Environment Health Techniques Sphere of influence of IAA and NO in bacteria
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Review Sphere of influence of indole acetic acid and nitric oxide in bacteria Vatsala Koul, Alok Adholeya and Mandira Kochar TERI Deakin Nanobiotechnology Centre, Biotechnology and Bioresources Division, The Energy and Resources Institute, Darbari Seth Block, India Habitat Centre, Lodhi Road, New Delhi, India
Bacterial biosynthesis of the phytohormone, indole-3-acetic acid (IAA) is well established and along with the diffusible gaseous molecule, nitric oxide (NO) is known to positively regulate the developmental processes of plant roots. IAA and NO act as signaling molecules in plant–microbe interactions as they modulate the gene expression in both, plants and microorganisms. Although IAA and NO may not be required for essential bacterial physiological processes, numerous studies point towards a crosstalk between IAA and NO in the rhizosphere. In this review, we describe various IAA and NO-responsive or sensing genes/proteins/regulators. There is also growing evidence for the interaction of IAA and NO with other plant growth regulators and the involvement of NO with the quorum sensing system in biofilm formation and virulence. This interactive network can greatly impact the host plant–microbe interactions in the soil. Coupled with this, the specialized s54-dependent transcription observed in some of the IAA and NO-influenced genes can confer inducibility to these traits in bacteria and may allow the expression of IAA and NO-influenced microbial genes in nutrient limiting or changing environmental conditions for the benefit of plants. Keywords: Indole acetic acid / Nitric oxide / Plant growth promoting bacteria Received: March 17, 2014; accepted: April 26, 2014 DOI 10.1002/jobm.201400224
Introduction Plant growth promoting (PGP) bacteria Azospirillum, Azotobacter, Bacillus, Pseudomonas, Rhizobium, Bradyrhizobium, and others enhance plant growth either directly by producing growth metabolites (phytohormones and other plant growth regulators) and increasing available nutrient uptake (phosphate solubilization and accelerating mineralization) or indirectly by biologically controlling plant diseases (complex antibiotics and siderophores) [1–6]. In recent times, nitric oxide (NO) has emerged as an essential, multifunctional, diffusible cell signaling molecule not only in animals but also plants and bacteria. In humans, its involvement in multiple biological functions
Correspondence: Mandira Kochar, TERI Deakin Nanobiotechnology Centre, Biotechnology and Bioresources Division, The Energy and Resources Institute, Darbari Seth Block, India Habitat Centre, Lodhi Road, New Delhi 110003, India E-mail: [email protected], [email protected] Phone: þ91 11 24682100 Fax: þ91 11 24682144 ß 2014 WILEY-VCH Verlag GmbH & Co. KGaA,Weinheim
like neurotransmission, platelet aggregation, egg fertilization, cardiovascular, and immune responses is well elucidated [7–9]. In plants too, it plays an essential role in actions like programmed cell death, stomatal closure, seed dormancy, stress physiology, and many others [9– 11]. However, the exact mechanism of NO action and interaction with other molecules is yet to be conclusively understood. With increasing research focusing on NO, it has come up as an essential intermediary signaling molecule in plant–microbe interactions although most of the information available till date is from plants [4, 12– 16]. In bacteria, two main pathways exist for the production of NO, arginine (Arg)-dependent and Argindependent. The key gene involved in the Arg-dependent pathway is nitric oxide synthase (nos) [9, 17] whereas in the latter, the genes involved are nitrate reductase (nar) and nitrite reductase (nir) [4, 5]. Indole-3-acetic acid (IAA) plays an indispensible role in coordination of plant growth and development [reviewed in Ref. [18]] and has been established as a crucial player in various plant–microbe interactions [19–21]. Although
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IAA production in plants and bacteria share similar biosynthesis pathways, the documented pathways in bacteria are largely classified as tryptophan (Trp)dependent and Trp-independent pathways [22, 23]. Recent advances highlight that both IAA and NO modulate the expression of genes and accumulation of signaling molecules that are a part of essential transduction cascades [2, 6, 22, 24–27]. Results presented in earlier reports confirm that in plants there is a correlation between the NO and IAA levels as observed in case of control explants, control explants containing the NO scavenger 2-(4-carboxyphenyl)-4,4,5,5,-tetramethylimidazoline-1-oxyl-3-oxide (cPTIO), auxin depleted explants, explants with exogenous auxin addition, and those with additional auxin and cPTIO [14, 16]. Similar correlation of NO and IAA levels has not been reported from bacteria till date. Hence, the study of the bacterial genes influenced by these phytohormones and gasotransmitters will yield important information that may subsequently be applied to a variety of aspects of microbial biotechnology and agriculture including biofertilizers and biopesticides. This review attempts to identify such bacterial genes or their elements that may have implications for future use in improving plant productivity and plant–microbe interactions.
The IAA impact IAA is an auxin which plays a crucial role in a number of aspects of plant growth and development ranging from apical dominance to senescence [28, 29]. Apart from its production in plants, various bacteria are known to produce IAA, essentially PGP bacteria [2]. Bacteria do not require IAA for their physiological processes and its biosynthesis can be cited as an example of mutualistic existence [6]. IAA influences a number of plant genes most of which have been cloned and characterized further [reviewed in Refs. 30, 31–33]. In contrast, there are only few reports regarding bacterial genes influenced by IAA and these are summarized in Table 1. Over the years, various biosynthetic pathways have been studied for the production of IAA in plants and bacteria and these include the indole-3-pyruvic acid (IPyA) and indole-3-acetamide (IAM) pathway. Indole-3pyruvate decarboxylase (ipdC or ppdC) is the main gene of the IPyA pathway while tryptophan-2-monooxygenase (iaaM) is the gene central to the IAM pathway [34, 35]. The auxin (IAA)-responsive nature of ipdC in A. brasilense was demonstrated by creating an ipdC derivative of strain Sp245 [36]. This study confirmed the upregulation of ipdC under IAA induction, however, no upregulation was ß 2014 WILEY-VCH Verlag GmbH & Co. KGaA,Weinheim
observed with the IAA precursor (Trp), acetic acid or IAA conjugates. This was the first report describing induction of any bacterial gene by IAA. Vande Broek et al. [37] studied the A. brasilense Sp245 ipdC promoter region, which revealed a bacterial auxinresponsive element (AuxRE). Subsequent mutational analysis of IaaC demonstrated that this protein is involved in controlling IAA biosynthesis and not ipdC expression in strain Sp245. Other A. brasilense strains, Sp7 and SM were found not to harbor the iaaC gene and sequence analysis of strain SM ipdC locus confirmed a 705 bp deletion from the 50 end of the iaaC gene [19]. Thus, the structural organization of the ipdC locus varies in different strains of A. brasilense and the presence of IaaC along with specialized promoter features determines the gene response or inducibility to auxins, other chemicals, and environmental conditions like pH and temperature [19]. Apart from acting as a positive regulator in the IPyA pathway, IAA has been established as a signaling molecule in A. brasilense. A high throughput gene expression analysis was carried out to investigate the effect of exogenous IAA on A. brasilense Sp245 genes [38]. The study was conducted with both wildtype and ipdC mutant and eight clusters of differentially expressed genes were found. Such genes included genes for signal transduction, energy production and conversion, NO production, aromatic hydrocarbon degradation, outer membrane biogenesis, type VI secretion system (T6SS), etc. This study established that IAA could be the trigger for A. brasilense to interact with plants. Further work needs to be done in this area for functional characterization of these differentially expressed genes and determine their relevance in the context of bacteria–plant interactions. In addition to the PGP bacteria–plant interaction, another beneficial association exists in the soil, between the rhizobia, and leguminous plants [39]. In this interaction, rhizobia detect the signaling molecules (e.g., flavonoids) released by the plants and the subsequent signaling pathway elicits nodulation in the plants [29]. Studies have shown the accumulation of IAA in these root nodules and subsequently the partial prokaryotic nature of this IAA was confirmed [[40, 41], and references therein]. Spaepen et al. [42] analyzed the change in gene expression of various rhizobial genes under the influence of IAA in Rhizobium etli CNPAF512 using a transposon (mTn5gusA-oriV) mutant library. Prior to this study, the definitive role of IAA from the bacterial partner of this symbiotic relationship was not known. Of the 30 selected genes studied by mutagenesis only four mutants showed significantly altered gene
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expression and were involved in essential processes like motility, signaling, and plant root attachment. The four gene sequences when translated in silico, showed sequence homology with cbg1-encoded b-glucosidase of Agrobacterium tumifaciens B3/73, RapB1 protein of R. leguminosarum bv. trifolii R200, flagellar hook protein FlgE, and hypothetical protein RL0670 of R. leguminosarum bv. viciae 3841. The above mentioned Rhizobium-adhering protein (Rap) possesses the Ra (Rhizobium-adhering) domain and is capable of interacting with bacterial cell surfaces [43]. Studies by Mongiardini et al. [44] have shown that overexpression of Rap genes cause higher adsorption of rhizobia to plant roots. FlgE showed a downregulation in its expression under IAA induction. Flagellar hook which connects the basal body with the filament, is a highly curved tubular structure made of about 120 copies of a single protein, FlgE. The hook is essential for dynamic and efficient bacterial motility and taxis [45]. Decreased expression of this protein and overexpression of Rap genes under IAA induced conditions suggest that IAA could play an essential role in colonization of the bacteria over the root surfaces. In future, it may be interesting to look at the presence and function of similar genes like the ones mentioned here from known PGP strains and evaluate their role in plant root colonization and regulation of PGP fuctions. The most well established and studied model system involving IAA in plant–pathogen interactions is crown
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gall formation by Agrobacterium tumefaciens [25]. IPyA is the key pathway for IAA biosynthesis both in plants as well as bacteria, however, indole-3-acetamide (IAM) pathway is exclusive to bacteria as a two-step Trpdependent pathway which may be constitutive in nature [46]. Herein, the iaaM encoded enzyme decarboxylates Trp to form the intermediate IAM which is converted to IAA by the iaaH encoded enzyme, indole acetamide hydrolase (IAH). The IAM pathway is mostly involved in gall formation and most of the phytopathogens possess this pathway [25, 26]. Nevertheless, there are preliminary reports of the IAM pathway’s existence in PGP bacteria P. fluorescens Psd [46]. Hutcheson and Kosuge [47] elucidated for the first time that IAA production in P. syringae pv. savastanoi is regulated by feedback inhibition from IAM and IAA. The conversion of Trp to IAA is regulated at the first step involving iaaM. This clearly indicates that iaaM is an IAA responsive gene. In A. tumefaciens, these genes are located on the T-DNA of the Ti plasmid in all virulent strains and may play crucial roles in their pathogenicity [25, 48]. Strains with mutated/cured Ti plasmids lose their pathogenicity and when reintroduced pathogenicity was reinstated [25, 49]. In phytopathogens, IAA is presumed to enhance their ability to act as an epiphyte on plant surfaces, detoxify tryptophan analogues, and inhibit the plant hypersensitive response to expedite bacterial invasion. The presence of IAM pathway for IAA biosynthesis was demonstrated
Table 1. Bacterial genes and proteins influenced by Indole-3-acetic acid. Gene/protein influenced ipdC iaaM RapB1 FlgE RL0670 leuD sucA gltA sucD sdhB/sdhC aceA cycA dnaK leuB glpK adhE arcD galR ogl pelD/pelI/pelL dspE hrpN
Known/predicted function
Expression
Organism
Reference
IAA production (IPyA pathway) IAA production (IAM pathway) Rhizobium adherence Flagella formation Hypothetical protein 3-Isopropylmalate isomerase 2-Oxoglutarate dehydrogenase Citrate synthase Succinyl-CoA synthetase Succinate dehydrogenase aceA Isocitrate lyase D-Alanine/D-serine/glycine transport protein Chaperone Hsp70 3-Isopropylmalate dehydrogenase Glycerol kinase Alcohol dehydrogenase Arginine/ornithine antiporter Transcriptional repressor for galactose utilization Oligogalacturonate lyase Endopectate lyase putative T3SS effector T3SS harpin
Upregulated Upregulated Upregulated Downregulated Upregulated Upregulated Upregulated Upregulated Upregulated Upregulated Upregulated Upregulated Upregulated Upregulated Upregulated Downregulated Downregulated Downregulated
Azospirillum brasilense Pseudomonas syrinae pv. savastanoi Rhizobium etli CNPAF512 R. etli CNPAF512 R. etli CNPAF512 Escherichia coli MG1655 E. coli MG1655 E. coli MG1655 E. coli MG1655 E. coli MG1655 E. coli MG1655 E. coli MG1655 E. coli MG1655 E. coli MG1655 E. coli MG1655 E. coli MG1655 E. coli MG1655 E. coli MG1655
[19, 36, 37] [47] [42] [42] [42] [24] [24] [24] [24] [24] [24] [24] [24] [24] [24] [24] [24] [24]
Upregulated Upregulated Upregulated Upregulated
Erwinia chrysanthemi 3937 E. chrysanthemi 3937 E. chrysanthemi 3937 E. chrysanthemi 3937
[50] [50] [50] [50]
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in the non-gall forming phytopathogen, Erwinia chrysanthemi 3937. The decreased production of IAA caused reduced levels of the extra-cellular enzyme, pectate lyase and down-regulation of the type III secretion system (T3SS) genes. In the iaaM knockout mutant, the expression levels of an oligogalacturonate lyase gene, ogl, and three endopectate lyase genes, pelD, pelI, and pelL were reduced in comparison to the wild-type strain. The cytoplasmic oligogalacturonate lyase and pectate lyases, cleave glycosidic linkages by b-elimination, thereby causing maceration and soft rotting of plant tissue. Also, the transcription of T3SS genes, dspE (a putative T3SS effector) and hrpN (T3SS harpin), was found to be diminished in the iaaM mutant [50]. T3SS of Gramnegative bacteria allow establishment of bacterial pathogenicity by translocation of virulence factors from bacteria into host eukaryotic cells [51]. Apart from soil PGP bacteria, IAA has been reported to influence more than one percent genes in the central metabolic pathways in the laboratory strain, Escherichia coli K-12 MG 1655 [24]. Though, it is not exposed to IAA in its natural environment, in vitro studies revealed that IAA induction mainly altered the expression of essential genes associated with energy metabolism and amino acid biosynthesis. Genes with upregulated expression were involved in the TCA cycle (gltA, sucA, sucD, sdhB, and sdhC), glyoxylate shunt, and amino acid biosynthesis (proA). Also a correlation was seen between the upregulation of gene expression (aceA) and activation of the corresponding enzymes (isocitrate lyase). As no physiological function of IAA is clear from the soil PGP bacteria, similar studies could be carried out in various soil and PGP bacteria to demonstrate the definitive role of IAA in essential metabolic pathways of soil microbes. This information will be valuable in aiding the selection of microbial strains for use as biofertilizers, for specific soil types and application in specific environmental conditions. Recently, IAA-responsive genes were also identified in Saccharomyces cerevisiae, and perception of IAA was found to cause differentiation of the yeast cells into a filamentous, invasive form [27]. These findings suggest that proteins involved in IAA perception and signal transduction are not only present in higher plants but also in bacteria and fungi which provide leads for further investigation into the subject and to generate insights for development of host plant.
