Skip to content
naulon
Get started

No retraction, correction or concern found when last checked on Oct 16, 2026.

Plant growth-promoting rhizobacteria and root system functioning

Jordan Vacheron, Guilhem Desbrosses, Marie-Lara Bouffaud and 6 more

Frontiers in Plant Science · 2013 · Review

doi:10.3389/fpls.2013.00356

Abstract

The rhizosphere supports the development and activity of a huge and diversified microbial community, including microorganisms capable to promote plant growth. Among the latter, plant growth-promoting rhizobacteria (PGPR) colonize roots of monocots and dicots, and enhance plant growth by direct and indirect mechanisms. Modification of root system architecture by PGPR implicates the production of phytohormones and other signals that lead, mostly, to enhanced lateral root branching and development of root hairs. PGPR also modify root functioning, improve plant nutrition and influence the physiology of the whole plant. Recent results provided first clues as to how PGPR signals could trigger these plant responses. Whether local and/or systemic, the plant molecular pathways involved remain often unknown. From an ecological point of view, it emerged that PGPR form coherent functional groups, whose rhizosphere ecology is influenced by a myriad of abiotic and biotic factors in natural and agricultural soils, and these factors can in turn modulate PGPR effects on roots. In this paper, we address novel knowledge and gaps on PGPR modes of action and signals, and highlight recent progress on the links between plant morphological and physiological effects induced by PGPR. We also show the importance of taking into account the size, diversity, and gene expression patterns of PGPR assemblages in the rhizosphere to better understand their impact on plant growth and functioning. Integrating mechanistic and ecological knowledge on PGPR populations in soil will be a prerequisite to develop novel management strategies for sustainable agriculture.

Full text

From PubMed Central, U.S. National Library of Medicine, as current on Oct 16, 2026. Paragraph numbers are ours, so an answer can point at one.

INTRODUCTION

Photosynthetic terrestrial plants play key roles as ecosystem engineers. They contribute, for instance, to the establishment of specific microbial ecological niches in plant-based systems. This is particularly the case in the rhizosphere, i.e., the soil in contact with plant roots. Besides its role in plant anchorage in soil, absorption of water and ions, nutrient storage, and plant vegetative growth, the root system is in close contact with a wide range of soil microbial populations.

Despite their interactions with the biotic environment, the root system and its rhizosphere have received much less attention by plant physiologists than the rest of the plant. Plant roots exude a huge diversity of organic nutrients (organic acids, phytosiderophores, sugars, vitamins, amino acids, nucleosides, mucilage) and signals that attract microbial populations, especially those able to metabolize plant-exuded compounds and proliferate in this microbial habitat. Root exudates being the largest source of carbon supply within soil, the rhizosphere compartment houses a rich microbial community, comprising up to 1010 bacteria per gram of soil and encompassing a large diversity of taxa. The corresponding microbial community associated to plant roots can be referred to as the rhizo-microbiome. Its composition is distinct from that of the microbial community of the surrounding soil, a direct consequence of bacterial competition for nutrients liberated in the vicinity of plant roots. Since root exudate composition changes along the root system, according to stages of plant development and to plant genotypes, the rhizo-microbiome composition differs accordingly. Plant-driven selection of bacteria is an important issue recently discussed in several reviews.

Within the rhizo-microbiome, some microorganisms can promote plant growth and provide better plant health through several indirect or direct mechanisms. Beneficial plant-microbe interactions are symbiotic interactions in which costs and benefits are shared by the plants and the microorganisms and can be categorized into two main types of interactions. First, mutualistic interactions correspond to intimate and mostly obligate interactions between microbes and a restricted range of compatible host plants. They generally lead to the formation of a structure specifically dedicated to the interaction (e.g., nodules during the symbiosis between nodulating rhizobia and Fabaceae, arbuscules in the endomycorrhizal symbiosis;; ). Second, cooperations (also called associative symbioses) correspond to less obligate and specific interactions. They involve soil bacteria able to colonize the surface of the root system (and sometimes root inner tissues) and to stimulate the growth and health of the plant, and are referred to as plant growth-promoting rhizobacteria (PGPR; ). Colonization of plant host roots by PGPR is heterogeneous along the root system; their competitiveness regarding this process is a sine qua non for plant growth promotion (discussed in;;; ). In comparison to mutualistic symbionts, PGPR are thought to interact with a large range of host plant species and to encompass a huge taxonomic diversity, especially within the Firmicutes and Proteobacteria phyla. PGPR can enhance plant nutrition via associative nitrogen fixation, phosphate solubilization, or phytosiderophore production. They can improve root development and growth through the production of phytohormones or enzymatic activities, as well as favor the establishment of rhizobial or mycorrhizal symbioses. Others can protect the plant through inhibition of phytoparasites, based on antagonism or competition mechanisms, and/or by eliciting plant defenses such as induced systemic resistance (ISR;; ). Some PGPR can also help plants withstand abiotic stresses including contamination by heavy metals or other pollutants; certain are even able to increase the capacity of plants to sequester heavy metals. Therefore, utilizing PGPR is a new and promising approach for improving the success of phytoremediation of contaminated soils (for recent reviews see;; ).

