr.] 17 qBNF-17 Nodule size & number 12.6–18.6
Lotus japonicus 2 TM0550–TM0324 Acetylene reduction activity per plant (ARA/P) 15.1
Lotus japonicus 2 TM0550–TM0002 ARA per nodule number (ARA/NN) 11.1
Lotus japonicus 4 TM0664 ARA per nodule weight (ARA/NW) 10.8
Lotus japonicus 5 TM1417–TM0095 ARA per nodule weight (ARA/NW) 13
Lotus japonicus 3 TM0083 Nodule number (NN) 21.6
Lotus japonicus 1 TM0113–TM0805 Stem length (SL) 13.3
Lotus japonicus 1 TM0027–TM0063 Shoot length without inoculation (SL bac−) 16.7
Lotus japonicus 1 TM0113–TM0805 Shoot length without inoculation (SL bac−) 16
Lotus japonicus 5 TM0095–TM0909 Shoot dry weight without inoculation (SW bac−) 10.7
Cowpea [Vigna unguiculata (L.) Walp.] 4 (Likage group) 2_12850/2_54418 Nodule number 48.4
Cowpea [Vigna unguiculata (L.) Walp.] 6 (Likage group) 2_11936/2_49231 Nodule fresh weight 21.4


  1. Ney, L.; Franklin, D.; Mahmud, K.; Cabrera, M.; Hancock, D.; Habteselassie, M.; Newcomer, Q.; Fatzinger, B. Rebuilding Soil Ecosystems for Improved Productivity in Biosolarized Soils. Int. J. Agron. 2019, 2019, 5827585.
  2. Vitousek, P.; Howarth, R. Nitrogen limitation on land and in the sea: How can it occur? Biogeochemistry 1991, 13, 87–115.
  3. Hedin, L.O.; Brookshire, E.J.; Menge, D.N.; Barron, A.R. The Nitrogen Paradox in Tropical Forest Ecosystems. Annu. Rev. Ecol. Evol. Syst. 2009, 40, 613–635.
  4. Galloway, J.N.; Townsend, A.R.; Erisman, J.W.; Bekunda, M.; Cai, Z.; Freney, J.R.; Martinelli, L.A.; Seitzinger, S.P.; Sutton, M.A. Transformation of the Nitrogen Cycle: Recent Trends, Questions, and Potential Solutions. Science 2008, 320, 889–892.
  5. Vitousek, P.M.; Menge, D.N.L.; Reed, S.C.; Cleveland, C.C. Biological nitrogen fixation: rates, patterns and ecological controls in terrestrial ecosystems. Philos. Trans. R. Soc. B: Boil. Sci. 2013, 368, 20130119.
  6. Dobermann, A. Nutrient use efficiency—Measurement and management. In Proceedings of the International Fertilizer Industry Association, Brussels, Belgium, 7–9 March 2007; pp. 1–22.
  7. Westhoff, P. The economics of biological nitrogen fixation in the global economy. Agron. Monogr. 2009, 52, 309–328.
  8. Santi, C.; Bogusz, D.; Franche, C. Biological nitrogen fixation in non-legume plants. Ann. Bot. 2013, 111, 743–767.
  9. Da Silva, J.G.; Serra, G.E.; Moreira, J.R.; Conçalves, J.C.; Goldemberg, J. Energy Balance for Ethyl Alcohol Production from Crops. Science 1978, 201, 903–906.
  10. Sulieman, S.; Tran, L. Legume Nitrogen Fixation in a Changing Environment; Springer International Publishing: Cham, Switzerland, 2016.
  11. Lindström, K.; Murwira, M.; Willems, A.; Altier, N. The biodiversity of beneficial microbe-host mutualism: the case of rhizobia. Res. Microbiol. 2010, 161, 453–463.