The NO-influence Nitric oxide is a free radical with its role in toxicity and as a signaling molecule well elucidated in mammals [52, 53]. ß 2014 WILEY-VCH Verlag GmbH & Co. KGaA,Weinheim
However, little is known about its biological role in plants and bacteria. Grün et al. [13] carried out a large scale transcriptional analysis to identify the effect of NO on various essential genes in Arabidopsis thaliana. These genes were involved in processes like stress response, S-nitrosylation, and plant–pathogen interactions. Further details of NO responsive genes from plants can be found in Besson-Bard et al. [54]. Despite its increasing significance, not much information is available about the NO-influenced bacterial genes. Cyclic Nucleotide Monophosphates (cNMPs) are wellestablished members of key signal-transduction pathways in eukaryotes and recently, cAMP, c-di-GMP, c-di-AMP, and cGMP have been found to play essential roles in bacteria, with cyclic dimeric GMP (c-di-GMP) and cyclic dimeric AMP (c-di-AMP) being ubiquitous bacterial messengers [55–58]. Synthesis of cAMPs, cGMPs, c-diAMP, and c-di-GMP is catalyzed by nucleotidyl cyclases and dinucleotidyl cyclases, while degradation of cNMPs/cdi-NMPs is achieved by phosphodiesterases (PDE) [55]. Thus, the concentration of cNMP/c-di-NMP is regulated in the cell by the antagonistic action of these two enzymes. Guanylyl cyclases (GCs) are expressed in two isoforms: the soluble (sGC) and particulate or membrane-bound (pGC) form [59]. Bacterial cNMP and c-di-NMPs have been reported to influence essential physiological characteristics like surface attachment, motility, virulence, and biofilm/cyst formation [57, 58, 60–64]. However, the exact mechanism is mostly unknown. Although it was known that sGCs sense NO by means of its heme moiety but the presence of Heme-Nitric oxide/OXygen (H-NOX) domain in the N-terminal extensions of sGCs by in silico analysis has been identified [65]. H-NOX is a large family of heme binding proteins which have the ability to bind diatomic gases (like NO, O2, CO, etc.) with selective discrimination [66, 67]. HNOB (heme NO binding) domains have been found to be either fused to other receptors like methyl-accepting domains of chemotaxis receptors or as standalone proteins [65, 68]. The presence of a distal pocket tyrosine for discrimination between O2 and NO binding is the molecular basis for the remarkable ligand selection displayed by H-NOX and subsequently by sGC [66]. In the absence of tyrosine, the dissociation rate of O2 increases and formation of any O2 complex is not possible; however, the dissociation of NO remains unchanged and leads to specific NO affinity [69]. Thus, H-NOX domain of bacterial sGC acts as a NO sensor and it can now be predicted that the genes possessing it will be NO-responsive. Consequently, NO modulation in bacteria may be achieved through such target genes. Since the activation of sGC directly leads to cyclization of GTP to cGMP, any alteration in its expression can lead
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to major changes in the cGMP-dependent/involved pathways. Figure 1 shows the different aspects of cGMP in bacterial systems, its relationship with NO and downstream pathways. Even though biofilm formation is a complex process with its exact mechanism largely unknown, cGMP/c-di-GMPs have been established as the essential signaling molecules in this process [56, 70–72]. Liu et al. [72] demonstrated the negative effect of NO on biofilm formation in Shewanella woodyi MS32 by regulating c-di-GMP levels. Nanomolar concentration of NO is detected by S. woodyi H-NOX (SwH-NOX) causing a decrease in intracellular c-di-GMP levels and subsequent decrease in biofilm formation. S. woodyi diguanylate cyclase (SwDGC) was reported to be a dual-functioning DGC with both DGC and PDE activities where DGC activity is predicted by a conserved GGDEF amino acid motif and that of PDE by EAL or HD-GYP domains [63, 73]. The study revealed that in the absence of NO, SwH-NOX activates the DGC activity of SwDGC. However, in its presence, SwHNOX upregulates PDE activity and c-di-GMP degradation is enhanced, subsequently leading to thinning of the biofilm. Prior to this work, the role of biofilm dispersal induced by NO in opportunistic bacteria, Pseudomonas aeruginosa was investigated [74, 75]. Low levels of NO were shown to stimulate PDE activity and subsequent switch from biofilm to planktonic phenotype. Further analysis validated that this process required c-di-GMP and the chemotaxis transducer BdlA and a direct link between NO
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and c-di-GMP was established. Such results point to the fact that cNMPs may play an important role in the signaling and sensing of NO produced by PGP bacteria and this is worth investigating in future. Cell-to-cell communication between the bacteria in a cell density-dependent manner is a mechanism defined as quorum sensing (QS) which has now been observed in both Gram-negative and Gram-positive bacteria to regulate processes like bioluminescence, biofilm formation, and virulence [76, 77]. Any QS system consists of the genes involved in the production and sensing of the autoinducer (AI) signaling molecules, commonly N-acyl-homoserine lactones (AHL). In Vibrio harveyi, three QS circuits have been demonstrated so far: LuxM/LuxN, LuxS/LuxPQ , and CqsA/CqsS, named for the AI synthase/receptor pair [78]. Above a threshold concentration of the AI, the receptor molecule switches its activity from kinase to phosphatase, causing the transfer of phosphate to the common phosphorelay protein, LuxU. LuxU subsequently phosphorylates the transcription factor, LuxO which indirectly represses the master regulator of QS, LuxR [53, 78]. Thus, at low cell density and low AI levels, expression of LuxR is repressed and V. harveyi does not show bioluminescence. The H-NOX/HqsK (heme-nitric oxide/oxygen binding domain; H-NOX-associated quorum sensing kinase) QS pathway was recently discovered in V. harveyi where NO/ H-NOX regulates phosphorylation of the kinase and initiates the phosphorylation through LuxU/LuxO/LuxR
Figure 1. Schematic representation of synthesis, degradation, and function of cGMP. The three targets of cGMP molecules are (i) cGMP dependent protein kinases, (ii) cGMP gated ion channels and (iii) cGMP-dependent phosphodiesterases. While phosphodiesterases are involved in the degradation of cGMP to GMP, the protein kinases and activation of ion channels are subsequently involved in various bacterial signaling pathways. GTP: Guanosine 50 -triphosphate; sGC: soluble guanylate cyclase; NO: nitric oxide; H-NOX: Heme-Nitric oxide/Oxygen
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pathway. This study established that NO acts analogously with other AIs and positively regulates bioluminescence in V. harveyi [78]. Apart from bioluminescence, in recent times NO-responsive biofilm formation is also being explored in V. harveyi. Biofilm formation in bacteria in response to NO has already been established but it has been associated with c-di-GMP signaling [52, 60, 64, 74, 79]. However, it has been reported that biofilm formation is also regulated by the H-NOX/HqsK QS pathway. Mutational, genetic, and proteomic studies were carried out to illustrate that at low concentration of NO, H-NOX positively regulates the V. harveyi biofilm enhancement through the H-NOX-associated QS kinase [79]. It still waits to be seen if the similar traits of PGP bacteria involve NO-dependent signaling. It may also be important to study if some other PGP traits in addition to biofilm formation involve QS mechanisms. Detoxifying enzymes like flavorubredoxin nitric oxide reductase (NorVW), nitric oxide reductase (NorB), and nitrite reductase (NrfA) convert NO to less toxic derivatives-nitrate, nitrous oxide, and ammonia and this is controlled by a variety of transcription factors [53]. These processes include regulatory proteins which may or may not be involved in the bacterial response to NO and include SoxR, FNR, NorR, Fur, NnrR, NsrR, H-Nox [detailed in Ref. 67]. SoxR was the first reported case of a bacterial transcriptional regulator responding to NO. It is a redox-sensitive activator dependent on the oxidation state of its binuclear [2Fe–2S] cluster, which is sensitive to NO [80, 81]. Ding and Demple [82] demonstrated that in E. coli, SoxR activation by NO occurs through direct modification of the iron–sulfur center to form proteinbound dinitrosyl–iron dithiol adducts. This observation was made in case of intact bacterial cells as well as in purified SoxR after NO treatment and established the direct role of NO in signal transduction [82]. Another regulator is FNR which possesses an iron–sulfur cluster. A study by Cruz-Ramos et al. [83] accentuated that the flavohaemoglobin Hmp of E. coli is involved in the protective response to NO. The transcription of hmp is
regulated by FNR, which was known to possess [4Fe–4S] cluster and be O2-responsive in nature. Aerobically, Hmp detoxifies NO by acting as an NO oxygenase or denitrosylase, whereas, under anaerobic conditions, the DNA-binding activity of FNR is lowered as NO reacts with the Fe–S cluster and forms dinitrosyl–iron complexes converting NO to lesser toxic forms like nitrous oxide [83–85]. Proteins/regulators that have been identified as NO sensors are mentioned in Table 2.
Genetic regulation (s54-dependence) Various molecular approaches such as macroarray/ microarray analysis and real-time PCR have been used to study primary plant auxin responsive genes. Within the promoters of these genes, cis elements have been observed that confer auxin responsiveness and are referred to as auxin-responsive elements or AuxREs. Associated to these is a family of trans-acting transcription factors that are identified as auxin-response factors or ARFs that bind with specificity to AuxREs. A family of auxin regulated proteins referred to as Aux/IAA proteins also play a key role in regulating these auxin responsive genes. Auxins may regulate transcription of early response genes in plants by influencing this type of interactions between ARFs and Aux/IAAs [32]. The alternative sigma factor, s54 controls several ancillary processes including phytochemical degradation, pilin synthesis and flagellar assembly, arginine catabolism, nitrogen fixation, and auxin biosynthesis among many other processes. It is unable to initiate transcription spontaneously and is dependent on additional factors called enhancer binding proteins (EBP) [86]. s54 recognises promoter sequences carrying conserved GG and GC elements at 24 and 12 positions in a variety of genes along with their EBP [86]. Most prominently, these include nif (nitrogen fixation structural genes), glnB (regulatory protein for glutamine synthase) genes from soil bacteria Azospirillum, Rhizobium, Bradyrhizobium,
Table 2. Bacterial proteins influenced by nitric oxide. Protein/regulator influenced
Known/predicted function
NO sensor
Organism
Reference
SoxR FNR NorR
Defence against superoxide and NO NO detoxification NO detoxification
[2Fe–2S] [4Fe–4S] Non-heme iron
[68, 80–82] [68, 81, 83, 93] [68, 81, 88, 93]
H-NOX
Sensing diatomic gases (O2/NO)
Heme
Hmp
NO detoxification
[4Fe–4S]
Escherichia coli E. coli, Rhodobacter sphaeroides E. coli, Ralstonia eutropha, Pseudomonas aeruginosa Vibrio harveyi, V. cholerae, Shewanella woodyi, Thermoanaerobacter tengcongensis E. coli
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[65, 66, 68, 72, 81] [83, 84, 93]
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Klebsiella, Pseudomonas, and Azorhizobium. Further details of the domain architectures may be found in Studholme and Dixon [87]. More recently, the transcription of norVW is activated by a s54-dependent enhancer binding protein, NorR, to which the NO sensing property is imparted by the mononuclear non-heme iron centre [68, 88]. Expression studies of a cytochrome P450 homolog from Rhizobium sp. BR816, CYP127A2 pointed to a NifA- and s54dependent transcription [89]. The conserved regions of the s54-dependent promoters and the upstream activating sequence (UAS) that activates s54-dependent transcription (RpoN) were found in the P450 homolog [89]. Such UAS sequences have also been reported upstream of the nifHc gene of R. etli [90]. In Rhizobium CNPAF512, NifA has been shown to control the symbiotic expression of nif genes [91]. CYP127A2 was expressed at a low level under free-living conditions, whereas higher expression was reported from the bacteroids. This expression pattern of CYP127A2 is in accordance with the wild-type Rhizobium strain BR816 and confirmed that CYP127A2 expression is regulated by RpoN and NifA [89]. A dyadic sequence (DS, ATTGTTTC(GAAT)GAAACAAT) is located in the 50 upstream region of ipdC between positions 58 and 38, with a perfect two 8-bp inverted repeat separated by a 4-bp spacer [19, 37]. Site-directed mutagenesis and deletion demonstrated that this element, referred to as a bacterial auxin-regulated element, is essential for the IAA inducibility of genes and is related to the AuxRE of plants, TGTCNC or the degenerate version (G/T)GTCCCAT. The short sequence, TGTCCC (Sequence Element 1 or SE1) was found to be located at position 3 to 8 in A. brasilense [19, 37, 92]. An in silico sequence analysis based on homology of the A. brasilense SM ipdC gene with that from Sp245 and Sp7 showed the three SEs in the 50 upstream region of the ipdC coding region. These included SE1 and SE2 which are a part of composite promoters of auxin-responsive genes that function together with a coupling element overlapping or adjacent to the AuxRE. The two SEs occupy the 12 and 24 recognition sequence of the s54-dependent promoters [19]. SE3 was same as the DS, centered at position 48 in Sp245 as explained by Vande Broek et al. [37]. Since the presence of such features determine the auxin inducibility of associated genes, they may play an important role in determining the application of the PGP bacteria as biofertilizers for important plant growth.