Understanding and quantifying the impact of PGPR on roots and the whole plant remain challenging. One strategy is to inoculate roots with a PGPR in vitro and monitor the resulting effects on plant. This showed that many PGPR may reduce the growth rate of the primary root, increase the number and/or length of lateral roots, and stimulate root hair elongation in vitro. Consequently, the uptake of minerals and water, and thus the growth of the whole plant, can be increased. Some of these effects, including increased root and shoot biomass, are also documented for PGPR-inoculated plants growing in soil.

The focus of this paper is to review the main modes of action of PGPR strains, the functioning of PGPR populations, and their ecology in the rhizosphere. Description of plant-beneficial properties of PGPR has been the focus of several reviews (e.g.,;; ), but without integrating actual PGPR gene expression on roots, the interactions between different PGPR populations in the rhizosphere, or the resulting plant-beneficial effects. This paper is organized into four sections. In the first section, we present the molecular mechanisms through which PGPR may affect the architecture of the root system and interfere with the plant hormonal pathways, and review our current understanding of their impact on the structural properties of the roots. In the second section, recent findings related to the impact of PGPR on the physiology of the whole plant are presented, with a focus on plant nutrient acquisition, plant transcriptome and plant metabolome. The third section shows how expression of plant-beneficial properties can be affected within the rhizosphere by molecules emitted by other microbial populations or by the plant. As PGPR strains are not acting individually in the rhizosphere, the ecology of PGPR populations and notably the complexity of the interactions taking place between PGPR populations is discussed in the fourth section. Finally, we conclude on the importance of integrating molecular investigations on the modes of action and ecology of PGPR strains with high-throughput analyses on the abundance, taxonomic/functional diversity and activity of rhizosphere microbial communities, and with the monitoring of plant molecular responses.

IMPACT OF PGPR ON ROOT SYSTEM ARCHITECTURE AND ROOT STRUCTURE

Most terrestrial plants develop their root system to explore soil and find nutrients to sustain growth. Root is a complex organ made of distinct regions such as the root tip, root meristem, differentiation and elongation zones, and emerging lateral roots. These regions have distinct roles. For instance, root hairs are differentiated epidermal cells important for plant mineral nutrition, as inferred from gene expression studies and nutrient accumulation measurements. Root functional specificity is also reflected at the level of plant-microbe interactions. In Fabaceae for example, the root tip is the most important region to initiate the rhizobial colonization process leading eventually to the formation of a root nodule. In Poaceae, root hairs and lateral roots are preferentially colonized by PGPR, where they may express their plant beneficial properties. Root system architecture (RSA) integrates root system topology, the spatial distribution of primary and lateral roots, and the number and length of various types of roots. Several abiotic and biotic factors can influence RSA, including PGPR strains. PGPR modify RSA and the structure of root tissues mainly through their ability to interfere with the plant hormonal balance (Figure 1).

PGPR EFFECTS ON RSA VIA MODULATION OF HOST HORMONAL BALANCE

Changes in RSA may result from interferences of PGPR with the main hormonal pathways involved in regulating plant root development: auxin, cytokinin, ethylene, and to a lesser extend gibberellin, and abscisic acid (ABA). The balance between auxin and cytokinin is a key regulator of plant organogenesis, and shapes root architecture. The auxin to cytokinin ratio can be affected by PGPR because they are able to produce a wide range of phytohormones, including auxins and/or cytokinins, and secondary metabolites that can interfere with these hormonal pathways.