  12. Dahal, S.; Franklin, D.H.; Cabrera, M.L.; Hancock, D.W.; Stewart, L.; Ney, L.C.; Subedi, A.; Mahmud, K. Spatial Distribution of Inorganic Nitrogen in Pastures as Affected by Management, Landscape, and Cattle Locus. J. Environ. Qual. 2018, 47, 1468–1477.
  13. Franche, C.; Lindström, K.; Elmerich, C. Nitrogen-fixing bacteria associated with leguminous and non-leguminous plants. Plant Soil 2009, 321, 35–59.
  14. Lam, H.-M.; Coschigano, K.T.; Oliveira, I.C.; Melo-Oliveira, R.; Coruzzi, G.M. The molecular-genetics of nitrogen assimilation into amino acids in higher plants. Annu. Rev. Plant Boil. 1996, 47, 569–593.
  15. Graham, P.H. Stress tolerance in Rhizobium and Bradyrhizobium, and nodulation under adverse soil conditions. Can. J. Microbiol. 1992, 38, 475–484.
  16. Peoples, M.B.; Brockwell, J.; Herridge, D.F.; Rochester, I.J.; Alves, B.J.R.; Urquiaga, S.; Boddey, R.M.; Dakora, F.D.; Bhattarai, S.; Maskey, S.L.; et al. The contributions of nitrogen-fixing crop legumes to the productivity of agricultural systems. Symbiosis 2009, 48, 1–17.
  17. Ramírez-Puebla, S.T.; Ormeño-Orrillo, E.; Rogel, M.A.; López-Guerrero, M.G.; López-López, A.; Martínez-Romero, J.; Negrete-Yankelevich, S.; Martínez-Romero, E. La diversidad de rizobios nativos de México a la luz de la genómica. Rev. Mex. Biodivers. 2019, 90, 902681.
  18. Fustec, J.; Lesuffleur, F.; Mahieu, S.; Cliquet, J.-B. Nitrogen rhizodeposition of legumes. A review. Agron. Sustain. Dev. 2010, 30, 57–66.
  19. Rosenblueth, M.; Ormeño-Orrillo, E.; López-López, A.; Rogel, M.A.; Reyes-Hernández, B.J.; Martínez-Romero, J.C.; Reddy, P.M.; Martínez-Romero, E. Nitrogen Fixation in Cereals. Front. Microbiol. 2018, 9, 9.
  20. Morris, J.J.; Schniter, E.J. Black Queen markets: Commensalism, dependency, and the evolution of cooperative specialization in human society. J. Bioecon. 2018, 20, 69–105.
  21. Peix, A.; Ramírez-Bahena, M.H.; Velázquez, E.; Bedmar, E.J. Bacterial associations with legumes. Crit. Rev. Plant Sci. 2015, 34, 17–42.
  22. Graham, P.H.; Vance, C.P. Legumes: Importance and constraints to greater use. Plant Physiol. 2003, 131, 872–877.
  23. King, C.A.; Purcell, L.C. Inhibition of N2 fixation in soybean is associated with elevated ureides and amino acids. Plant Physiol. 2005, 137, 1389–1396.
  24. Liu, Y.; Wu, L.; Baddeley, J.A.; Watson, C.A. Models of Biological Nitrogen Fixation of Legumes. In Sustainable Agriculture; Springer: Dordrecht, The Netherlands, 2011; Volume 2, pp. 883–905.
  25. Purcell, L.C.; Serraj, R.; De Silva, M.; Sinclair, T.R.; Bona, S. Ureide concentration of field-grown soybean in response to drought and the relationship to nitrogen fixation. J. Plant Nutr. 1998, 21, 949–966.
  26. Zahran, H.H. Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol. Mol. Biol. Rev. 1999, 63, 968–989.
  27. Schultze, M.; Kondorosi, A.J. Regulation of symbiotic root nodule development. Annu. Rev. Genet. 1998, 32, 33–57.
  28. Oldroyd, G.E.; Downie, J.A. Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu. Rev. Plant Biol. 2008, 59, 519–546.