Conclusion Plants convert various inorganic molecules into essential organic compounds like sugars, amino acids, organic ß 2014 WILEY-VCH Verlag GmbH & Co. KGaA,Weinheim
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acids, antibiotics, and secondary metabolites in the presence of sunlight. A part of the root exudates is released by plants into the rhizosphere creating a conducive/favorable environment for diverse microbial growth that act as insurance for improving plant productivity. This includes their ability to form wellstructured biofilms, provide them advantages like communicating by cell-to-cell signaling, nutrient acquisition, migrating collectively, and increased resistance against environmental and other stresses. Microbes maintain a critical mass of cells so that they can excrete essential metabolites above a threshold concentration that is required by the associated host plant. Being a part of a biofilm will also augment the ability of the microbe to act as a biocontrol agent for plants. NO, a small diatomic molecule is gaining immense importance in the field of research which can be substantiated by an increase in the number of publications elucidating its role in mammals, plants, and most importantly bacteria. However, the exact working mechanism of NO is still widely debated due to its gaseous nature and high reactivity which causes experimental limitations. Also, inadequate information is available about various NO-responsive and influenced genes. Similarly, IAA is known as an essential phytohormone for a long time but on IAA exposure, a number of bacterial genes are influenced. It is likely that IAA and NO produced by PGP bacteria may interact in the rhizosphere with other members of the rhizosphere microbiome and the presence of s54 transcription for genes involved in the metabolism of such plant growth regulators may open up a further field of study under changing environments (nutrient and limiting environment conditions). The bacterial NO and IAA induced genes or proteins may play an important role in signaling and sensing of other hormones by plants in the rhizosphere. Figure 2 shows a hypothetical model of the crosstalk involving IAA and NO produced by the rhizosphere bacteria and their effect on plants. This model highlights the importance of signaling involving the auxins, and NO and their likely common genetic regulation. For better understanding of the interactions between these molecules, more information needs to be gathered about the genes and proteins which are involved in these processes. Future efforts should be made to identify differentially expressed genes in response to these plant growth regulators and their relevance in improving plant growth as many of the PGP bacteria act as biofertilisers. Keeping in view the current available information, interplay between IAA and NO cannot be ruled out in the rhizosphere
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Figure 2. Schematic representation of the crosstalk involving indole-3-acetic acid (IAA) and nitric oxide (NO) produced by rhizosphere bacteria and their effect on plants. cGMP acts as an extracellular signal in plants which are likely modulated by bacterial NO through IAA. NO-mediated inhibition of ethylene biosynthesis has also been observed. Microbially produced IAA directly influences plant root proliferation. The NH3 released in the rhizosphere is fixed by N2-fixing PGPR which along with biomineralization of complex nutrient sources allows enhanced mineral/nutrient uptake leading to improved plant growth. NO activates metabolic and physiological responses in plants by three distinct mechanisms involving [a] a cGMP-dependent pathway, [b] a cGMP-independent route, and [c] NO action on MAPK activities, which are involved in many physiological adaptation and developmental processes [22]. IAA is self-inducible which may be initiated by signals from plant root exudates. [—] represents inhibition of processes, [!] shows induction of biosynthesis, and [ ] identify the mechanisms that beneficially influence plant growth.
bacteria. Consequently, it is extremely important to study the extent of influence of microbial plant growth regulators, IAA and NO so that their effect on plants can be judged for their appropriate action and application.
Acknowledgments The review was prepared as part of a project funded by the Department of Biotechnology to M.K. The authors thank Director General, TERI for the infrastructure support provided.
References [1] Benizri, E., Baudoin, E., Guckert, A., 2001. Root colonization by inoculated plant growth-promoting rhizobacteria. Biocontrol Sci. Technol., 11, 557–574. [2] Kochar, M., Srivastava, S., 2012. Surface colonization by Azospirillum brasilense SM in the indole-3-acetic acid dependent growth improvement of sorghum. J. Basic Microbiol., 52, 123–131. [3] Mazzola, M., Cook, R.J., Thomashow, L.S., Weller, D.M., Pierson, L.S., 1992. Contribution of phenazine antibiotic biosynthesis to the ecological competence of fluorescent pseudomonads in soil habitats. Appl. Environ. Microbiol., 58, 2616–2624.
Conflict of interest statement
[4] Molina-Favero, C., Creus, C.M., Lanteri, M.L., CorreaAragunde, N. et al., 2007. Nitric oxide and plant growth promoting rhizobacteria: common features influencing root growth and development. Adv. Bot. Res., 46, 1–33.
There is no conflict of interest.
[5] Molina-Favero, C., Creus, C.M., Simontacchi, M., Puntarulo, S., Lamattina, L., 2008. Aerobic nitric oxide production by
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www.jbm-journal.com
J. Basic Microbiol. 2014, 54, 1–11
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Azospirillum brasilense Sp245 and its influence on root architecture in tomato. Mol. Plant Microbe Interact., 21, 1001–1009. [6] Somers, E., Vanderleyden, J., Srinivasan, M., 2004. Rhizosphere bacterial signalling: a love parade beneath our feet. Crit. Rev. Microbiol., 30, 205–240. [7] Boon, E.M., Marletta, M.A., 2005. Ligand specificity of HNOX domains: from sGC to bacterial NO sensors. J. Inorg. Biochem., 99, 892–902. [8] Dobutovic, B., Smiljani, K., Soski, S., Düngen, H., Isenovi, E.R., 2011. Nitric oxide and its role in cardiovascular diseases. Open Nitric Oxide J., 3, 65–71. [9] Rafferty, S., 2011. Nitric oxide synthases of bacteria – and other unicellular organisms. Open Nitric Oxide J., 3, 325– 332. [10] Garcia-Mata, C., Lamattina, L., 2002. Nitric oxide and abscisic acid cross talk in guard cells. Plant Physiol., 128, 790–792. [11] Giba, Z., Grubišić, D., Konjević, R., 2006. Seeking the role of NO in breaking seed dormancy, in: Lamattina, L., Polacco, J.C. (Eds.), Nitric Oxide in Plant Growth. Plant Cell Monographs, Springer-Verlag, Berlin, Heidelberg, 91–111. [12] Cohen, M.F., Lamattina, L., Yamasaki, H., 2010. Nitric oxide signaling by plant-associated bacteria, in: Hayat, S., Mori, M., Pichtel, J., Ahmad, A. (Eds.), Nitric Oxide in Plant Physiology, Wiley-VCH, Verlag GmbH and Co. KGaA, Weinheim, 161–172.
9
[22] Kochar, M., Vaishnavi, A., Upadhyay, A., Srivastava, S., 2013. Bacterial biosynthesis of indole-3-acetic acid: signal messenger service, in: de Bruijn, F.J. (Ed.), Molecular Microbial Ecology of the Rhizosphere: Volume 1. John Wiley & Sons, Inc., Hoboken, NJ, USA, 309–326. [23] Spaepen, S., Vanderleyden, J., Remans, R., 2007. Indole-3acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol. Rev., 31, 425–448. [24] Bianco, C., Imperlini, E., Calogero, R., Senatore, B. et al., 2006. Indole-3-acetic acid regulates the central metabolic pathways in Escherichia coli. Microbiology, 152, 2421–2431. [25] Jameson, P.E., 2000. Cytokinins and auxins in plant– pathogen interactions – an overview. Plant Growth Reg., 32, 369–380. [26] Lambrecht, M., Okon, Y., Vande Broek, A., Vanderleyden, J., 2000. Indole-3-acetic acid: a reciprocal signalling molecule in bacteria–plant interactions. Trends Microbiol., 8, 298–300. [27] Prusty, R., Grisafi, P., Fink, G.R., 2004. The plant hormone indole acetic acid induces invasive growth in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA., 101, 4153–4157. [28] Kukreja, K., Suneja, S., Goyal, S., Narula, N., 2004. Phytohormone production by Azotobacter – a review. Agric. Rev., 25, 70–75. [29] Spaepen, S., Dobbelaere, S., Croonenborghs, A., Vanderleyden, J., 2008. Effects of Azospirillum brasilense indole-3acetic acid production on inoculated wheat plants. Plant Soil, 312, 15–23.
[13] Grün, S., Lindermayr, C., Sell, S., Durner, J., 2006. Nitric oxide and gene regulation in plants. J. Exp. Bot., 57, 507– 516.
[30] Chapman, E.J., Estelle, M., 2009. Mechanism of auxinregulated gene expression in plants. Annu. Rev. Genet., 43, 265–285.
[14] Pagnussat, G.C., Lanteri, M.L., Lamattina, L., 2003. Nitric oxide and cyclic GMP are messengers in the indole acetic acid-induced adventitious rooting process. Plant Physiol., 132, 1241–1248.
[31] Goda, H., Sawa, S., Asami, T., Fujioka, S. et al., 2004. Comprehensive comparison of auxin-regulated and brassinosteroid-regulated genes in Arabidopsis. Plant Physiol., 134, 1555–1573.
[15] Pagnussat, G.C., Lanteri, M.L., Lamattina, L., 2004. Nitric oxide mediates the indole acetic acid induction of a mitogen-activated protein kinase cascade involved in adventitious root development. Plant Physiol., 135, 279– 286.
[32] Hagen, G., Guilfoyle, T., 2002. Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol. Biol., 49, 373–385.
[16] Pagnussat, G.C., Simontacchi, M., Puntarulo, S., Lamattina, L., 2002. Nitric oxide is required for root organogenesis. Plant Physiol., 129, 954–956.
[34] Malhotra, M., Srivastava, S., 2006. Targeted engineering of Azospirillum brasilense strain SM with Indole acetamide pathway for IAA over-expression. Can. J. Microbiol., 52, 1078–1084.
[17] Chen, Y., Rosazza, J.P.N., 1994. A bacterial nitric oxide synthase from a Nocardia species. Biochem. Biophys. Res. Commun., 203, 1251–1258.
[33] Simon, S., Petrášek, J., 2011. Why plants need more than one type of auxin. Plant Sci., 180, 454–460.
[18] Woodward, A.W., Bartel, B., 2005. Auxin: regulation, action, and interaction. Ann. Bot., 95, 707–735.
[35] Steenhoudt, O., Vanderleyden, J., 2000. Azospirillum, a freeliving nitrogen-fixing bacterium closely associated with grasses: genetic, biochemical and ecological aspects. FEMS Microbiol. Rev., 24, 487–506.
[19] Malhotra, M., Srivastava, S., 2008. Organization of the ipdC region regulates IAA levels in different Azospirillum brasilense strains: molecular and functional analysis of ipdC in strain SM. Environ. Microbiol., 10, 1365–1373.
[36] Vande Broek, A., Lambrecht, M., Eggermont, K., Vanderleyden, J., 1999. Auxins upregulate expression of the indole-3-pyruvate decarboxylase gene in Azospirillum brasilense. J. Bacteriol., 181, 1338–1342.
[20] Spaepen, S., Vanderleyden, J., 2011. Auxin and plant– microbe interactions. Cold Spring Harb. Perspect. Biol., 3, a001438.
[37] Vande Broek, A., Gysegom, P., Ona, O., Hendrickx, N. et al., 2005. Transcriptional analysis of the Azospirillum brasilense indole-3-pyruvate decarboxylase gene and identification of a cis-acting sequence involved in auxin responsive expression. Mol. Plant Microbe Interact., 18, 311–323.