Many PGPR are able to produce phytohormones and secondary metabolites interfering with the plant auxin pathway, such as auxins, 2,4-diacetylphloroglucinol (DAPG), and nitric oxide (NO). Indole-3-acetic acid (IAA) is the best-characterized auxin produced by many plant-associated bacteria, including PGPR. Exogenous IAA controls a wide variety of processes in plant development and plant growth: low concentrations of IAA can stimulate primary root elongation, whereas high IAA levels stimulate the formation of lateral roots, decrease primary root length and increase root hair formation (Figure 1;;;;; ). IAA is usually synthesized by rhizobacteria from tryptophan, which is found at different concentrations in root exudates according to plant genotype. In PGPR strains, several IAA biosynthetic pathways have been described depending on the metabolic intermediates. The indole-3-pyruvate decarboxylase (encoded by the ipdC/ppdC bacterial gene) is a key enzyme involved in the indolepyruvic acid pathway. Effects of ipdC mutants on plant root morphology are often altered in comparison to those of wild-type strains.

Plant growth promotion by PGPR can also result from indirect stimulation of the plant auxin pathway. For example, several PGPR strains like Azospirillum brasilense have a nitrite reductase activity and consequently are able to produce NO during root colonization. NO is involved in the auxin signaling pathway controlling lateral root formation. DAPG is a well-known antimicrobial compound produced by biocontrol fluorescent pseudomonads. At lower concentrations, DAPG can also be a signal molecule for plants, inducing systemic resistance, stimulating root exudation, and enhancing root branching. DAPG can interfere with an auxin-dependent signaling pathway and thus modify RSA. Indeed, applications of exogenous DAPG, at a concentration around 10 μM, inhibited primary root growth and stimulated lateral root production in tomato seedlings. Furthermore, roots of an auxin-resistant diageotropica mutant of tomato displayed reduced DAPG sensitivity.

The growth-promotion effect of auxin or auxin-like compounds by PGPR may require functional signaling pathways in the host plant. To test that hypothesis, one could use a host plant defective at a particular step of the hormone-signaling pathway and assess whether PGPR inoculation complements or not the effect of the mutation. This strategy requires the use of model plant such as Arabidopsis, the only biological system that provides to date enough documented mutant plants. Consistent with that, some Arabidopsis auxin-signaling mutants failed to show the typical root architecture changes in response to the beneficial rhizobacterium Phyllobacterium brassicacearum STM196. However, auxin content was not increased in roots upon inoculation with Phyllobacterium brassicacearum STM196, ruling out the potential implication of auxin of bacterial origin. Nevertheless, the use of Arabidopsis DR5::GUS reporter line, whose expression is restricted to the root meristem where the auxin maximum is located, showed a change of expression pattern in response to STM196 inoculation (Figure 2). GUS staining appeared more intense on a wider region of the root tip as well as in the vasculature, suggesting that there was a change of auxin distribution in the root in response to STM196 inoculation, even though this strain is a low auxin producer. Interestingly, a similar observation was made when Arabidopsis plantlets were inoculated with the PGPR Bacillus subtilis GB03, which emits volatile organic compounds (VOCs), or with Pseudomonas fluorescens WCS417.

Cytokinin production (especially zeatin) has been documented in various PGPR like Arthrobacter giacomelloi, Azospirillum brasilense, Bradyrhizobium japonicum, Bacillus licheniformis, Pseudomonas fluorescens, and Paenibacillus polymyxa. Cytokinins stimulate plant cell division, control root meristem differentiation, induce proliferation of root hairs, but inhibit lateral root formation and primary root elongation. Inoculation of plants with bacteria producing cytokinin has been shown to stimulate shoot growth and reduce the root to shoot ratio. Bacterial genes involved in cytokinin biosynthetic pathways have been identified in silico but their role has not yet been validated through functional analyses. Consequently, the contribution of cytokinin production by PGPR to RSA modifications remains speculative.

