(, Khammas However, in response to the cellular N-content and the oxygen tension, A. brasilense NifA activity is modulated [158]. The regulation of nif transcription involves a different regulatory system, rather than the ntr system. Although structurally similar to PII, the PZ protein seems to be functionally different. T. J. L. de Zamaroczy So far, studies concerning these bacteria mainly dealt with establishing their endophytic nature. A similar increase of nitrogen fixation capability in the presence of WGA has been demonstrated in A. lipoferum[91]. M.G. ), pp. (, Austin The Alphaproteobacterial class of Azospirillum include physiologically distinct, rhizosphere competent, plant growth-promoting bacteria (PGPB) that promote the growth of a wide range of plants through diverse, direct and indirect mechanisms [1, 2].Nitrogen fixation is not the most significant field function of this bacterial group, and it is the production of the plant growth regulators … draTG from A. brasilense and A. lipoferum have been cloned and sequenced [25–27]. Karpati S. J. I. In such a simple case, a particular signal would cause the simultaneous activation of DRAT and inactivation of DRAG, whereas the absence of that signal would cause the reverse. J. ), pp. I. Verreth Döbereiner (1989) Isolation and properties of Azospirillum lipoferum and Azospirillum brasilense surface polysaccharide mutants. It furthers the University's objective of excellence in research, scholarship, and education by publishing worldwide, This PDF is available to Subscribers Only. These characteristics, together with the endophytic nature of the A. diazotrophicus and H. seropedicae plant interactions holds promise, as nitrogen fixed by these bacteria might be far more available to the plant than in the rhizosphere associations. Of the two motifs known to be essential for feedback inhibition of anthranilate synthase by Trp, only one has been located in A. brasilense TrpE(G). A. brasilense NifA protein activity Brazilian Journal of Medical and Biological Research (1998) 31: 1363-1374 ISSN 0100-879X Purification and binding analysis of the nitrogen fixation regulatory NifA protein from Azospirillum brasilense Departamentos de 1Biotecnologia and … (, Dörr M.A. Merrick, M.J. (1992) Regulation of nitrogen fixation genes in free-living and symbiotic bacteria. The A. brasilense exoC correcting locus apparently encodes an enzymatic activity different from the one that is missing in the R. meliloti exoC mutant (phosphoglucomutase). B. Enderlin In enteric bacteria the global nitrogen regulatory system (ntr) depends on four gene products (GlnD, GlnB, NtrBC) and controls the expression of several N-regulated operons, including the nitrogen fixation operon nifLA[143]. J. Fuentes-Ramirez Elmerich However, the plant root interaction by other associative nitrogen-fixing bacteria, like A. diazotrophicus, H. seropedicae and Azoarcus, clearly displays an endophytic character [42]. Microbiol. A. Nur et al. Vanderleyden de Zamaroczy, M., Delorme, F. and Elmerich, C. (, de Zamaroczy, M., Paquelin, A. and Elmerich, C. (, de Zamaroczy, M., Paquelin, A., Peltre, G., Forchhammer, K. and Elmerich, C. (. Armitage Dixon Blum Bacterial species discussed in this review are listed in Table 1. L.U. (, Sevilla Hartmann However, the glnB gene product is not essential for nitrogen fixation [41]. A.C.G. has been isolated from Kallar grass grown in saline soils in Pakistan [64–66] and was repeatedly found inside Kallar grass roots, where it is thought to benefit from a more efficient transfer of metabolites between host and diazotrophs [67]. J. A. Van Bastelaere The recent discovery of a PII-like protein encoded by glnK in A. vinelandii, supports a similar mechanism of regulation of NifL activity in response to fixed N [141, 142]. A major outer membrane protein of about 42 kDa (MOMP) has been identified in A. brasilense. An A. brasilense gene encoding this N-regulated ammonium transporter (amtB) has been characterized [138]. The primary effect of ntrBC mutations