[21] Sukumar, P., Legué, V., Vayssières, A., Martin, F. et al., 2013. Involvement of auxin pathways in modulating root architecture during beneficial plant–microorganism interactions. Plant Cell Environ., 36, 909–919. ß 2014 WILEY-VCH Verlag GmbH & Co. KGaA,Weinheim
[38] Van Puyvelde, S., Cloots, L., Engelen, K., Das, F. et al., 2011. Transcriptome analysis of the rhizosphere bacterium
www.jbm-journal.com
J. Basic Microbiol. 2014, 54, 1–11
10
Vatsala Koul et al.
Azospirillum brasilense reveals an extensive auxin response. Microb. Ecol., 61, 723–728. [39] Theunis, M., Kobayashi, H., Broughton, W.J., Prinsen, E., 2004. Flavonoids, NodD1, NodD2, and nod-box NB15 modulate expression of the y4wEFG locus that is required for indole-3-acetic acid synthesis in Rhizobium sp. strain NGR234. Mol. Plant Microbe Interact., 17, 1153–1161. [40] Mathesius, U., Schlaman, H.R., Spaink, H.P., Sautter, C. et al., 1998. Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides. Plant J., 14, 23–34. [41] Glick, B.R., 2012. Plant growth-promoting bacteria: mechanisms and applications. Scientifica, Article ID: 963401. [42] Spaepen, S., Das, F., Luyten, E., Michiels, J., Vanderleyden, J., 2009. Indole-3-acetic acid-regulated genes in Rhizobium etli CNPAF512. FEMS Microbiol. Lett., 291, 195–200. [43] Ausmees, N., Jacobsson, K., Lindberg, M., 2001. A unipolarly located, cell-surface-associated agglutinin, RapA, belongs to a family of Rhizobium-adhering proteins (Rap) in Rhizobium leguminosarum bv. trifolii. Microbiology. 147, 549–559. [44] Mongiardini, E.J., Ausmees, N., Perez-Gimenez, J., Althabegoiti, M.J. et al., 2008. The rhizobial adhesion protein RapA1 is involved in adsorption of rhizobia to plant roots but not in nodulation. FEMS Microbiol. Ecol., 65, 279–288. [45] Samatey, F.A., Matsunami, H., Imada, K., Nagashima, S. et al., 2004. Structure of the bacterial flagellar hook and implication for the molecular universal joint mechanism. Nature, 431, 1062–1068. [46] Kochar, M., Upadhyay, A., Srivastava, S., 2011. Indole-3acetic acid biosynthesis in the biocontrol strain Pseudomonas fluorescens Psd and plant growth regulation by hormone overexpression. Res. Microbiol., 162, 426–435. [47] Hutcheson, S.W., Kosuge, T., 1985. Regulation of 3indoleacetic acid production in Pseudomonas syringae pv. savastanoi. purification and properties of tryptophan 2monooxygenase. J. Biol. Chem., 260, 6281–6287. [48] Morris, R.O., 1995. Molecular aspects of hormone synthesis and action-genes specifying auxin and cytokinin biosynthesis in prokaryotes, in: Davies P.J. (Ed.), Plant Hormones, Kluwer Academic Publishers, Dordecht, 318–339. [49] Nester, E.W., Kosuge, T., 1981. Plasmids specifying plant hyperplasias. Ann. Rev. Microbiol., 35, 531–565. [50] Yang, S., Zhang, Q., Guo, J., Charkowski, A.O. et al., 2007. Global effect of indole-3-acetic acid biosynthesis on multiple virulence factors of Erwinia chrysanthemi 3937. Appl. Environ. Microbiol., 73, 1079–1088. [51] Stuber, K., Frey, J., Burnens, A.P., Kuhnert, P., 2003. Detection of type III secretion genes as a general indicator of bacterial virulence. Mol. Cell Probes, 17, 25–32. [52] Plate, L., Marletta, M.A., 2012. Nitric oxide modulates bacterial biofilm formation through a multicomponent cyclic-di-GMP signaling network. Mol. Cell, 46, 449–460. [53] Plate, L., Marletta, M.A., 2013. Nitric oxide-sensing H-NOX proteins govern bacterial communal behavior. Trends Biochem. Sci., 38, 566–575. ß 2014 WILEY-VCH Verlag GmbH & Co. KGaA,Weinheim
[54] Besson-Bard, A., Astier, J., Rasul, S., Wawer, I. et al., 2009. Current view of nitric oxide-responsive genes in plants. Plant Sci., 177, 302–309. [55] Corrigan, R.M., Gründling, A., 2013. Cyclic di-AMP: another second messenger enters the fray. Nat. Rev. Microbiol., 11, 513–524. [56] D’Argenio, D.A., Miller, S.I., 2004. Cyclic di-GMP as a bacterial second messenger. Microbiology, 150, 2497–2502. [57] Gomelsky, M., 2011. cAMP, c-di-GMP, c-di-AMP and now cGMP: bacteria use them all! Mol. Microbiol., 79, 562–565. [58] Krasteva, P.V., Giglio, K.M., Sondermann, H., 2012. Sensing the messenger: the diverse ways that bacteria signal through c-di-GMP. Protein Sci., 21, 929–948. [59] Beste, K.Y., Spangler, C.M., Burhenne, H., Koch, K.W. et al., 2013. Nucleotidyl cyclase activity of particulate guanylyl cyclase A: comparison with particulate guanylyl cyclases E and F, soluble guanylyl cyclase and bacterial adenylyl cyclases CyaA and edema factor. PLoS ONE, 29, e70223. [60] Cotter, P.A., Stibitz, S., 2007. c-di-GMP-mediated regulation of virulence and biofilm formation. Curr. Opin. Microbiol., 10, 17–23. [61] Marden, J.N., Dong, Q., Roychowdhury, S., Berleman, J.E., Bauer, C.E., 2011. Cyclic GMP controls Rhodospirillum centenum cyst development. Mol. Microbiol., 79, 600–615. [62] Sisti, F., Ha, D.G., O’Toole, G.A., Hozbor, D., Fernández, J., 2013. Cyclic-di-GMP signalling regulates motility and biofilm formation in Bordetella bronchiseptica. Microbiology, 159, 869–879. [63] Tao, F., He, Y.W., Wu, D.H., Swarup, S., Zhang, L.H., 2010. The cyclic nucleotide monophosphate domain of Xanthomonas campestris global regulator Clp defines a new class of cyclic di-GMP effectors. J. Bacteriol., 192, 1020–1029. [64] Yan, W., Qu, T., Zhao, H., Su, L. et al., 2010. The effect of cdi-GMP (30 -50 -cyclic diguanylic acid) on the biofilm formation and adherence of Streptococcus mutans. Microbiol. Res., 165, 87–96. [65] Iyer, L.M., Anantharaman, V., Aravind, L., 2003. Ancient conserved domains shared by animal soluble guanylyl cyclases and bacterial signaling proteins. BMC Genomics, 4, 5. [66] Boon, E.M., Huang, S.H., Marletta, M.A., 2005. A molecular basis for NO selectivity in soluble guanylate cyclase. Nat. Chem. Biol., 1, 53–59. [67] Derbyshire, E.R., Marletta, M.A., 2009. Biochemistry of soluble guanylate cyclase. Handb. Exp. Pharmacol., 191, 17–31. [68] Spiro, S., 2007. Regulators of bacterial responses to nitric oxide. FEMS Microbiol. Rev., 31, 193–211. [69] Boon, E.M., Marletta, M.A., 2005. Ligand discrimination in soluble guanylate cyclase and the H-NOX family of heme sensor proteins. Curr. Opin. Chem. Biol., 9, 441–446. [70] Gomelsky, M., Galperin, M.Y., 2013. Bacterial second messengers, cGMP and c-di-GMP, in a quest for regulatory dominance. EMBO J., 32, 2421–2423. [71] Jenal, U., 2004. Cyclic di-guanosine-monophosphate comes of age: a novel secondary messenger involved in modulating cell surface structures in bacteria? Curr. Opin. Microbiol., 7, 185–191.
www.jbm-journal.com
J. Basic Microbiol. 2014, 54, 1–11
Sphere of influence of IAA and NO in bacteria
[72] Liu, N., Xu, Y., Hossain, S., Huang, N. et al., 2012. Nitric oxide regulation of cyclic di-GMP synthesis and hydrolysis in Shewanella woodyi. Biochemistry, 51, 2087–2099. [73] Simm, R., Morr, M., Kader, A., Nimtz, M., Romling, U., 2004. GGDEF and EAL domains inversely regulate cyclic diGMP levels and transition from sessility to motility. Mol. Microbiol., 53, 1123–1134. [74] Barraud, N., Schleheck, D., Klebensberger, J., Webb, J.S. et al., 2009. Nitric oxide signaling in Pseudomonas aeruginosa biofilms mediates phosphodiesterase activity, decreased cyclic di-GMP levels, and enhanced dispersal. J. Bacteriol., 191, 7333–7342. [75] Boyle, K.E., Heilmann, S., van Ditmarsch, D., Xavier, J.B., 2013. Exploiting social evolution in biofilms. Curr. Opin. Microbiol., 16, 207–212. [76] Fuqua, C., Greenberg, E.P., 2002. Listening in on bacteria: acyl-homoserine lactone signaling. Nat. Rev. Mol. Cell. Biol., 3, 685–695. [77] Miller, M.B., Bassler, B.L., 2001. Quorum sensing in bacteria. Annu. Rev. Microbiol., 55, 165–199. [78] Henares, B.M., Higgins, K.E., Boon, E.M., 2012. Discovery of a nitric oxide responsive quorum sensing circuit in Vibrio harveyi. ACS Chem. Biol., 7, 1331–1336. [79] Henares, B.M., Xu, Y., Boon, E.M., 2013. A nitric oxideresponsive quorum sensing circuit in Vibrio harveyi regulates flagella production and biofilm formation. Int. J. Mol. Sci., 14, 16473–16484. [80] Krapp, A.R., Humbert, M.V., Carrillo, N., 2011. The soxRS response of Escherichia coli can be induced in the absence of oxidative stress and oxygen by modulation of NADPH content. Microbiology, 157, 957–965. [81] Spiro, S., 2006. Nitric oxide-sensing mechanisms in Escherichia coli. Biochem. Soc. Trans., 34, 200–202. [82] Ding, H., Demple, B., 2000. Direct nitric oxide signal transduction via nitrosylation of iron–sulfur centers in the SoxR transcription activator. Proc. Natl. Acad. Sci. USA, 97, 5146–5150. [83] Cruz-Ramos, H., Crack, J., Wu, G., Hughes, M.N. et al., 2002. NO sensing by FNR: regulation of the Escherichia coli NOdetoxifying flavohaemoglobin, Hmp. EMBO J., 21, 3235–3244.
ß 2014 WILEY-VCH Verlag GmbH & Co. KGaA,Weinheim
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[84] Poole, R.K., 2008. Microbial haemoglobins: proteins at the crossroads of oxygen and nitric oxide metabolism, in: Bolognesi, M., di Prisco, G., Verde, C. (Eds.), Dioxygen Binding and Sensing Proteins, a Tribute to Beatrice and Jonathan Wittenberg, Springer-Verlag, Milan, 241–257. [85] Stevanin, T.M., Read, R.C., Poole, R.K., 2007. The hmp gene encoding the NO-inducible flavohaemoglobin in Escherichia coli confers a protective advantage in resisting killing within macrophages, but not in vitro: links with swarming motility. Gene, 398, 62–68. [86] Barrios, H., Valderrama, B., Morett, E., 1999. Compilation and analysis of sigma (54)-dependent promoter sequences. Nucleic Acids Res., 27, 4305–4313. [87] Studholme, D.J., Dixon, R., 2003. Domain architectures of sigma (54)-dependent transcriptional activators. J. Bacteriol., 185, 1757–1767. [88] D’Autréaux, B., Tucker, N.P., Dixon, R., Spiro, S., 2005. A non-haem iron centre in the transcription factor NorR senses nitric oxide. Nature, 437, 769–772. [89] Luyten, E., Swinnen, E., Vlassak, K., Verreth, C. et al., 2001. Analysis of a symbiosis-specific cytochrome P450 homolog in Rhizobium sp. BR816. Mol. Plant Microbe Interact., 14, 918–924. [90] Valderrama, B., Dávalos, A., Girard, L., Morett, E., Mora, J., 1996. Regulatory proteins and cis-acting elements involved in the transcriptional control of Rhizobium etli reiterated nifH genes. J. Bacteriol., 178, 3119–3126. [91] Michiels, J., D’Hooghe, I., Verreth, C., Pelemans, H., Vanderleyden, J., 1994. Characterization of the Rhizobium leguminosarum biovar phaseoli nifA gene, a positive regulator of nif gene expression. Arch. Microbiol., 161, 404–408. [92] Lambrecht, M., Vande Broek, A., Dosselaere, F., Vanderleyden, J., 1999. The ipdC promoter auxin-responsive element of Azospirillum brasilense, a prokaryotic ancestral form of the plant AuxRE? Mol. Microbiol., 32, 889–891. [93] Pullan, S.T., Gidley, M.D., Jones, R.A., Barrett, J. et al., 2007. Nitric oxide in chemostat-cultured Escherichia coli is sensed by Fnr and other global regulators: unaltered methionine biosynthesis indicates lack of S-nitrosation. J. Bacteriol., 189, 1845–1855.