Ethylene is another key phytohormone, which inhibits root elongation and auxin transport, promotes senescence and abscission of various organs, and leads to fruit ripening. Ethylene is also involved in plant defense pathways. This phytohormone can be produced in small amounts from the precursor methionine by some PGPR, like Azospirillum brasilense. The ability of Azospirillum brasilense to produce ethylene presumably promotes root hair development in tomato plants. Indeed, exogenous ethylene supply to the plant mimicked the effect of Azospirillum brasilense inoculation, while the addition of an ethylene biosynthesis inhibitor blocked this effect. Actually, PGPR are more widely able to lower plant ethylene levels through deamination of 1-aminocyclopropane-1-carboxylic acid (ACC). Many genomes of PGPR do contain a gene (acdS) coding for an ACC deaminase, which degrades ACC into ammonium and α-ketobutyrate. By lowering the abundance of the ethylene precursor ACC, the PGPR AcdS activity is thought to decrease root ethylene production, which can in turn alleviate the repressing effect of ethylene on root growth. Despite being widely accepted and supported by experimental data, the model raises issues that have not been well addressed yet. The first one deals with ethylene production within roots. Light is promoting ethylene biosynthesis, providing there is a sufficient CO2 supply for shoots. Exposition of roots to light was shown to trigger an increase in ethylene production. In soil however, roots are sheltered from light, suggesting that this organ might not be able to synthesize large amounts of ethylene. In agreement with that, Fabaceae roots did produce ethylene in response to rhizobial colonization in presence of light, but less when they were in the dark. Secondly, there is a regulation of ethylene synthesis by a feedback loop. This loop should stimulate ethylene biosynthesis when the level of ACC is low. Unless PGPR disconnect that feedback loop, lowering ACC content would eventually result in stimulation of ethylene production. There is no indication yet how the feedback loop would work in presence of a PGPR. Last but not least, if ethylene plays a key role during the plant-PGPR interaction, one would expect that either plant ethylene mutants or impaired AcdS activity in the bacteria would result in clear disturbance of the plant responses to bacteria. However, minor effects on RSA were observed when plants were inoculated with an acdS bacterial mutant, or when plants affected in their ethylene signaling pathway were inoculated with wild-type PGPR. It suggests that ethylene participates to the root architecture response but is not a key player. Taken together, the functional importance of the bacterial ACC deaminase function needs further clarification. One hypothesis could be that AcdS contributes to the fine-tuning of ethylene biosynthesis during the plant-PGPR cooperation.

Several reports have revealed that PGPR are able to produce ABA or gibberellic acid, or to control the level of these hormones in plants. The first one, ABA, is well known for its involvement in drought stress. During water stress, increase in ABA levels causes closing of stomata, thereby limiting water loss. However, this hormone also plays different roles during lateral root development. Inoculation with Azospirillum brasilense Sp245 led to an increase of ABA content in Arabidopsis, especially when grown under osmotic stress. Gibberellins promote primary root elongation and lateral root extension. Production of gibberellins has been documented in several PGPR belonging to Achromobacter xylosoxidans, Acinetobacter calcoaceticus, Azospirillum spp., Azotobacter spp., Bacillus spp., Herbaspirillum seropedicae, Gluconobacter diazotrophicus and rhizobia. Application of gibberellic acid on maize, at a concentration similar to that produced by Azospirillum, promotes root growth; furthermore, gibberellin content increases in maize root inoculated with Azospirillum. In addition to playing a role in plant RSA, these two hormones are involved in plant defense mechanisms. Thus, PGPR producing these hormones may modulate the hormonal balance involved in plant defense, including the jasmonate and salicylic acid pathways (for a review see ).

Although the production of hormones by PGPR has been well described, the genetic determinants involved in their biosynthesis remain largely unknown and bacterial mutants affected in hormone biosynthesis are mostly lacking. Consequently, the involvement of hormones of bacterial origin in the modulation of plant hormonal balance has not been fully demonstrated.

MODIFICATION OF ROOT CELL WALL AND ROOT TISSUE STRUCTURAL PROPERTIES BY PGPR

Many PGPR can lead to modifications of the chemical composition and therefore structural properties of root cell walls (Figure 1;; ). For example, the biocontrol agent Bacillus pumilus INR-7 is able to enhance lignin deposition in pearl millet epidermal tissues, and this plant defense response appears much more rapidly in PGPR-primed plants infected by the pathogen Sclerospora graminicola compared to non-primed plants. The sole inoculation of INR-7 led to callose apposition. Although the precise location of these deposited polymers was not investigated, it is possible that their enhanced accumulation may participate to pathogen inhibition and disease suppression. A similar response was also triggered by Bacillus pumilus SE34 and Bacillus subtilis UMAF6639 when inoculated to respectively pea and melon roots. In both cases, it led to enhanced fungal pathogen tolerance. Inoculation of Pseudomonas fluorescens 63-28R to pea roots induced accumulation of lignin in root cells and inhibited colonization by the oomycete Pythium ultimum. The same result was observed with a Pseudomonas putida strain inoculated on bean roots. These cell wall modifications have been reported in the case of PGPR that protect plants against phytopathogens by activating ISR plant defense responses. One of the consequences of ISR is thus the reinforcement of the cell wall through enhanced lignin synthesis and callose apposition, which restricts the progression of phytopathogens through plant tissues.