probably involves changes in DraG activity [144, 145, 181]. (, Castellanos nitrogen fixers ( Sivasakthivelan and Saranraj, 2013 ). DNA hybridization experiments suggested that the corresponding sequence is widespread in A. brasilense, A. lipoferum, A. halopraeferens, but absent in A. irakense. Both in greenhouse and in field trials, Azospirillum was shown to exert beneficial effects on plant growth and crop yields [5, 6]. Detail of the mechanisms for the regulation of DRAT and DRAG activities are still unknown. The N-terminal domain of all NifA proteins shows a low degree of sequence similarity [120, 122, 126, 157]. Dixon At present, five species have been described: Azospirillum lipoferum, Azospirillum brasilense[7], Azospirillum amazonense[8], Azospirillum halopraeferens[9] and Azospirillum irakense[10]. 18, 1990. Janssens Laboratory of Genetics, Katholieke Universiteit Leuven, Kard. R.J. It is considered a free-living soil bacterium that has the ability to affect the growth of numerous agricultural crops worldwide through the excretion of various hormones and the bacteria’s ability of nitrogen fixation. Springer, Berlin. Reis Bacteriol. (, Reinhold-Hurek An increased number of lateral roots and root hairs enlarges the root surface available for nutrients. C. C. (, Pelanda On the other hand, NifA activity is controlled by the inhibitor protein NifL, both in response to oxygen and to fixed nitrogen. Less knowledge has been attained at the genetic level. A recently characterized glnD (UTase) null-mutant strain exhibits a Nif− phenotype, confirming that PII-UMP is the active form required for NifA activation [160]. In: Nitrogen Fixation with Non-legumes (Skinner, F.A., Boddey, R.M. Both PII and PZ were demonstrated to be uridylylated under N-limiting conditions, most probably at a conserved tyrosine residue (Tyr-51). 77–89. Van Dommelen, A. Baldani This is due to reduced DRAG protein in this mutant. M. IAM, indole-3-acetamide; IPyA, indole-3-pyruvic acid; IAAld, indole-3-acetaldehyde; IAA, indole-3-acetic acid; X, unknown precursor; AS, anthranilate synthase; TMO, tryptophan-2-monooxygenase; AAT, aromatic amino acid aminotransferase. Within the phylum of Proteobacteria there are multiple subgroups; A.brasilense belongs to th… Moreover, these studies provided evidence for the presence of an additional Trp-independent pathway of IAA biosynthesis in A. brasilense (Fig. Antonyuk, L., Fomina, O., Kalinina, A., Semenov, S., Nesmeyanova, M. and Ignatov, V. (1995) Wheat lectin possibly serves as a signal molecule in the Azospirillum-wheat association. (, Westby De Troch A. brasilense strains with mutations in draTG were constructed and physiologically characterized[27]. V.V. ), pp. A. Many countries use bacterial inoculants containing A.brasilense alone or in concert with other plant growth promoting bacteria. Other free‐living diazotrophs repeatedly detected in association with plant roots, include Acetobacter diazotrophicus, Herbaspirillum seropedicae, Azoarcusspp. However, its level of expression is lower under conditions incompatible with N2 fixation [120, 158]. C. (, Lambrecht These findings and the recognition of a TGTCCC element, reminiscent of auxin responsive elements (AuxRE) in plants, make the presence of proteins for IAA binding and signal transduction likely [202]. Nitrogen-fixing Azoarcus cells developed into a hyperinduced state under certain conditions in empirically optimized batch cultures, in response to a shift to extremely low oxygen concentrations [211]. (1994) Azospirillum/plant associations, pp. (, Lopez-de-Victoria P.A. E.K. Bespalov Martinez-Romero Kennedy However, a recent draTG-lac Z fusion study in A. lipoferum showed that draTG expression can be repressed by O2[26]. Addition of NH+4 can then completely eliminate this residual activity[9]. Dean H.