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Review Sphere of influence of indole acetic acid and nitric oxide in bacteria Vatsala Koul, Alok Adholeya and Mandira Kochar TERI Deakin Nanobiotechnology Centre, Biotechnology and Bioresources Division, The Energy and Resources Institute, Darbari Seth Block, India Habitat Centre, Lodhi Road, New Delhi, India
Bacterial biosynthesis of the phytohormone, indole-3-acetic acid (IAA) is well established and along with the diffusible gaseous molecule, nitric oxide (NO) is known to positively regulate the developmental processes of plant roots. IAA and NO act as signaling molecules in plant–microbe interactions as they modulate the gene expression in both, plants and microorganisms. Although IAA and NO may not be required for essential bacterial physiological processes, numerous studies point towards a crosstalk between IAA and NO in the rhizosphere. In this review, we describe various IAA and NO-responsive or sensing genes/proteins/regulators. There is also growing evidence for the interaction of IAA and NO with other plant growth regulators and the involvement of NO with the quorum sensing system in biofilm formation and virulence. This interactive network can greatly impact the host plant–microbe interactions in the soil. Coupled with this, the specialized s54-dependent transcription observed in some of the IAA and NO-influenced genes can confer inducibility to these traits in bacteria and may allow the expression of IAA and NO-influenced microbial genes in nutrient limiting or changing environmental conditions for the benefit of plants. Keywords: Indole acetic acid / Nitric oxide / Plant growth promoting bacteria Received: March 17, 2014; accepted: April 26, 2014 DOI 10.1002/jobm.201400224
Introduction Plant growth promoting (PGP) bacteria Azospirillum, Azotobacter, Bacillus, Pseudomonas, Rhizobium, Bradyrhizobium, and others enhance plant growth either directly by producing growth metabolites (phytohormones and other plant growth regulators) and increasing available nutrient uptake (phosphate solubilization and accelerating mineralization) or indirectly by biologically controlling plant diseases (complex antibiotics and siderophores) [1–6]. In recent times, nitric oxide (NO) has emerged as an essential, multifunctional, diffusible cell signaling molecule not only in animals but also plants and bacteria. In humans, its involvement in multiple biological functions
Correspondence: Mandira Kochar, TERI Deakin Nanobiotechnology Centre, Biotechnology and Bioresources Division, The Energy and Resources Institute, Darbari Seth Block, India Habitat Centre, Lodhi Road, New Delhi 110003, India E-mail: [email protected], [email protected] Phone: þ91 11 24682100 Fax: þ91 11 24682144 ß 2014 WILEY-VCH Verlag GmbH & Co. KGaA,Weinheim
like neurotransmission, platelet aggregation, egg fertilization, cardiovascular, and immune responses is well elucidated [7–9]. In plants too, it plays an essential role in actions like programmed cell death, stomatal closure, seed dormancy, stress physiology, and many others [9– 11]. However, the exact mechanism of NO action and interaction with other molecules is yet to be conclusively understood. With increasing research focusing on NO, it has come up as an essential intermediary signaling molecule in plant–microbe interactions although most of the information available till date is from plants [4, 12– 16]. In bacteria, two main pathways exist for the production of NO, arginine (Arg)-dependent and Argindependent. The key gene involved in the Arg-dependent pathway is nitric oxide synthase (nos) [9, 17] whereas in the latter, the genes involved are nitrate reductase (nar) and nitrite reductase (nir) [4, 5]. Indole-3-acetic acid (IAA) plays an indispensible role in coordination of plant growth and development [reviewed in Ref. [18]] and has been established as a crucial player in various plant–microbe interactions [19–21]. Although
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IAA production in plants and bacteria share similar biosynthesis pathways, the documented pathways in bacteria are largely classified as tryptophan (Trp)dependent and Trp-independent pathways [22, 23]. Recent advances highlight that both IAA and NO modulate the expression of genes and accumulation of signaling molecules that are a part of essential transduction cascades [2, 6, 22, 24–27]. Results presented in earlier reports confirm that in plants there is a correlation between the NO and IAA levels as observed in case of control explants, control explants containing the NO scavenger 2-(4-carboxyphenyl)-4,4,5,5,-tetramethylimidazoline-1-oxyl-3-oxide (cPTIO), auxin depleted explants, explants with exogenous auxin addition, and those with additional auxin and cPTIO [14, 16]. Similar correlation of NO and IAA levels has not been reported from bacteria till date. Hence, the study of the bacterial genes influenced by these phytohormones and gasotransmitters will yield important information that may subsequently be applied to a variety of aspects of microbial biotechnology and agriculture including biofertilizers and biopesticides. This review attempts to identify such bacterial genes or their elements that may have implications for future use in improving plant productivity and plant–microbe interactions.
The IAA impact IAA is an auxin which plays a crucial role in a number of aspects of plant growth and development ranging from apical dominance to senescence [28, 29]. Apart from its production in plants, various bacteria are known to produce IAA, essentially PGP bacteria [2]. Bacteria do not require IAA for their physiological processes and its biosynthesis can be cited as an example of mutualistic existence [6]. IAA influences a number of plant genes most of which have been cloned and characterized further [reviewed in Refs. 30, 31–33]. In contrast, there are only few reports regarding bacterial genes influenced by IAA and these are summarized in Table 1. Over the years, various biosynthetic pathways have been studied for the production of IAA in plants and bacteria and these include the indole-3-pyruvic acid (IPyA) and indole-3-acetamide (IAM) pathway. Indole-3pyruvate decarboxylase (ipdC or ppdC) is the main gene of the IPyA pathway while tryptophan-2-monooxygenase (iaaM) is the gene central to the IAM pathway [34, 35]. The auxin (IAA)-responsive nature of ipdC in A. brasilense was demonstrated by creating an ipdC derivative of strain Sp245 [36]. This study confirmed the upregulation of ipdC under IAA induction, however, no upregulation was ß 2014 WILEY-VCH Verlag GmbH & Co. KGaA,Weinheim
observed with the IAA precursor (Trp), acetic acid or IAA conjugates. This was the first report describing induction of any bacterial gene by IAA. Vande Broek et al. [37] studied the A. brasilense Sp245 ipdC promoter region, which revealed a bacterial auxinresponsive element (AuxRE). Subsequent mutational analysis of IaaC demonstrated that this protein is involved in controlling IAA biosynthesis and not ipdC expression in strain Sp245. Other A. brasilense strains, Sp7 and SM were found not to harbor the iaaC gene and sequence analysis of strain SM ipdC locus confirmed a 705 bp deletion from the 50 end of the iaaC gene [19]. Thus, the structural organization of the ipdC locus varies in different strains of A. brasilense and the presence of IaaC along with specialized promoter features determines the gene response or inducibility to auxins, other chemicals, and environmental conditions like pH and temperature [19]. Apart from acting as a positive regulator in the IPyA pathway, IAA has been established as a signaling molecule in A. brasilense. A high throughput gene expression analysis was carried out to investigate the effect of exogenous IAA on A. brasilense Sp245 genes [38]. The study was conducted with both wildtype and ipdC mutant and eight clusters of differentially expressed genes were found. Such genes included genes for signal transduction, energy production and conversion, NO production, aromatic hydrocarbon degradation, outer membrane biogenesis, type VI secretion system (T6SS), etc. This study established that IAA could be the trigger for A. brasilense to interact with plants. Further work needs to be done in this area for functional characterization of these differentially expressed genes and determine their relevance in the context of bacteria–plant interactions. In addition to the PGP bacteria–plant interaction, another beneficial association exists in the soil, between the rhizobia, and leguminous plants [39]. In this interaction, rhizobia detect the signaling molecules (e.g., flavonoids) released by the plants and the subsequent signaling pathway elicits nodulation in the plants [29]. Studies have shown the accumulation of IAA in these root nodules and subsequently the partial prokaryotic nature of this IAA was confirmed [[40, 41], and references therein]. Spaepen et al. [42] analyzed the change in gene expression of various rhizobial genes under the influence of IAA in Rhizobium etli CNPAF512 using a transposon (mTn5gusA-oriV) mutant library. Prior to this study, the definitive role of IAA from the bacterial partner of this symbiotic relationship was not known. Of the 30 selected genes studied by mutagenesis only four mutants showed significantly altered gene
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expression and were involved in essential processes like motility, signaling, and plant root attachment. The four gene sequences when translated in silico, showed sequence homology with cbg1-encoded b-glucosidase of Agrobacterium tumifaciens B3/73, RapB1 protein of R. leguminosarum bv. trifolii R200, flagellar hook protein FlgE, and hypothetical protein RL0670 of R. leguminosarum bv. viciae 3841. The above mentioned Rhizobium-adhering protein (Rap) possesses the Ra (Rhizobium-adhering) domain and is capable of interacting with bacterial cell surfaces [43]. Studies by Mongiardini et al. [44] have shown that overexpression of Rap genes cause higher adsorption of rhizobia to plant roots. FlgE showed a downregulation in its expression under IAA induction. Flagellar hook which connects the basal body with the filament, is a highly curved tubular structure made of about 120 copies of a single protein, FlgE. The hook is essential for dynamic and efficient bacterial motility and taxis [45]. Decreased expression of this protein and overexpression of Rap genes under IAA induced conditions suggest that IAA could play an essential role in colonization of the bacteria over the root surfaces. In future, it may be interesting to look at the presence and function of similar genes like the ones mentioned here from known PGP strains and evaluate their role in plant root colonization and regulation of PGP fuctions. The most well established and studied model system involving IAA in plant–pathogen interactions is crown
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gall formation by Agrobacterium tumefaciens [25]. IPyA is the key pathway for IAA biosynthesis both in plants as well as bacteria, however, indole-3-acetamide (IAM) pathway is exclusive to bacteria as a two-step Trpdependent pathway which may be constitutive in nature [46]. Herein, the iaaM encoded enzyme decarboxylates Trp to form the intermediate IAM which is converted to IAA by the iaaH encoded enzyme, indole acetamide hydrolase (IAH). The IAM pathway is mostly involved in gall formation and most of the phytopathogens possess this pathway [25, 26]. Nevertheless, there are preliminary reports of the IAM pathway’s existence in PGP bacteria P. fluorescens Psd [46]. Hutcheson and Kosuge [47] elucidated for the first time that IAA production in P. syringae pv. savastanoi is regulated by feedback inhibition from IAM and IAA. The conversion of Trp to IAA is regulated at the first step involving iaaM. This clearly indicates that iaaM is an IAA responsive gene. In A. tumefaciens, these genes are located on the T-DNA of the Ti plasmid in all virulent strains and may play crucial roles in their pathogenicity [25, 48]. Strains with mutated/cured Ti plasmids lose their pathogenicity and when reintroduced pathogenicity was reinstated [25, 49]. In phytopathogens, IAA is presumed to enhance their ability to act as an epiphyte on plant surfaces, detoxify tryptophan analogues, and inhibit the plant hypersensitive response to expedite bacterial invasion. The presence of IAM pathway for IAA biosynthesis was demonstrated
Table 1. Bacterial genes and proteins influenced by Indole-3-acetic acid. Gene/protein influenced ipdC iaaM RapB1 FlgE RL0670 leuD sucA gltA sucD sdhB/sdhC aceA cycA dnaK leuB glpK adhE arcD galR ogl pelD/pelI/pelL dspE hrpN
Known/predicted function
Expression
Organism
Reference
IAA production (IPyA pathway) IAA production (IAM pathway) Rhizobium adherence Flagella formation Hypothetical protein 3-Isopropylmalate isomerase 2-Oxoglutarate dehydrogenase Citrate synthase Succinyl-CoA synthetase Succinate dehydrogenase aceA Isocitrate lyase D-Alanine/D-serine/glycine transport protein Chaperone Hsp70 3-Isopropylmalate dehydrogenase Glycerol kinase Alcohol dehydrogenase Arginine/ornithine antiporter Transcriptional repressor for galactose utilization Oligogalacturonate lyase Endopectate lyase putative T3SS effector T3SS harpin
Upregulated Upregulated Upregulated Downregulated Upregulated Upregulated Upregulated Upregulated Upregulated Upregulated Upregulated Upregulated Upregulated Upregulated Upregulated Downregulated Downregulated Downregulated
Azospirillum brasilense Pseudomonas syrinae pv. savastanoi Rhizobium etli CNPAF512 R. etli CNPAF512 R. etli CNPAF512 Escherichia coli MG1655 E. coli MG1655 E. coli MG1655 E. coli MG1655 E. coli MG1655 E. coli MG1655 E. coli MG1655 E. coli MG1655 E. coli MG1655 E. coli MG1655 E. coli MG1655 E. coli MG1655 E. coli MG1655
[19, 36, 37] [47] [42] [42] [42] [24] [24] [24] [24] [24] [24] [24] [24] [24] [24] [24] [24] [24]
Upregulated Upregulated Upregulated Upregulated
Erwinia chrysanthemi 3937 E. chrysanthemi 3937 E. chrysanthemi 3937 E. chrysanthemi 3937
[50] [50] [50] [50]
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in the non-gall forming phytopathogen, Erwinia chrysanthemi 3937. The decreased production of IAA caused reduced levels of the extra-cellular enzyme, pectate lyase and down-regulation of the type III secretion system (T3SS) genes. In the iaaM knockout mutant, the expression levels of an oligogalacturonate lyase gene, ogl, and three endopectate lyase genes, pelD, pelI, and pelL were reduced in comparison to the wild-type strain. The cytoplasmic oligogalacturonate lyase and pectate lyases, cleave glycosidic linkages by b-elimination, thereby causing maceration and soft rotting of plant tissue. Also, the transcription of T3SS genes, dspE (a putative T3SS effector) and hrpN (T3SS harpin), was found to be diminished in the iaaM mutant [50]. T3SS of Gramnegative bacteria allow establishment of bacterial pathogenicity by translocation of virulence factors from bacteria into host eukaryotic cells [51]. Apart from soil PGP bacteria, IAA has been reported to influence more than one percent genes in the central metabolic pathways in the laboratory strain, Escherichia coli K-12 MG 1655 [24]. Though, it is not exposed to IAA in its natural environment, in vitro studies revealed that IAA induction mainly altered the expression of essential genes associated with energy metabolism and amino acid biosynthesis. Genes with upregulated expression were involved in the TCA cycle (gltA, sucA, sucD, sdhB, and sdhC), glyoxylate shunt, and amino acid biosynthesis (proA). Also a correlation was seen between the upregulation of gene expression (aceA) and activation of the corresponding enzymes (isocitrate lyase). As no physiological function of IAA is clear from the soil PGP bacteria, similar studies could be carried out in various soil and PGP bacteria to demonstrate the definitive role of IAA in essential metabolic pathways of soil microbes. This information will be valuable in aiding the selection of microbial strains for use as biofertilizers, for specific soil types and application in specific environmental conditions. Recently, IAA-responsive genes were also identified in Saccharomyces cerevisiae, and perception of IAA was found to cause differentiation of the yeast cells into a filamentous, invasive form [27]. These findings suggest that proteins involved in IAA perception and signal transduction are not only present in higher plants but also in bacteria and fungi which provide leads for further investigation into the subject and to generate insights for development of host plant.