Modifications of the chemical composition of root cell walls are also triggered by PGPR that directly promote plant growth (Figure 1). Through the analysis of the infrared spectral characteristics of crude cell wall preparations of maize roots, concluded that roots inoculated with Azospirillum lipoferum CRT1 had lower lignin content than uninoculated ones. This result contrasts with those aforementioned for biocontrol agents. Nevertheless, lower lignin content may facilitate cell elongation, and therefore overall root elongation. Similarly, Azospirillum irakense produces pectate lyases that are capable of degrading the pectate content of root cell wall and might allow its progression between root cortex cells and its functioning as an endophyte. Up to now, the impact on plant lignin content of PGPR that are both inducing ISR and promoting root growth has not been clarified.

Modifications of root cell wall ultrastructure are thought to result mainly from PGPR-triggered changes in plant gene expression. Indeed, Bacillus subtilis GB03 promotes Arabidopsis growth by producing VOCs that were shown to modulate the expression of 38 genes with known functions associated with cell wall structure. Among them, 30 were implicated in cell wall expansion or loosening. The endophytic PGPR Azospirillum irakense was also shown to stimulate the expression of polygalacturonase genes in inoculated rice roots.

Chemical mediators involved in the effects of PGPR on root cell walls have received little attention. A single report has indicated that the exogenous addition of auxins enhanced the induced polygalacturonase activities observed in Azospirillum irakense inoculated rice roots.

SYSTEMIC EFFECTS OF PGPR ON WHOLE PLANT PHYSIOLOGY AND FUNCTIONING

In addition to their effects on root tissues, PGPR can modify the physiology and functioning of plant tissues located at a substantial distance from the colonized sites, such as shoots. Two types of mechanisms are involved. On the one hand, some PGPR can enhance nutrient availability/uptake for plant roots. Stimulation of plant nutrition will lead to modifications in primary metabolism and consequently will contribute to enhance growth. On the other hand, certain PGPR trigger specific systemic responses, mostly by unknown signaling mechanisms. High-throughput analyses of plant transcriptomic and metabolomic responses have evidenced the effects of PGPR on plant gene expression and metabolite accumulation, respectively. These results highlight the extensive effect of PGPR on whole plant physiology and functioning (Figure 1), and provide clues to understand the systemic effect of PGPR.

IMPACT OF PGPR ON PLANT NUTRITION

The impact of PGPR on plant nutrition may result from effects on plant nutrient uptake and/or on plant growth rate. It is indeed commonly hypothesized that nutrient uptake is increased as a consequence of increased root surface area triggered by PGPR. However, root ion transporters are under the control of regulatory processes that adjust their activity to the plant nutritional demand, so that regulations of root development and ion transporter activities are antagonistically coordinated to maintain steady nutrient acquisition rate. Hence, PGPR must interfere with pathways coordinating plant development and plant nutrition to elicit both increased nutrient acquisition rate and plant growth promotion (Figure 1).

Plant growth-promoting rhizobacteria can directly increase nutrient supply in the rhizosphere and/or stimulate ion transport systems in root. With regards to increased nutrient supply, two main types of bacterial activities can be considered. Firstly, phosphate solubilization is one key effect of PGPR on plant nutrition. Soils generally contain a large amount of phosphorus, which accumulates in the wake of regular fertilizer applications, but only a small proportion of the latter is available for plants. Plants are able to absorb on their own mono and dibasic phosphate; organic or insoluble forms of phosphate need to be mineralized or solubilized by microorganisms, respectively. Many PGPR – such as Pseudomonas, Bacillus, Rhizobium – are able to dissolve insoluble forms of phosphate (for a review see ). Two main processes exist: acidification of the external medium through the release of low molecular weight organic acids (such as gluconic acid) that chelate the cations bound to phosphate, and production of phosphatases/phytases that hydrolyse organic forms of phosphate compounds. Secondly, many associated bacteria can fix N2 so that they could provide nitrogen to the plant. Evidence in favor of the participation of PGPR to the plant N budget has been reported for several plants, especially sugar cane. However, the impact of N2-fixation by PGPR is still debated and is rarely credited for the stimulation of plant growth (for review see ). In addition, non-fixing rhizobacteria can promote plant growth, showing that N provision is not obligatory for plant growth promotion. For instance, Phyllobacterium brassicacearum STM196 is unlikely to fix N2 while it promotes the growth of canola and Arabidopsis.