-M. Lawrence K. Yates Alvarez 835–876. Vanderleyden Hill T. (. J.I. Keijers Monitoring the expression of putative Azospirillum–plant interaction genes during plant association by the use of reporter genes, and the application of strains carrying mutations in those genes, may lead to a better understanding of the bacterial determinants controlling this association, and may therefore constitute an important step towards engineering and exploitation of more efficient plant growth-promoting Azospirillum strains. By assaying the ability of truncated NifA proteins to drive nifH–lacZ transcription in the absence or presence of ammonium in wild-type and mutant strains, it has been proposed that the N-terminal domain of NifA is involved in the negative regulation of its own activity in the presence of ammonium. Both A. brasilense DraT and DraG themselves are subject to posttranslational regulation [179]. Caruso K.W. CRC Press, Boca Raton, FL. M. The attempt to isolate plant-inducible bacterial genes of A. brasilense, based on analysis of protein patterns of bacteria grown in the presence and absence of plant root exudates, resulted in the identification of an acidic 40-kDa protein, SbpA. H.K. J. The plants were fertilized at seeding with a limiting amount of combined nitrogen and maintained with an … The microbial dimension of submarine groundwater discharge: current challenges and future directions, Verrucomicrobial methanotrophs: ecophysiology of metabolically versatile acidophiles, Functional hydrocolloids, gut microbiota and health: picking food additives for personalized nutrition, About the Federation of European Microbiological Societies, 5 Production of plant growth regulating substances, https://doi.org/10.1111/j.1574-6976.2000.tb00552.x, Receive exclusive offers and updates from Oxford Academic, Factors affecting poly-β-hydroxybutyrate accumulation in cyanobacteria and in purple non-sulfur bacteria, Cellular differentiation and the NtcA transcription factor in filamentous cyanobacteria, Hydrogen metabolism and energy costs of nitrogen fixation, Roots and rhizosphere soil of Gramineae, Amazon region, BrazilÂ, Roots of Kallar grass, grown in saline soils in PakistanÂ, Cereal roots (maize, sorghum, rice), BrazilÂ, Genes encoding glycosyl hydrolases of family 3Â, Motility, synthesis/functioning lateral flagellaÂ, Motility, synthesis/functioning lateral and polar flagellaÂ, Regulator which controls CPS production, flocculation, wheat root colonizationÂ, Chromosomal virulence gene required for plant infection by, Structural gene dinitrogenase reductase (Fe protein)Â, Structural gene dinitrogenase (MoFe protein, α-subunit)Â, Structural gene dinitrogenase (MoFe protein, β-subunit)Â, Transcriptional activator of the nitrogen fixation (, Uridylyltransferase/uridylyl-removing enzyme (UTase/UR)Â, Sensor protein of two-component regulatory system involved in general nitrogen controlÂ, Regulator protein of two-component regulatory system involved in general nitrogen controlÂ, Dinitrogenase reductase ADP ribosyl-transferaseÂ, Dinitrogenase reductase activating glycohydrolaseÂ, Copyright © 2021 Federation of European Microbiological Societies. Steffens M.J. F. For full access to this pdf, sign in to an existing account, or purchase an annual subscription. Searle-van Leeuwen Feeding experiments with 3H-Trp and 3H-IAM confirmed the existence of two Trp-dependent pathways. Many factors appear to affect the association between Azospirillum and the plant. Ali J. However, the mechanism for this inhibition appears to be different from ADP-ribosylation [183]. It has been found in high numbers inside roots, stems and leaves of these graminaceous plants [57], but not within leaves of sugar cane [62]. Kaiser (, Del Gallo In: Nitrogen Fixation with Non-legumes (Hegazi, N.A., Fayez, M. and Monib, M., Eds. Hurek was shown to invade Kallar grass roots inter- and intracellularly, where it infects the cortex region and penetrates the stele of the roots [67, 68]. A. Unlike DRAT, however, the regulation of DRAG is not transient, but reflects the current physiological status. Abstract. They display a versatile C- and N-metabolism, which makes them well adapted to establish in the competitive environment of the rhizosphere. (, Milcamps