The NO-influence Nitric oxide is a free radical with its role in toxicity and as a signaling molecule well elucidated in mammals [52, 53]. ß 2014 WILEY-VCH Verlag GmbH & Co. KGaA,Weinheim
However, little is known about its biological role in plants and bacteria. Grün et al. [13] carried out a large scale transcriptional analysis to identify the effect of NO on various essential genes in Arabidopsis thaliana. These genes were involved in processes like stress response, S-nitrosylation, and plant–pathogen interactions. Further details of NO responsive genes from plants can be found in Besson-Bard et al. [54]. Despite its increasing significance, not much information is available about the NO-influenced bacterial genes. Cyclic Nucleotide Monophosphates (cNMPs) are wellestablished members of key signal-transduction pathways in eukaryotes and recently, cAMP, c-di-GMP, c-di-AMP, and cGMP have been found to play essential roles in bacteria, with cyclic dimeric GMP (c-di-GMP) and cyclic dimeric AMP (c-di-AMP) being ubiquitous bacterial messengers [55–58]. Synthesis of cAMPs, cGMPs, c-diAMP, and c-di-GMP is catalyzed by nucleotidyl cyclases and dinucleotidyl cyclases, while degradation of cNMPs/cdi-NMPs is achieved by phosphodiesterases (PDE) [55]. Thus, the concentration of cNMP/c-di-NMP is regulated in the cell by the antagonistic action of these two enzymes. Guanylyl cyclases (GCs) are expressed in two isoforms: the soluble (sGC) and particulate or membrane-bound (pGC) form [59]. Bacterial cNMP and c-di-NMPs have been reported to influence essential physiological characteristics like surface attachment, motility, virulence, and biofilm/cyst formation [57, 58, 60–64]. However, the exact mechanism is mostly unknown. Although it was known that sGCs sense NO by means of its heme moiety but the presence of Heme-Nitric oxide/OXygen (H-NOX) domain in the N-terminal extensions of sGCs by in silico analysis has been identified [65]. H-NOX is a large family of heme binding proteins which have the ability to bind diatomic gases (like NO, O2, CO, etc.) with selective discrimination [66, 67]. HNOB (heme NO binding) domains have been found to be either fused to other receptors like methyl-accepting domains of chemotaxis receptors or as standalone proteins [65, 68]. The presence of a distal pocket tyrosine for discrimination between O2 and NO binding is the molecular basis for the remarkable ligand selection displayed by H-NOX and subsequently by sGC [66]. In the absence of tyrosine, the dissociation rate of O2 increases and formation of any O2 complex is not possible; however, the dissociation of NO remains unchanged and leads to specific NO affinity [69]. Thus, H-NOX domain of bacterial sGC acts as a NO sensor and it can now be predicted that the genes possessing it will be NO-responsive. Consequently, NO modulation in bacteria may be achieved through such target genes. Since the activation of sGC directly leads to cyclization of GTP to cGMP, any alteration in its expression can lead
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to major changes in the cGMP-dependent/involved pathways. Figure 1 shows the different aspects of cGMP in bacterial systems, its relationship with NO and downstream pathways. Even though biofilm formation is a complex process with its exact mechanism largely unknown, cGMP/c-di-GMPs have been established as the essential signaling molecules in this process [56, 70–72]. Liu et al. [72] demonstrated the negative effect of NO on biofilm formation in Shewanella woodyi MS32 by regulating c-di-GMP levels. Nanomolar concentration of NO is detected by S. woodyi H-NOX (SwH-NOX) causing a decrease in intracellular c-di-GMP levels and subsequent decrease in biofilm formation. S. woodyi diguanylate cyclase (SwDGC) was reported to be a dual-functioning DGC with both DGC and PDE activities where DGC activity is predicted by a conserved GGDEF amino acid motif and that of PDE by EAL or HD-GYP domains [63, 73]. The study revealed that in the absence of NO, SwH-NOX activates the DGC activity of SwDGC. However, in its presence, SwHNOX upregulates PDE activity and c-di-GMP degradation is enhanced, subsequently leading to thinning of the biofilm. Prior to this work, the role of biofilm dispersal induced by NO in opportunistic bacteria, Pseudomonas aeruginosa was investigated [74, 75]. Low levels of NO were shown to stimulate PDE activity and subsequent switch from biofilm to planktonic phenotype. Further analysis validated that this process required c-di-GMP and the chemotaxis transducer BdlA and a direct link between NO
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and c-di-GMP was established. Such results point to the fact that cNMPs may play an important role in the signaling and sensing of NO produced by PGP bacteria and this is worth investigating in future. Cell-to-cell communication between the bacteria in a cell density-dependent manner is a mechanism defined as quorum sensing (QS) which has now been observed in both Gram-negative and Gram-positive bacteria to regulate processes like bioluminescence, biofilm formation, and virulence [76, 77]. Any QS system consists of the genes involved in the production and sensing of the autoinducer (AI) signaling molecules, commonly N-acyl-homoserine lactones (AHL). In Vibrio harveyi, three QS circuits have been demonstrated so far: LuxM/LuxN, LuxS/LuxPQ , and CqsA/CqsS, named for the AI synthase/receptor pair [78]. Above a threshold concentration of the AI, the receptor molecule switches its activity from kinase to phosphatase, causing the transfer of phosphate to the common phosphorelay protein, LuxU. LuxU subsequently phosphorylates the transcription factor, LuxO which indirectly represses the master regulator of QS, LuxR [53, 78]. Thus, at low cell density and low AI levels, expression of LuxR is repressed and V. harveyi does not show bioluminescence. The H-NOX/HqsK (heme-nitric oxide/oxygen binding domain; H-NOX-associated quorum sensing kinase) QS pathway was recently discovered in V. harveyi where NO/ H-NOX regulates phosphorylation of the kinase and initiates the phosphorylation through LuxU/LuxO/LuxR
Figure 1. Schematic representation of synthesis, degradation, and function of cGMP. The three targets of cGMP molecules are (i) cGMP dependent protein kinases, (ii) cGMP gated ion channels and (iii) cGMP-dependent phosphodiesterases. While phosphodiesterases are involved in the degradation of cGMP to GMP, the protein kinases and activation of ion channels are subsequently involved in various bacterial signaling pathways. GTP: Guanosine 50 -triphosphate; sGC: soluble guanylate cyclase; NO: nitric oxide; H-NOX: Heme-Nitric oxide/Oxygen
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pathway. This study established that NO acts analogously with other AIs and positively regulates bioluminescence in V. harveyi [78]. Apart from bioluminescence, in recent times NO-responsive biofilm formation is also being explored in V. harveyi. Biofilm formation in bacteria in response to NO has already been established but it has been associated with c-di-GMP signaling [52, 60, 64, 74, 79]. However, it has been reported that biofilm formation is also regulated by the H-NOX/HqsK QS pathway. Mutational, genetic, and proteomic studies were carried out to illustrate that at low concentration of NO, H-NOX positively regulates the V. harveyi biofilm enhancement through the H-NOX-associated QS kinase [79]. It still waits to be seen if the similar traits of PGP bacteria involve NO-dependent signaling. It may also be important to study if some other PGP traits in addition to biofilm formation involve QS mechanisms. Detoxifying enzymes like flavorubredoxin nitric oxide reductase (NorVW), nitric oxide reductase (NorB), and nitrite reductase (NrfA) convert NO to less toxic derivatives-nitrate, nitrous oxide, and ammonia and this is controlled by a variety of transcription factors [53]. These processes include regulatory proteins which may or may not be involved in the bacterial response to NO and include SoxR, FNR, NorR, Fur, NnrR, NsrR, H-Nox [detailed in Ref. 67]. SoxR was the first reported case of a bacterial transcriptional regulator responding to NO. It is a redox-sensitive activator dependent on the oxidation state of its binuclear [2Fe–2S] cluster, which is sensitive to NO [80, 81]. Ding and Demple [82] demonstrated that in E. coli, SoxR activation by NO occurs through direct modification of the iron–sulfur center to form proteinbound dinitrosyl–iron dithiol adducts. This observation was made in case of intact bacterial cells as well as in purified SoxR after NO treatment and established the direct role of NO in signal transduction [82]. Another regulator is FNR which possesses an iron–sulfur cluster. A study by Cruz-Ramos et al. [83] accentuated that the flavohaemoglobin Hmp of E. coli is involved in the protective response to NO. The transcription of hmp is
regulated by FNR, which was known to possess [4Fe–4S] cluster and be O2-responsive in nature. Aerobically, Hmp detoxifies NO by acting as an NO oxygenase or denitrosylase, whereas, under anaerobic conditions, the DNA-binding activity of FNR is lowered as NO reacts with the Fe–S cluster and forms dinitrosyl–iron complexes converting NO to lesser toxic forms like nitrous oxide [83–85]. Proteins/regulators that have been identified as NO sensors are mentioned in Table 2.
Genetic regulation (s54-dependence) Various molecular approaches such as macroarray/ microarray analysis and real-time PCR have been used to study primary plant auxin responsive genes. Within the promoters of these genes, cis elements have been observed that confer auxin responsiveness and are referred to as auxin-responsive elements or AuxREs. Associated to these is a family of trans-acting transcription factors that are identified as auxin-response factors or ARFs that bind with specificity to AuxREs. A family of auxin regulated proteins referred to as Aux/IAA proteins also play a key role in regulating these auxin responsive genes. Auxins may regulate transcription of early response genes in plants by influencing this type of interactions between ARFs and Aux/IAAs [32]. The alternative sigma factor, s54 controls several ancillary processes including phytochemical degradation, pilin synthesis and flagellar assembly, arginine catabolism, nitrogen fixation, and auxin biosynthesis among many other processes. It is unable to initiate transcription spontaneously and is dependent on additional factors called enhancer binding proteins (EBP) [86]. s54 recognises promoter sequences carrying conserved GG and GC elements at 24 and 12 positions in a variety of genes along with their EBP [86]. Most prominently, these include nif (nitrogen fixation structural genes), glnB (regulatory protein for glutamine synthase) genes from soil bacteria Azospirillum, Rhizobium, Bradyrhizobium,
Table 2. Bacterial proteins influenced by nitric oxide. Protein/regulator influenced
Known/predicted function
NO sensor
Organism
Reference
SoxR FNR NorR
Defence against superoxide and NO NO detoxification NO detoxification
[2Fe–2S] [4Fe–4S] Non-heme iron
[68, 80–82] [68, 81, 83, 93] [68, 81, 88, 93]
H-NOX
Sensing diatomic gases (O2/NO)
Heme
Hmp
NO detoxification
[4Fe–4S]
Escherichia coli E. coli, Rhodobacter sphaeroides E. coli, Ralstonia eutropha, Pseudomonas aeruginosa Vibrio harveyi, V. cholerae, Shewanella woodyi, Thermoanaerobacter tengcongensis E. coli
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[65, 66, 68, 72, 81] [83, 84, 93]
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Klebsiella, Pseudomonas, and Azorhizobium. Further details of the domain architectures may be found in Studholme and Dixon [87]. More recently, the transcription of norVW is activated by a s54-dependent enhancer binding protein, NorR, to which the NO sensing property is imparted by the mononuclear non-heme iron centre [68, 88]. Expression studies of a cytochrome P450 homolog from Rhizobium sp. BR816, CYP127A2 pointed to a NifA- and s54dependent transcription [89]. The conserved regions of the s54-dependent promoters and the upstream activating sequence (UAS) that activates s54-dependent transcription (RpoN) were found in the P450 homolog [89]. Such UAS sequences have also been reported upstream of the nifHc gene of R. etli [90]. In Rhizobium CNPAF512, NifA has been shown to control the symbiotic expression of nif genes [91]. CYP127A2 was expressed at a low level under free-living conditions, whereas higher expression was reported from the bacteroids. This expression pattern of CYP127A2 is in accordance with the wild-type Rhizobium strain BR816 and confirmed that CYP127A2 expression is regulated by RpoN and NifA [89]. A dyadic sequence (DS, ATTGTTTC(GAAT)GAAACAAT) is located in the 50 upstream region of ipdC between positions 58 and 38, with a perfect two 8-bp inverted repeat separated by a 4-bp spacer [19, 37]. Site-directed mutagenesis and deletion demonstrated that this element, referred to as a bacterial auxin-regulated element, is essential for the IAA inducibility of genes and is related to the AuxRE of plants, TGTCNC or the degenerate version (G/T)GTCCCAT. The short sequence, TGTCCC (Sequence Element 1 or SE1) was found to be located at position 3 to 8 in A. brasilense [19, 37, 92]. An in silico sequence analysis based on homology of the A. brasilense SM ipdC gene with that from Sp245 and Sp7 showed the three SEs in the 50 upstream region of the ipdC coding region. These included SE1 and SE2 which are a part of composite promoters of auxin-responsive genes that function together with a coupling element overlapping or adjacent to the AuxRE. The two SEs occupy the 12 and 24 recognition sequence of the s54-dependent promoters [19]. SE3 was same as the DS, centered at position 48 in Sp245 as explained by Vande Broek et al. [37]. Since the presence of such features determine the auxin inducibility of associated genes, they may play an important role in determining the application of the PGP bacteria as biofertilizers for important plant growth.