With regards to the impact of PGPR on nutrient uptake systems, only very few studies have been published so far. Inoculation of canola with Achromobacter sp. strain U80417 resulted in an increase of both and K+ net influx rates per root surface area unit. In this study, the net H+ efflux was also enhanced, so that increased and K+ uptake rates may be part of a general mechanism leading to increased ion uptake rate, similar to energization of nutrient transport by enhanced proton pump activity. In favor of this hypothesis, acidification of the rhizosphere has also been reported with Arabidopsis exposed to the VOC-emitting Bacillus subtilis strain GB03.

In Arabidopsis, uptake measurement in response to PGPR, over time, can lead to contradictory results: influx was increased in seedlings, upon 24 h-inoculation with Phyllobacterium brassicacearum STM196, while it was reduced 7 days later. However, it is hard to draw a firm conclusion as the net uptake rate remained unknown since ion efflux was not measured in these experiments. Except for the NRT2.5 and NRT2.6 genes, the accumulation of transcripts of nitrate and ammonium transporters was very slightly or not significantly changed upon Phyllobacterium brassicacearum STM196 inoculation. Interestingly, these two genes have recently been shown to be required in Arabidopsis growth promotion by this PGPR. Since these two genes code for two plasma membrane-localized transporters, this discovery raises the question of the interactions between N nutrition and plant development in PGPR-inoculated plants. The NRT2.5 and NRT2.6 genes are predominantly expressed in shoots. Their role in Phyllobacterium brassicacearum STM196 plant growth promotion and/or root architecture modification are not linked to changes in uptake rate or distribution between roots and shoots, suggesting an involvement in N-signaling rather than a direct role in N-metabolism.

Evidence in favor of a regulation of ion transporters at a transcriptional level by PGPR has been obtained in studies with Bacillus subtilis GB03. This strain induces concomitant down- and up-regulation of HKT1 expression in roots and shoots of Arabidopsis seedlings, respectively. In the shoots, HKT1 functions in phloem tissues to retrieve Na+ from the xylem and in the roots it is involved in Na+ uptake. The differential regulation of HKT1 expression in roots and shoots resulted in reduced accumulation of Na+ and increased accumulation of K+ in both organs of GB03-inoculated seedlings under salt-stress conditions. Consistent with the effect of GB03 on HKT1, GB03 failed to rescue salt-stressed hkt1 mutant seedlings from elevated Na+ accumulation.

Volatile organic compounds emitted by GB03 also activate the plant’s iron acquisition machinery leading to increased iron assimilation. Firstly, this PGPR leads to acidification of the rhizosphere, both directly due to chemical effects of some unidentified VOCs and indirectly through increased root proton efflux. Secondly, GB03 up-regulates the expression levels of FRO2 and IRT1 genes, coding respectively for a Fe3+ chelate reductase and a Fe2+ transporter. As a result, GB03-exposed Arabidopsis has enhanced ferric chelate reductase activity and increased iron content. Finally, it has been shown that this PGPR induces the expression of the FIT1 transcription factor that regulates positively FRO2 and IRT1 expressions. The fact that GB03 fails to increase root ferric reductase activity and plant iron content in Arabidopsis fit1 mutants shows that PGPR can modify indirectly ion uptake by interfering with plant regulatory processes that control ion transporter expressions and/or activities.

IMPACT OF PGPR ON PLANT TRANSCRIPTOME

Targeted or genome-wide analyses of plant gene expression following root inoculation by PGPR were reported with various bacterial models: phytostimulating PGPR, endophytes and PGPR exerting a biocontrol activity. Inoculation of the phytostimulator Pseudomonas putida MTCC5279 triggered overexpression of 520 genes and repression of 364 genes (threefold changes) in leaves of Arabidopsis; upregulated genes were involved in maintenance of genome integrity, growth hormone and amino acid syntheses, ABA signaling and ethylene suppression, Ca2+ dependent signaling and induction of ISR. On rice, a recent study performed with Azospirillum points towards association specificity. The targeted expression of ethylene receptors was followed after inoculation of Azospirillum brasilense Sp245 on two rice cultivars of contrasted ability to gain nitrogen from biological nitrogen fixation. Seedlings of cultivar IR42, which enabled higher nitrogen fixation, also displayed higher expression of ethylene receptors compared to cultivar IAC 4440. The transcript accumulation of all ethylene receptors might be necessary for the establishment of a beneficial association between the plant and the bacteria.