K. Bacteria belonging to the genus Azospirillum are highly motile. Unlike regulation seen in Klebsiella pneumoniae, transcription of nifA does not require NTRB/NTRC in A. brasilense and the expression of nifHDK is controlled by posttranslational regulation of NIFA activity. Two glnB-like genes have been reported in H. seropedicae, of which one has been sequenced. S. (, Machado (, Fischer J. Syst. Nitrogen fixation structural genes (nif) are highly conserved among all nitrogen-fixing bacteria, and in all diazotrophic species of the class of proteobacteria examined, the transcriptional activator NifA is required for expression of other nif genes in response to two major environmental signals (oxygen and fixed N). Croonenborghs Vanstockem (, Hartmann Doetsch (, Reinhold A. diazotrophicus has been found almost exclusively in association with sugar-rich plants, such as sugar cane, sweet potato and Cameroon grass [51–53] and was shown to be completely absent in the soil [54]. American University in Cairo Press, Cairo. (, Magalhães Smirnoff Y.M. (, Malik From studies with transcriptional nifA–lacZ and nifL–lacZ fusions, A. vinelandii nifLA appears to be constitutively expressed [165, 166]. S. All characterized NifA proteins have the three-domain structure characteristic of the family of σ54-dependent activator proteins. F.O. Hartmann J. I. (1988) Purification and characterization of ADP-ribosylarginine hydrolase from turkey erythrocytes. Buck The subsequent oxidation reaction results in IAA formation (Fig. P. Although no specific effector has been identified for the signal transduction of negative stimuli to DRAT/DRAG system, it might involve a general signal transduction pathway. Woese I. In A. brasilense nifA is constitutively expressed independently of the presence of combined N or of the oxygen concentration. DraG is active under nitrogen fixation conditions and is inactivated by a negative stimulus. Complete genome sequence of the methanogenic archaeon, Isolation and properties of an NAD- and guanidine-dependent ADP-ribosyltransferase from turkey erythrocytes, Purification and partial characterization of arginine-specific ADP-ribosyltransferase from skeletal muscle microsomal membranes, Arginine-specific ADP-ribosyltransferase from rabbit skeletal muscle sarcoplasmic reticulum is solubilized as the active form with trypsin: partial purification and characterization, Amino acid-specific ADP-ribosylation: Evidence for two distinct NAD:arginine ADP-ribosyltransferases in turkey erythrocytes, Sequence of a chicken erythroblast mono(ADP-ribosyl)transferase-encoding gene and its upstream region, Molecular characterization of a glycosylphosphatidylinositol-linked ADP-ribosyltransferase from lymphocytes, Cloning and characterization of a novel membrane-associated lymphocyte NAD:arginine ADP-ribosyltransferase, Cloning and expression of cDNA for arginine-specific ADP-ribosyltransferase from chicken bone marrow cells, Molecular characterization of NAD:arginine ADP-ribosyltransferase from rabbit skeletal muscle, Three conserved consensus sequences identify the NAD-binding site of ADP-ribosylating enzymes, expressed by eukaryotes, bacteria and T-even bacteriophages, Molecular and immunological characterization of ADP-ribosylarginine hydrolases, Cloning and site-directed mutagenesis of human ADP-ribosylarginine hydrolase. In Azotobacter vinelandii (γ-subgroup) nifA is cotranscribed with a second gene nifL. An alternative mechanism of posttranslational regulation of nitrogenase in response to ammonium has been suggested based on the finding that strains, expressing a dinitrogenase reductase that could not be ADP-ribosylated, still showed partially NH4+ inhibited nitrogenase activity [182]. Lory J. Van Montagu Labandera-Gonzalez Elmerich Perroud Pedrosa ), pp. Vanderleyden B. S. The structural organization of the A. brasilense GS encoding region differs substantially from the glnA–ntrBC operon of enteric bacteria and Azotobacter [41, 121, 135]. Edwards H.B. Rigo ADP-ribosyltransferases have