Conclusion Plants convert various inorganic molecules into essential organic compounds like sugars, amino acids, organic ß 2014 WILEY-VCH Verlag GmbH & Co. KGaA,Weinheim
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acids, antibiotics, and secondary metabolites in the presence of sunlight. A part of the root exudates is released by plants into the rhizosphere creating a conducive/favorable environment for diverse microbial growth that act as insurance for improving plant productivity. This includes their ability to form wellstructured biofilms, provide them advantages like communicating by cell-to-cell signaling, nutrient acquisition, migrating collectively, and increased resistance against environmental and other stresses. Microbes maintain a critical mass of cells so that they can excrete essential metabolites above a threshold concentration that is required by the associated host plant. Being a part of a biofilm will also augment the ability of the microbe to act as a biocontrol agent for plants. NO, a small diatomic molecule is gaining immense importance in the field of research which can be substantiated by an increase in the number of publications elucidating its role in mammals, plants, and most importantly bacteria. However, the exact working mechanism of NO is still widely debated due to its gaseous nature and high reactivity which causes experimental limitations. Also, inadequate information is available about various NO-responsive and influenced genes. Similarly, IAA is known as an essential phytohormone for a long time but on IAA exposure, a number of bacterial genes are influenced. It is likely that IAA and NO produced by PGP bacteria may interact in the rhizosphere with other members of the rhizosphere microbiome and the presence of s54 transcription for genes involved in the metabolism of such plant growth regulators may open up a further field of study under changing environments (nutrient and limiting environment conditions). The bacterial NO and IAA induced genes or proteins may play an important role in signaling and sensing of other hormones by plants in the rhizosphere. Figure 2 shows a hypothetical model of the crosstalk involving IAA and NO produced by the rhizosphere bacteria and their effect on plants. This model highlights the importance of signaling involving the auxins, and NO and their likely common genetic regulation. For better understanding of the interactions between these molecules, more information needs to be gathered about the genes and proteins which are involved in these processes. Future efforts should be made to identify differentially expressed genes in response to these plant growth regulators and their relevance in improving plant growth as many of the PGP bacteria act as biofertilisers. Keeping in view the current available information, interplay between IAA and NO cannot be ruled out in the rhizosphere
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Figure 2. Schematic representation of the crosstalk involving indole-3-acetic acid (IAA) and nitric oxide (NO) produced by rhizosphere bacteria and their effect on plants. cGMP acts as an extracellular signal in plants which are likely modulated by bacterial NO through IAA. NO-mediated inhibition of ethylene biosynthesis has also been observed. Microbially produced IAA directly influences plant root proliferation. The NH3 released in the rhizosphere is fixed by N2-fixing PGPR which along with biomineralization of complex nutrient sources allows enhanced mineral/nutrient uptake leading to improved plant growth. NO activates metabolic and physiological responses in plants by three distinct mechanisms involving [a] a cGMP-dependent pathway, [b] a cGMP-independent route, and [c] NO action on MAPK activities, which are involved in many physiological adaptation and developmental processes [22]. IAA is self-inducible which may be initiated by signals from plant root exudates. [—] represents inhibition of processes, [!] shows induction of biosynthesis, and [ ] identify the mechanisms that beneficially influence plant growth.
bacteria. Consequently, it is extremely important to study the extent of influence of microbial plant growth regulators, IAA and NO so that their effect on plants can be judged for their appropriate action and application.
Acknowledgments The review was prepared as part of a project funded by the Department of Biotechnology to M.K. The authors thank Director General, TERI for the infrastructure support provided.
References [1] Benizri, E., Baudoin, E., Guckert, A., 2001. Root colonization by inoculated plant growth-promoting rhizobacteria. Biocontrol Sci. Technol., 11, 557–574. [2] Kochar, M., Srivastava, S., 2012. Surface colonization by Azospirillum brasilense SM in the indole-3-acetic acid dependent growth improvement of sorghum. J. Basic Microbiol., 52, 123–131. [3] Mazzola, M., Cook, R.J., Thomashow, L.S., Weller, D.M., Pierson, L.S., 1992. Contribution of phenazine antibiotic biosynthesis to the ecological competence of fluorescent pseudomonads in soil habitats. Appl. Environ. Microbiol., 58, 2616–2624.
Conflict of interest statement
[4] Molina-Favero, C., Creus, C.M., Lanteri, M.L., CorreaAragunde, N. et al., 2007. Nitric oxide and plant growth promoting rhizobacteria: common features influencing root growth and development. Adv. Bot. Res., 46, 1–33.
There is no conflict of interest.
[5] Molina-Favero, C., Creus, C.M., Simontacchi, M., Puntarulo, S., Lamattina, L., 2008. Aerobic nitric oxide production by
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J. Basic Microbiol. 2014, 54, 1–11
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Azospirillum brasilense Sp245 and its influence on root architecture in tomato. Mol. Plant Microbe Interact., 21, 1001–1009. [6] Somers, E., Vanderleyden, J., Srinivasan, M., 2004. Rhizosphere bacterial signalling: a love parade beneath our feet. Crit. Rev. Microbiol., 30, 205–240. [7] Boon, E.M., Marletta, M.A., 2005. Ligand specificity of HNOX domains: from sGC to bacterial NO sensors. J. Inorg. Biochem., 99, 892–902. [8] Dobutovic, B., Smiljani, K., Soski, S., Düngen, H., Isenovi, E.R., 2011. Nitric oxide and its role in cardiovascular diseases. Open Nitric Oxide J., 3, 65–71. [9] Rafferty, S., 2011. Nitric oxide synthases of bacteria – and other unicellular organisms. Open Nitric Oxide J., 3, 325– 332. [10] Garcia-Mata, C., Lamattina, L., 2002. Nitric oxide and abscisic acid cross talk in guard cells. Plant Physiol., 128, 790–792. [11] Giba, Z., Grubišić, D., Konjević, R., 2006. Seeking the role of NO in breaking seed dormancy, in: Lamattina, L., Polacco, J.C. (Eds.), Nitric Oxide in Plant Growth. Plant Cell Monographs, Springer-Verlag, Berlin, Heidelberg, 91–111. [12] Cohen, M.F., Lamattina, L., Yamasaki, H., 2010. Nitric oxide signaling by plant-associated bacteria, in: Hayat, S., Mori, M., Pichtel, J., Ahmad, A. (Eds.), Nitric Oxide in Plant Physiology, Wiley-VCH, Verlag GmbH and Co. KGaA, Weinheim, 161–172.
9
[22] Kochar, M., Vaishnavi, A., Upadhyay, A., Srivastava, S., 2013. Bacterial biosynthesis of indole-3-acetic acid: signal messenger service, in: de Bruijn, F.J. (Ed.), Molecular Microbial Ecology of the Rhizosphere: Volume 1. John Wiley & Sons, Inc., Hoboken, NJ, USA, 309–326. [23] Spaepen, S., Vanderleyden, J., Remans, R., 2007. Indole-3acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol. Rev., 31, 425–448. [24] Bianco, C., Imperlini, E., Calogero, R., Senatore, B. et al., 2006. Indole-3-acetic acid regulates the central metabolic pathways in Escherichia coli. Microbiology, 152, 2421–2431. [25] Jameson, P.E., 2000. Cytokinins and auxins in plant– pathogen interactions – an overview. Plant Growth Reg., 32, 369–380. [26] Lambrecht, M., Okon, Y., Vande Broek, A., Vanderleyden, J., 2000. Indole-3-acetic acid: a reciprocal signalling molecule in bacteria–plant interactions. Trends Microbiol., 8, 298–300. [27] Prusty, R., Grisafi, P., Fink, G.R., 2004. The plant hormone indole acetic acid induces invasive growth in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA., 101, 4153–4157. [28] Kukreja, K., Suneja, S., Goyal, S., Narula, N., 2004. Phytohormone production by Azotobacter – a review. Agric. Rev., 25, 70–75. [29] Spaepen, S., Dobbelaere, S., Croonenborghs, A., Vanderleyden, J., 2008. Effects of Azospirillum brasilense indole-3acetic acid production on inoculated wheat plants. Plant Soil, 312, 15–23.
[13] Grün, S., Lindermayr, C., Sell, S., Durner, J., 2006. Nitric oxide and gene regulation in plants. J. Exp. Bot., 57, 507– 516.
[30] Chapman, E.J., Estelle, M., 2009. Mechanism of auxinregulated gene expression in plants. Annu. Rev. Genet., 43, 265–285.
[14] Pagnussat, G.C., Lanteri, M.L., Lamattina, L., 2003. Nitric oxide and cyclic GMP are messengers in the indole acetic acid-induced adventitious rooting process. Plant Physiol., 132, 1241–1248.
[31] Goda, H., Sawa, S., Asami, T., Fujioka, S. et al., 2004. Comprehensive comparison of auxin-regulated and brassinosteroid-regulated genes in Arabidopsis. Plant Physiol., 134, 1555–1573.
[15] Pagnussat, G.C., Lanteri, M.L., Lamattina, L., 2004. Nitric oxide mediates the indole acetic acid induction of a mitogen-activated protein kinase cascade involved in adventitious root development. Plant Physiol., 135, 279– 286.
[32] Hagen, G., Guilfoyle, T., 2002. Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol. Biol., 49, 373–385.
[16] Pagnussat, G.C., Simontacchi, M., Puntarulo, S., Lamattina, L., 2002. Nitric oxide is required for root organogenesis. Plant Physiol., 129, 954–956.
[34] Malhotra, M., Srivastava, S., 2006. Targeted engineering of Azospirillum brasilense strain SM with Indole acetamide pathway for IAA over-expression. Can. J. Microbiol., 52, 1078–1084.
[17] Chen, Y., Rosazza, J.P.N., 1994. A bacterial nitric oxide synthase from a Nocardia species. Biochem. Biophys. Res. Commun., 203, 1251–1258.
[33] Simon, S., Petrášek, J., 2011. Why plants need more than one type of auxin. Plant Sci., 180, 454–460.
[18] Woodward, A.W., Bartel, B., 2005. Auxin: regulation, action, and interaction. Ann. Bot., 95, 707–735.
[35] Steenhoudt, O., Vanderleyden, J., 2000. Azospirillum, a freeliving nitrogen-fixing bacterium closely associated with grasses: genetic, biochemical and ecological aspects. FEMS Microbiol. Rev., 24, 487–506.
[19] Malhotra, M., Srivastava, S., 2008. Organization of the ipdC region regulates IAA levels in different Azospirillum brasilense strains: molecular and functional analysis of ipdC in strain SM. Environ. Microbiol., 10, 1365–1373.
[36] Vande Broek, A., Lambrecht, M., Eggermont, K., Vanderleyden, J., 1999. Auxins upregulate expression of the indole-3-pyruvate decarboxylase gene in Azospirillum brasilense. J. Bacteriol., 181, 1338–1342.
[20] Spaepen, S., Vanderleyden, J., 2011. Auxin and plant– microbe interactions. Cold Spring Harb. Perspect. Biol., 3, a001438.
[37] Vande Broek, A., Gysegom, P., Ona, O., Hendrickx, N. et al., 2005. Transcriptional analysis of the Azospirillum brasilense indole-3-pyruvate decarboxylase gene and identification of a cis-acting sequence involved in auxin responsive expression. Mol. Plant Microbe Interact., 18, 311–323.