As for endophytes, differential colonization of rice roots was observed with an Azoarcus PGPR. In a less compatible interaction, a slight defense response occurred and was accompanied by the induction of pathogenesis-related proteins and proteins sharing domains with receptor-like kinases induced by pathogens; those proteins were also induced by a jasmonate treatment. Inoculation of rice roots with the endophytic PGPR Herbaspirillum seropedicae triggered the expression of genes responsive to auxin and ethylene and the repression of the defense-related proteins PBZ1 and thionins. These studies suggest that endophytes modulate plant defense responses during colonization.

Plants treated with biocontrol PGPR, usually belonging to the Pseudomonas genus, are more resistant to subsequent infections by bacterial or fungal pathogens. In Arabidopsis, this rhizobacteria-mediated ISR requires sensitivity to jasmonate and ethylene, and the regulators MYC2, NPR1, and MYB72 played a central role in this signaling. One of the earliest transcriptomic study performed with Pseudomonas fluorescens WCS417r indicated that bacteria elicited a substantial change in the expression of 97 genes in roots whereas none of the approximately 8,000 genes tested showed a consistent change in expression in the leaves. Subsequent studies on Arabidopsis reported an increase of defense-related transcripts, including PR-related proteins, in shoots of bacterized plants compared to untreated shoots. Interestingly, the ISR induced by Pseudomonas fluorescens SS101 was recently reported to be dependent on salicylic acid signaling and not on jasmonic acid and ethylene signaling; moreover, a prominent role of camalexin and glucosinolates in the ISR was proposed. In wheat, bacterization with Pseudomonas fluorescens Q8r1-96 also triggered the accumulation of defense-related transcripts and neither DAPG nor the type three secretion system were key single factors in the expression of these genes. The establishment of beneficial associations requires mutual recognition and substantial coordination of plant and microbial responses and consequently beneficial microbes modulate plant immunity.

IMPACT OF PGPR ON PLANT METABOLOME

Several studies have addressed the metabolomic changes triggered by PGPR inoculation, by analyzing metabolite contents of root exudates, root tissues and shoots under normal or stressful conditions (Figure 1). Some studies have shown that PGPR can elicit changes in the activities of root enzymes involved in the production of metabolites, especially flavonoids, leading to changes in the pattern of root exudation. Some Azospirillum PGPR stimulated by up to one-third the level of carbon compounds exuded from roots. Moreover, compounds of microbial origin, such as phenazines and DAPG, could enhance total net efflux of amino acids in plant species. On soybean roots, the PGPR Chryseobacterium balustinum Aur9 influences flavonoids exudation. PGPR strains from Chryseobacterium or Azospirillum may influence flavonoid exudation by Fabacea roots. This property can be important for the design of mixed inoculants that will include a PGPR strain promoting flavonoid exudation together with rhizobia that will respond to plant flavonoids.

In addition to effects on root exudates, PGPR can trigger modifications of metabolite composition of the whole plant. For instance, rice plants inoculated with Herbaspirillum seropedicae showed higher shoot contents in malate and in key amino acids than those of control plants. Many more studies focused on modifications of secondary metabolites. Elicitation of isoflavone accumulation was observed on soybean inoculated with various PGPR, either by increasing the total isoflavone content in seedlings or by causing an asymmetric distribution of isoflavones throughout the plant. Increase in the content of several alkaloid and terpenoid compounds of pharmaceutical relevance was demonstrated in medicinal plants following PGPR inoculation. Recent studies investigated the early impact of several Azospirillum strains on root and shoot secondary metabolite profiles of maize and rice; analysis of secondary metabolites of two maize cultivars, inoculated by three different Azospirillum strains under greenhouse conditions, revealed major qualitative and quantitative modifications of the contents of secondary metabolites, especially benzoxazinoids. In the same way, a metabolic profiling approach of two rice cultivars inoculated with two different Azospirillum strains under gnotobiotic conditions, showed that profiles of secondary metabolites were modified with phenolic compounds such as flavonoids and hydroxycinnamic derivatives being the main metabolites affected. Both studies evidenced a specific response, as plant metabolic changes differed according to the Azospirillum strain-cultivar combination. Moreover, PGPR applied to the roots can affect the composition of secondary metabolites in shoots, pointing towards systemic effects.