  29. Desbrosses, G.J.; Stougaard, J. Root nodulation: A paradigm for how plant-microbe symbiosis influences host developmental pathways. Cell Host Microbe 2011, 10, 348–358.
  30. Burén, S.; Rubio, L.M. State of the art in eukaryotic nitrogenase engineering. FEMS Microbiol. Lett. 2017, 365.
  31. Yates, M.; Jones, C. Respiration and Nitrogen Fixation in Azotobacter. In Advances in Microbial Physiology; Elsevier BV: Amsterdam, The Netherlands, 1974; Volume 11, pp. 97–135.
  32. Poole, R.K.; Hill, S. Respiratory protection of nitrogenase activity in Azotobacter vinelandii—Roles of the terminal oxidases. Biosci. Rep. 1997, 17, 303–317.
  33. Bulen, W.; LeComte, J.J. The nitrogenase system from Azotobacter: Two-enzyme requirement for N2 reduction, ATP-dependent H2 evolution, and ATP hydrolysis. Proc. Natl. Acad. Sci. USA 1966, 56, 979.
  34. Bishop, P.E.; Joerger, R.D. Genetics and molecular biology of alternative nitrogen fixation systems. Annu. Rev. Plant Biol. 1990, 41, 109–125.
  35. Shah, V.K.; Brill, W.J. Isolation of an iron-molybdenum cofactor from nitrogenase. Proc. Natl. Acad. Sci. USA 1977, 74, 3249–3253.
  36. Dos Santos, P.C.; Fang, Z.; Mason, S.W.; Setubal, J.C.; Dixon, R. Distribution of nitrogen fixation and nitrogenase-like sequences amongst microbial genomes. BMC Genom. 2012, 13, 162.
  37. McGlynn, S.E.; Boyd, E.S.; Peters, J.W.; Orphan, V.J. Classifying the metal dependence of uncharacterized nitrogenases. Front. Microbiol. 2013, 3, 419.
  38. Biswas, B.; Gresshoff, P.M. The role of symbiotic nitrogen fixation in sustainable production of biofuels. Int. J. Mol. Sci. 2014, 15, 7380–7397.
  39. Spaink, H.P. Root nodulation and infection factors produced by rhizobial bacteria. Annu. Rev. Microbiol. 2000, 54, 257–288.
  40. Redmond, J.W.; Batley, M.; Djordjevic, M.A.; Innes, R.W.; Kuempel, P.L.; Rolfe, B.G. Flavones induce expression of nodulation genes in Rhizobium. Nature 1986, 323, 632–635.
  41. Caetano-Anollés, G.; Gresshoff, P.M. Plant genetic control of nodulation. Annu. Rev. Microbiol. 1991, 45, 345–382.
  42. Denarie, J.; Debelle, F.; Prome, J.-C. Rhizobium lipo-chitooligosaccharide nodulation factors: Signaling molecules mediating recognition and morphogenesis. Annu. Rev. Biochem. 1996, 65, 503–535.
  43. Szczyglowski, K.; Shaw, R.S.; Wopereis, J.; Copeland, S.; Hamburger, D.; Kasiborski, B.; Dazzo, F.B.; De Bruijn, F.J. Nodule Organogenesis and Symbiotic Mutants of the Model Legume Lotus japonicus. Mol. Plant-Microbe Interact. 1998, 11, 684–697.
  44. Calvert, H.E.; Pence, M.K.; Pierce, M.; Malik, N.S.A.; Bauer, W.D. Anatomical analysis of the development and distribution of Rhizobium infections in soybean roots. Can. J. Bot. 1984, 62, 2375–2384.
  45. Mathews, A.; Carroll, B.; Gresshoff, P.J.P. Development of Bradyrhizobium infections in supernodulating and non-nodulating mutants of soybean (Glycine max Merrill). Protoplasma 1989, 150, 40–47.