[21] Sukumar, P., Legué, V., Vayssières, A., Martin, F. et al., 2013. Involvement of auxin pathways in modulating root architecture during beneficial plant–microorganism interactions. Plant Cell Environ., 36, 909–919. ß 2014 WILEY-VCH Verlag GmbH & Co. KGaA,Weinheim
[38] Van Puyvelde, S., Cloots, L., Engelen, K., Das, F. et al., 2011. Transcriptome analysis of the rhizosphere bacterium
www.jbm-journal.com
J. Basic Microbiol. 2014, 54, 1–11
10
Vatsala Koul et al.
Azospirillum brasilense reveals an extensive auxin response. Microb. Ecol., 61, 723–728. [39] Theunis, M., Kobayashi, H., Broughton, W.J., Prinsen, E., 2004. Flavonoids, NodD1, NodD2, and nod-box NB15 modulate expression of the y4wEFG locus that is required for indole-3-acetic acid synthesis in Rhizobium sp. strain NGR234. Mol. Plant Microbe Interact., 17, 1153–1161. [40] Mathesius, U., Schlaman, H.R., Spaink, H.P., Sautter, C. et al., 1998. Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides. Plant J., 14, 23–34. [41] Glick, B.R., 2012. Plant growth-promoting bacteria: mechanisms and applications. Scientifica, Article ID: 963401. [42] Spaepen, S., Das, F., Luyten, E., Michiels, J., Vanderleyden, J., 2009. Indole-3-acetic acid-regulated genes in Rhizobium etli CNPAF512. FEMS Microbiol. Lett., 291, 195–200. [43] Ausmees, N., Jacobsson, K., Lindberg, M., 2001. A unipolarly located, cell-surface-associated agglutinin, RapA, belongs to a family of Rhizobium-adhering proteins (Rap) in Rhizobium leguminosarum bv. trifolii. Microbiology. 147, 549–559. [44] Mongiardini, E.J., Ausmees, N., Perez-Gimenez, J., Althabegoiti, M.J. et al., 2008. The rhizobial adhesion protein RapA1 is involved in adsorption of rhizobia to plant roots but not in nodulation. FEMS Microbiol. Ecol., 65, 279–288. [45] Samatey, F.A., Matsunami, H., Imada, K., Nagashima, S. et al., 2004. Structure of the bacterial flagellar hook and implication for the molecular universal joint mechanism. Nature, 431, 1062–1068. [46] Kochar, M., Upadhyay, A., Srivastava, S., 2011. Indole-3acetic acid biosynthesis in the biocontrol strain Pseudomonas fluorescens Psd and plant growth regulation by hormone overexpression. Res. Microbiol., 162, 426–435. [47] Hutcheson, S.W., Kosuge, T., 1985. Regulation of 3indoleacetic acid production in Pseudomonas syringae pv. savastanoi. purification and properties of tryptophan 2monooxygenase. J. Biol. Chem., 260, 6281–6287. [48] Morris, R.O., 1995. Molecular aspects of hormone synthesis and action-genes specifying auxin and cytokinin biosynthesis in prokaryotes, in: Davies P.J. (Ed.), Plant Hormones, Kluwer Academic Publishers, Dordecht, 318–339. [49] Nester, E.W., Kosuge, T., 1981. Plasmids specifying plant hyperplasias. Ann. Rev. Microbiol., 35, 531–565. [50] Yang, S., Zhang, Q., Guo, J., Charkowski, A.O. et al., 2007. Global effect of indole-3-acetic acid biosynthesis on multiple virulence factors of Erwinia chrysanthemi 3937. Appl. Environ. Microbiol., 73, 1079–1088. [51] Stuber, K., Frey, J., Burnens, A.P., Kuhnert, P., 2003. Detection of type III secretion genes as a general indicator of bacterial virulence. Mol. Cell Probes, 17, 25–32. [52] Plate, L., Marletta, M.A., 2012. Nitric oxide modulates bacterial biofilm formation through a multicomponent cyclic-di-GMP signaling network. Mol. Cell, 46, 449–460. [53] Plate, L., Marletta, M.A., 2013. Nitric oxide-sensing H-NOX proteins govern bacterial communal behavior. Trends Biochem. Sci., 38, 566–575. ß 2014 WILEY-VCH Verlag GmbH & Co. KGaA,Weinheim
[54] Besson-Bard, A., Astier, J., Rasul, S., Wawer, I. et al., 2009. Current view of nitric oxide-responsive genes in plants. Plant Sci., 177, 302–309. [55] Corrigan, R.M., Gründling, A., 2013. Cyclic di-AMP: another second messenger enters the fray. Nat. Rev. Microbiol., 11, 513–524. [56] D’Argenio, D.A., Miller, S.I., 2004. Cyclic di-GMP as a bacterial second messenger. Microbiology, 150, 2497–2502. [57] Gomelsky, M., 2011. cAMP, c-di-GMP, c-di-AMP and now cGMP: bacteria use them all! Mol. Microbiol., 79, 562–565. [58] Krasteva, P.V., Giglio, K.M., Sondermann, H., 2012. Sensing the messenger: the diverse ways that bacteria signal through c-di-GMP. Protein Sci., 21, 929–948. [59] Beste, K.Y., Spangler, C.M., Burhenne, H., Koch, K.W. et al., 2013. Nucleotidyl cyclase activity of particulate guanylyl cyclase A: comparison with particulate guanylyl cyclases E and F, soluble guanylyl cyclase and bacterial adenylyl cyclases CyaA and edema factor. PLoS ONE, 29, e70223. [60] Cotter, P.A., Stibitz, S., 2007. c-di-GMP-mediated regulation of virulence and biofilm formation. Curr. Opin. Microbiol., 10, 17–23. [61] Marden, J.N., Dong, Q., Roychowdhury, S., Berleman, J.E., Bauer, C.E., 2011. Cyclic GMP controls Rhodospirillum centenum cyst development. Mol. Microbiol., 79, 600–615. [62] Sisti, F., Ha, D.G., O’Toole, G.A., Hozbor, D., Fernández, J., 2013. Cyclic-di-GMP signalling regulates motility and biofilm formation in Bordetella bronchiseptica. Microbiology, 159, 869–879. [63] Tao, F., He, Y.W., Wu, D.H., Swarup, S., Zhang, L.H., 2010. The cyclic nucleotide monophosphate domain of Xanthomonas campestris global regulator Clp defines a new class of cyclic di-GMP effectors. J. Bacteriol., 192, 1020–1029. [64] Yan, W., Qu, T., Zhao, H., Su, L. et al., 2010. The effect of cdi-GMP (30 -50 -cyclic diguanylic acid) on the biofilm formation and adherence of Streptococcus mutans. Microbiol. Res., 165, 87–96. [65] Iyer, L.M., Anantharaman, V., Aravind, L., 2003. Ancient conserved domains shared by animal soluble guanylyl cyclases and bacterial signaling proteins. BMC Genomics, 4, 5. [66] Boon, E.M., Huang, S.H., Marletta, M.A., 2005. A molecular basis for NO selectivity in soluble guanylate cyclase. Nat. Chem. Biol., 1, 53–59. [67] Derbyshire, E.R., Marletta, M.A., 2009. Biochemistry of soluble guanylate cyclase. Handb. Exp. Pharmacol., 191, 17–31. [68] Spiro, S., 2007. Regulators of bacterial responses to nitric oxide. FEMS Microbiol. Rev., 31, 193–211. [69] Boon, E.M., Marletta, M.A., 2005. Ligand discrimination in soluble guanylate cyclase and the H-NOX family of heme sensor proteins. Curr. Opin. Chem. Biol., 9, 441–446. [70] Gomelsky, M., Galperin, M.Y., 2013. Bacterial second messengers, cGMP and c-di-GMP, in a quest for regulatory dominance. EMBO J., 32, 2421–2423. [71] Jenal, U., 2004. Cyclic di-guanosine-monophosphate comes of age: a novel secondary messenger involved in modulating cell surface structures in bacteria? Curr. Opin. Microbiol., 7, 185–191.
www.jbm-journal.com
J. Basic Microbiol. 2014, 54, 1–11
Sphere of influence of IAA and NO in bacteria
[72] Liu, N., Xu, Y., Hossain, S., Huang, N. et al., 2012. Nitric oxide regulation of cyclic di-GMP synthesis and hydrolysis in Shewanella woodyi. Biochemistry, 51, 2087–2099. [73] Simm, R., Morr, M., Kader, A., Nimtz, M., Romling, U., 2004. GGDEF and EAL domains inversely regulate cyclic diGMP levels and transition from sessility to motility. Mol. Microbiol., 53, 1123–1134. [74] Barraud, N., Schleheck, D., Klebensberger, J., Webb, J.S. et al., 2009. Nitric oxide signaling in Pseudomonas aeruginosa biofilms mediates phosphodiesterase activity, decreased cyclic di-GMP levels, and enhanced dispersal. J. Bacteriol., 191, 7333–7342. [75] Boyle, K.E., Heilmann, S., van Ditmarsch, D., Xavier, J.B., 2013. Exploiting social evolution in biofilms. Curr. Opin. Microbiol., 16, 207–212. [76] Fuqua, C., Greenberg, E.P., 2002. Listening in on bacteria: acyl-homoserine lactone signaling. Nat. Rev. Mol. Cell. Biol., 3, 685–695. [77] Miller, M.B., Bassler, B.L., 2001. Quorum sensing in bacteria. Annu. Rev. Microbiol., 55, 165–199. [78] Henares, B.M., Higgins, K.E., Boon, E.M., 2012. Discovery of a nitric oxide responsive quorum sensing circuit in Vibrio harveyi. ACS Chem. Biol., 7, 1331–1336. [79] Henares, B.M., Xu, Y., Boon, E.M., 2013. A nitric oxideresponsive quorum sensing circuit in Vibrio harveyi regulates flagella production and biofilm formation. Int. J. Mol. Sci., 14, 16473–16484. [80] Krapp, A.R., Humbert, M.V., Carrillo, N., 2011. The soxRS response of Escherichia coli can be induced in the absence of oxidative stress and oxygen by modulation of NADPH content. Microbiology, 157, 957–965. [81] Spiro, S., 2006. Nitric oxide-sensing mechanisms in Escherichia coli. Biochem. Soc. Trans., 34, 200–202. [82] Ding, H., Demple, B., 2000. Direct nitric oxide signal transduction via nitrosylation of iron–sulfur centers in the SoxR transcription activator. Proc. Natl. Acad. Sci. USA, 97, 5146–5150. [83] Cruz-Ramos, H., Crack, J., Wu, G., Hughes, M.N. et al., 2002. NO sensing by FNR: regulation of the Escherichia coli NOdetoxifying flavohaemoglobin, Hmp. EMBO J., 21, 3235–3244.
ß 2014 WILEY-VCH Verlag GmbH & Co. KGaA,Weinheim
11
[84] Poole, R.K., 2008. Microbial haemoglobins: proteins at the crossroads of oxygen and nitric oxide metabolism, in: Bolognesi, M., di Prisco, G., Verde, C. (Eds.), Dioxygen Binding and Sensing Proteins, a Tribute to Beatrice and Jonathan Wittenberg, Springer-Verlag, Milan, 241–257. [85] Stevanin, T.M., Read, R.C., Poole, R.K., 2007. The hmp gene encoding the NO-inducible flavohaemoglobin in Escherichia coli confers a protective advantage in resisting killing within macrophages, but not in vitro: links with swarming motility. Gene, 398, 62–68. [86] Barrios, H., Valderrama, B., Morett, E., 1999. Compilation and analysis of sigma (54)-dependent promoter sequences. Nucleic Acids Res., 27, 4305–4313. [87] Studholme, D.J., Dixon, R., 2003. Domain architectures of sigma (54)-dependent transcriptional activators. J. Bacteriol., 185, 1757–1767. [88] D’Autréaux, B., Tucker, N.P., Dixon, R., Spiro, S., 2005. A non-haem iron centre in the transcription factor NorR senses nitric oxide. Nature, 437, 769–772. [89] Luyten, E., Swinnen, E., Vlassak, K., Verreth, C. et al., 2001. Analysis of a symbiosis-specific cytochrome P450 homolog in Rhizobium sp. BR816. Mol. Plant Microbe Interact., 14, 918–924. [90] Valderrama, B., Dávalos, A., Girard, L., Morett, E., Mora, J., 1996. Regulatory proteins and cis-acting elements involved in the transcriptional control of Rhizobium etli reiterated nifH genes. J. Bacteriol., 178, 3119–3126. [91] Michiels, J., D’Hooghe, I., Verreth, C., Pelemans, H., Vanderleyden, J., 1994. Characterization of the Rhizobium leguminosarum biovar phaseoli nifA gene, a positive regulator of nif gene expression. Arch. Microbiol., 161, 404–408. [92] Lambrecht, M., Vande Broek, A., Dosselaere, F., Vanderleyden, J., 1999. The ipdC promoter auxin-responsive element of Azospirillum brasilense, a prokaryotic ancestral form of the plant AuxRE? Mol. Microbiol., 32, 889–891. [93] Pullan, S.T., Gidley, M.D., Jones, R.A., Barrett, J. et al., 2007. Nitric oxide in chemostat-cultured Escherichia coli is sensed by Fnr and other global regulators: unaltered methionine biosynthesis indicates lack of S-nitrosation. J. Bacteriol., 189, 1845–1855.
www.jbm-journal.com
J. Basic Microbiol. 2014, 54, 1–11