been found in many animal tissues, and purified from turkey erythrocytes, rabbit skeletal muscle and other tissues [57–60]. S. Vanderleyden Ritchings Enhanced NH4+ excretion could be achieved by preventing ammonium assimilation. Hampel The nifL gene product inactivates NifA in response to high oxygen tension and cellular nitrogen-status. T. De Mot Evidence of a nifA-like gene A. brasilense was first obtained by Pedrosa and Yates (1984) by the isolation and characterization of a nifA mutant strain (FP10) . ), pp. Maris Henrissat P. Wheat germ agglutinin (WGA) has been proposed as a signal molecule in the association between Azospirillum and wheat roots. R.M. Nitrogen-fixation by Azospirillum brasilense CD is promoted when co-cultured with a mangrove rhizosphere bacterium (Staphylococcus sp.) J.W. L.T. Negi ), pp. S. (, Jacobson G. R. The conventional molybdenum nitrogenase is encoded by the nifHDK genes. K. M. Fuentes-Ramirez (, Raina carotovora exhibited reduced virulence in surface-inoculated tobacco plants and in stem-inoculated potato plants. F. Y. Vanderleyden R.A. Martinez-Toledo T. (, Barbieri ), pp. Chubatsu The nucleotide sequence of the ipdC gene has previously been reported for Enterobacter cloacae[199] and, more recently, for Erwinia herbicola[200]. Austin Four aspects of the Azospirillum–plant root interaction are highlighted: natural habitat, plant root interaction, nitrogen fixation and biosynthesis of plant growth hormones. Furthermore, flagella are designated functions in several attachment processes, including a number of bacteria–plant interactions [78]. F.M. Vanderleyden Quite recently, experimental data were presented that show intercellular root colonization of Arabidopsis thaliana (dicot) by H. seropedicae. (, Faure L.U. J.P. The benefits to plants by inoculation with Azospirillum have been primarily attributed to its capacity to fix atmospheric nitrogen, but also to its capacity to synthesize phytohormones, in particular indole-3-acetic acid. Effects of temperature, pH, NaC1 and Zn on the nitrogen-fixing potential of the strains in batch culture were studied. Indeed, some mutants which are resistant to ammonium analogs exhibit high nitrogenase activity even in the presence of high concentration of NH+4, indicating that these mutations have effects on both transcriptional and posttranslational regulatory pathways. de Bruijn Vanderleyden Similarly, sequences identical to the σ54 consensus sequence and NifA binding sites in the promoter region of H. seropedicae nifB and nifH and A. diazotrophicus nifB, suggested that nif gene expression in these organisms is likely to require NtrA and NifA [125–127, 157]. The inactivation of DRAG has been demonstrated with pulse-chase experiments[32]. J.D. A steady residual nitrogenase activity has been found under anaerobic conditions for A. brasilense and under NH+4 and darkness for R. rubrum. Dosselaere P.A. A. Cocking The A. brasilense exoC locus encodes a protein that displays significant homology with the P. aeruginosa algC gene product. In a first step, the bacteria adsorb to the roots as single cells in a rapid, weak and reversible way. R. Kluwer Academic, Dordrecht. M. The model for the ADP-ribosylation of dinitrogenase reductase is shown in Fig. Hurek Cannon M. F. Recently, a second PII-like protein (PZ) has been identified in A. brasilense. C. A. brasilense ntrBC mutants escape nitrogenase switch-off by ammonium. This behavioral response can be advantageous to guide the bacteria to optimal niches for nitrogen fixation [27]. Kirchhof F. B.L. The physiological signals responsive to anaerobiosis or fixed N and acting on DraT/DraG, however, still remain to be elucidated. Both genes are cotranscribed and their levels of expression are not significantly influenced by the fixed N supply. For example, both DRAT and DRAG are inactive after prolonged treatment with negative stimuli[9]. Two enzymes perform this reversible reaction. A. Olivares By means of strain-specific monoclonal antibodies and immunological techniques, A. brasilense