  46. Gresshoff, P.M.; Delves, A.C. Plant genetic approaches to symbiotic nodulation and nitrogen fixation in legumes. In Plant Gene Research; Springer Science and Business Media LLC: Vienna, Austria, 1986; pp. 159–206.
  47. Timmers, A.; Auriac, M.-C.; Truchet, G.J.D. Refined analysis of early symbiotic steps of the Rhizobium-Medicago interaction in relationship with microtubular cytoskeleton rearrangements. Development 1999, 126, 3617–3628.
  48. Wopereis, J.; Pajuelo, E.; Dazzo, F.B.; Jiang, Q.; Gresshoff, P.M.; De Bruijn, F.J.; Stougaard, J.; Szczyglowski, K. Short root mutant of Lotus japonicus with a dramatically altered symbiotic phenotype. Plant J. 2000, 23, 97–114.
  49. Newcomb, W.; Sippell, D.; Peterson, R.J. The early morphogenesis of Glycine max and Pisum sativum root nodules. Can. J. Bot. 1979, 57, 2603–2616.
  50. Rolfe, B.G.; Gresshoff, P.J.; Biology, P.M. Genetic analysis of legume nodule initiation. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1988, 39, 297–319.
  51. Galibert, F.; Finan, T.M.; Long, S.R.; Pühler, A.; Abola, P.; Ampe, F.; Barloy-Hubler, F.; Barnett, M.J.; Becker, A.; Boistard, P.; et al. The Composite Genome of the Legume Symbiont Sinorhizobium meliloti. Science 2001, 293, 668–672.
  52. Giraud, E.; Moulin, L.; Vallenet, D.; Barbe, V.; Cytryn, E.; Avarre, J.-C.; Jaubert, M.; Simon, D.; Cartieaux, F.; Prin, Y.; et al. Legumes Symbioses: Absence of Nod Genes in Photosynthetic Bradyrhizobia. Science 2007, 316, 1307–1312.
  53. Kaneko, T.; Nakamura, Y.; Sato, S.; Asamizu, E.; Kato, T.; Sasamoto, S.; Watanabe, A.; Idesawa, K.; Ishikawa, A.; Kawashima, K.; et al. Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti. DNA Res. 2000, 7, 331–338.
  54. Adams, T.H.; McClung, C.R.; Chelm, B.K. Physical organization of the Bradyrhizobium japonicum nitrogenase gene region. J. Bacteriol. 1984, 159, 857–862.
  55. Jacobson, M.R.; Brigle, K.E.; Bennett, L.T.; Setterquist, R.A.; Wilson, M.S.; Cash, V.L.; Beynon, J.; Newton, W.E.; Dean, D.R. Physical and genetic map of the major nif gene cluster from Azotobacter vinelandii. J. Bacteriol. 1989, 171, 1017–1027.
  56. Pedrosa, F.; Teixeira, K.; Machado, I.; Steffens, M.; Klassen, G.; Benelli, E.; Machado, H.; Funayama, S.; Rigo, L.; Ishida, M.; et al. Structural organization and regulation of the nif genes of Herbaspirillum seropedicae. Soil Boil. Biochem. 1997, 29, 843–846.
  57. Yan, Y.; Yang, J.; Dou, Y.; Chen, M.; Ping, S.; Peng, J.; Lu, W.; Zhang, W.; Yao, Z.; Li, H.; et al. Nitrogen fixation island and rhizosphere competence traits in the genome of root-associated Pseudomonas stutzeri A1501. Proc. Natl. Acad. Sci. USA 2008, 105, 7564–7569.
  58. Masepohl, B.; Drepper, T.; Paschen, A.; Gross, S.; Pawlowski, A.; Raabe, K.; Riedel, K.-U.; Klipp, W. Regulation of nitrogen fixation in the phototrophic purple bacterium Rhodobacter capsulatus. J. Mol. Microbiol. Biotechnol. 2002, 4, 243–248.
  59. Lee, S.; Reth, A.; Meletzus, D.; Sevilla, M.; Kennedy, C. Characterization of a Major Cluster of nif,fix, and Associated Genes in a Sugarcane Endophyte,Acetobacter diazotrophicus. J. Bacteriol. 2000, 182, 7088–7091.
  60. Kallas, T.; Coursin, T.; Rippka, R.J. Different organization of nif genes in nonheterocystous and heterocystous cyanobacteria. Plant Mol. Biol. 1985, 5, 321–329.
  61. Earl, C.; Ronson, C.; Ausubel, F.J. Genetic and structural analysis of the Rhizobium meliloti fixA, fixB, fixC, and fixX genes. J. Bacteriol. 1987, 169, 1127–1136.
  62. Edgren, T.; Nordlund, S.J. The fixABCX genes in Rhodospirillum rubrum encode a putative membrane complex participating in electron transfer to nitrogenase. J. Bacteriol. 2004, 186, 2052–2060.
  63. Cárdenas, L.; Domínguez, J.; Quinto, C.; López-Lara, I.M.; Lugtenberg, B.J.; Spaink, H.P.; Rademaker, G.J.; Haverkamp, J.; Thomas-Oates, J.E. Isolation, chemical structures and biological activity of the lipo-chitin oligosaccharide nodulation signals from Rhizobium etli. Plant Mol. Boil. 1995, 29, 453–464.
  64. Mus, F.; Crook, M.B.; Garcia, K.; Costas, A.G.; Geddes, B.A.; Kouri, E.D.; Paramasivan, P.; Ryu, M.-H.; Oldroyd, G.E.D.; Poole, P.S.; et al. Symbiotic Nitrogen Fixation and the Challenges to Its Extension to Nonlegumes. Appl. Environ. Microbiol. 2016, 82, 3698–3710.
  65. Perret, X.; Staehelin, C.; Broughton, W.J. Molecular basis of symbiotic promiscuity. Microbiol. Mol. Biol. Rev. 2000, 64, 180–201.
  66. Kamfwa, K.; Cichy, K.A.; Kelly, J.D. Identification of quantitative trait loci for symbiotic nitrogen fixation in common bean. Theor. Appl. Genet. 2019, 132, 1375–1387.
  67. Ohlson, E.W.; Seido, S.L.; Mohammed, S.; Santos, C.A.F.; Timko, M.P. QTL Mapping of Ineffective Nodulation and Nitrogen Utilization-Related Traits in the IC-1 Mutant of Cowpea. Crop Sci. 2018, 58, 264–272.
  68. Tominaga, A.; Gondo, T.; Akashi, R.; Zheng, S.H.; Arima, S.; Suzuki, A. Quantitative trait locus analysis of symbiotic nitrogen fixation activity in the model legume Lotus japonicus. J. Plant Res. 2012, 125, 395–406.
  69. Yang, J.; Xie, X.; Yang, M.; Dixon, R.; Wang, Y.-P. Modular electron-transport chains from eukaryotic organelles function to support nitrogenase activity. Proc. Natl. Acad. Sci. USA 2017, 114, E2460–E2465.
  70. Muñoz, N.; Qi, X.; Li, M.-W.; Xie, M.; Gao, Y.; Cheung, M.-Y.; Wong, F.-L.; Lam, H.-M. Improvement in nitrogen fixation capacity could be part of the domestication process in soybean. Heredity 2016, 117, 84–93.
  71. Li, X.; Zheng, J.; Yang, Y.; Liao, H. INCREASING NODULE SIZE1 Expression Is Required for Normal Rhizobial Symbiosis and Nodule Development. Plant Physiol. 2018, 178, 1233–1248.
Contributor MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to :
View Times: 1060
Revisions: 2 times (View History)
Update Date: 24 Nov 2021