Sp245 was detected in the root xylem of a particular Brazilian wheat cultivar, while A. brasilense Sp7 only colonized the root surface [45]. (. (. Vanderleyden B. Contrary to glnB, glnZ expression requires the transcriptional activator NtrC in conditions of nitrogen fixation as well as of ammonium assimilation. This indicates that free swimming through water films in the soil rather than swarming plays a major role in chemotactic behavior in natural environments. de Wilde Hill Heterologous expression of draTG from A. brasilense and R. rubrum in K. pneumoniae, which lacks this regulatory system, supports an appropriate regulation of its nitrogenase activity in response to NH+4[48]. Extracellular polysaccharide production has also been related to the process of flocculation of Azospirillum cells and might be similar to the fibrillar material produced during root association [85, 86]. In a glnK null mutant strain, NifA activity is inhibited by NifL even in the absence of fixed N, suggesting a role for the second PII-like protein, either directly or indirectly, in relieving NifL inhibition [172]. E. (, Benelli Chapman and Hall, New York. Bilal A. E.R. This physiological state of high respiration and N2 fixation rates is paralleled by the induction of complex intracytoplasmic membrane stacks, referred to as ‘diazosomes’[212, 213]. ), pp. R.H. Schrank H. V.M. D.H. 175. G. M. F. For example, A. brasilense DraG− displays about 25% residual nitrogenase activity after a shift to anaerobic conditions. Azospirillum lipoferum and A. brasilense have been reported to exert beneficial effects on the productivity of different crops (Cassán and Diaz-Zorita, 2016). T. Hill Vanderleyden Elmerich (, Zhang The sites of primary colonization seem to be the root tips at the zone of elongation and differentiation, and the points of lateral root emergence [67]. H. (, Onyeocha Okon J. T. Döbereiner H.B. A. Van Dommelen P. Although clearly N-regulated, expression of glnB-glnA does not involve NtrC, but requires an alternative transcriptional activator. Philip-Hollingsworth S.K. G. After returning cells to nitrogen-fixing conditions (stage D), DRAG becomes activated, and it removes the ADP-ribose from dinitrogenase reductase, thus restoring its activity. Mehnaz Croes (, Olivares (, Dobbelaere Monitoring the colonization pattern of A. brasilense Sp245 on wheat roots, using a constitutively expressed Escherichia coli gusA gene, it was shown that the sites of primary root colonization are the points of lateral root emergence and the root hair zones [44]. Springer, Basel. (, Arsène E. Döbereiner Bali Woodley J.I. M. Bacterial phytohormone production and nitrogen fixation are recognized as processes potentially involved in plant growth promotion by Azospirillum. Since Trp is a precursor for IAA synthesis, research has focused on elucidating the biosynthetic pathway for the production of this amino acid. D.A. Pz is expressed both under nitrogen-fixing and nitrogen excess conditions, and its function is unknown. T. Hennecke This is in agreement with the lack of σ54 and NtrC recognition motifs. Okon, Y. Nevertheless, the indole-3-pyruvate decarboxylase encoding ipdC gene is crucial in the overall IAA biosynthesis in Azospirillum. The role of the PZ protein in the nitrogen regulation cascade remains unclear [140, 146]. (, Reis Azospirillumrepresents the best characterized genus of plant growth‐promoting rhizobacteria. The presence of a −24/−12 consensus sequence and an NifA binding site in the nifA promoter region, favors the idea that NifA may autoregulate its own synthesis. Humphrey In: Azospirillum III: Genetics, Physiology, Ecology (Klingmüller, W., Ed. An A. brasilense ipdC knock-out mutant was found to synthesize less than 10% of the level of wild-type IAA production, indicating that IPyA decarboxylase is a key enzyme for IAA biosynthesis in this bacterium [193]. (, Moshiri F. Furthermore, it has been hypothesized that root lectins are involved in the process of root colonization [32]. B. Vanderleyden E.M.