Accumulation of secondary compounds was also modified in several plants inoculated with consortia containing arbuscular mycorrhizal fungus and PGPR. Blumenin accumulation triggered by Rhizophagus irregularis (formerly Glomus intraradices) in barley and wheat roots was increased when a rhizosphere bacterium was applied with the fungus. Leaf secondary metabolites (total phenols and ortho dihydroxy phenols), as well as leaf mineral content (phosphorus, potassium, zinc, copper, and iron) were maximal when Begonia malabarica or Solanum viarum were inoculated with consortia containing two fungi and a Bacillus coagulans strain. Field-inoculation of maize with selected strains of Pseudomonas, Azospirillum or Rhizophagus/Glomus, or with these strains combined two by two or all three together, led to qualitative and quantitative modifications of root secondary metabolites, particularly benzoxazinoids and diethylphthalate. These modifications depended on fertilization level and on the type of microorganisms inoculated. The three selected strains gave distinct results when used alone, but unexpectedly all microbial consortia gave somewhat similar metabolic responses.

Plant growth-promoting rhizobacteria can help plants to withstand saline stress, a feature that may be linked to accumulation of specific metabolites. A higher level of proline content was reported in inoculated Bacopa monnieri, as well as higher accumulation of glycine betaine-like quaternary compounds in rice inoculated with Pseudomonas pseudoalcaligenes. Similarly, Arabidopsis inoculation with the VOC-emitting strain Bacillus subtilis GB03 induced strong plant accumulation of glycine betaine and its precursor choline, and GB03-induced drought tolerance was lost in the xipotl mutant of Arabidopsis with reduced choline production. Alleviation of cold stress was demonstrated for Burkholderia phytofirmans PsJN on grapevine; this endophytic strain promotes plant post-chilling recovery by improving acclimation to cold. This is accompanied by accumulation of stress-related metabolites such as proline, malondialdehyde and aldehydes (known as lipid peroxidation markers), hydrogen peroxide, and by higher expression of defense- and cold-related genes. Bacterization resulted in a 1.2-fold increase in starch content and in a two-fold increase in total soluble sugars, with sugars known to be involved in low-temperature tolerance (glucose, sucrose, and raffinose) displaying higher concentrations in treated plantlets. Independently of temperature, inoculation also enhanced phenolic content.

EXPRESSION OF PLANT-BENEFICIAL FUNCTIONS OF PGPR IN THE RHIZOSPHERE

One PGPR strain can harbor several plant-beneficial properties, which may be co-regulated or not. Within the rhizosphere, the expression of PGPR’s plant-beneficial properties is affected by both abiotic factors (like pH, oxygen, clay mineralogy, heavy metals, etc.) and biotic factors (i.e., compounds produced by plants or the rhizo-microbiome) that can lead to distinct expression patterns in space and time, possibly with different effects on host plant. In this section, a focus is put on the regulation of the expression of PGPR plant-beneficial properties by biotic factors occurring in the rhizosphere.

REGULATION OF PGPR FUNCTIONS BY ROOT EXUDATES

Through the release of root exudates, plants can impact bacterial gene expression, especially genes encoding plant-beneficial traits. Composition of root exudates is dependent upon intra and inter-specific genetic variability, plant developmental stage and soil abiotic factors. One of the major studies aiming at analyzing the impact of root exudates variability on bacterial gene expression was carried out on phlA, involved in DAPG biosynthesis, in Pseudomonas protegens (formely Pseudomonas fluorescens) CHA0. The expression of phlA was increased fourfold in the rhizosphere of monocots (maize and wheat) compared to the rhizosphere of dicots (bean and cucumber). The analysis of six maize cultivars also revealed that phl expression and hence biocontrol activity could be affected by plant genotype. Specific components of root exudates, notably sugars, were shown to affect the production of antimicrobial compounds, such as DAPG, pyoluteorin and pyrrolnitrin by fluorescent pseudomonads, with some strain-dependent effects. Among 63 plant compounds related to defense or development, or involved in plant-microbe interactions (flavonoids, phenolic acids, phytohormones, etc.), many could modulate the expression of phlA and pltA in Pseudomonas protegens CHA0. No specific chemical structures were identified that generally induced or repressed phlA or pltA expression. Umbelliferone led to the strongest inhibition of phlA; salicylate, jasmonate, and methyl jasmonate, all slightly reduced phlA expression, whereas the plant hormone IAA induced phlA expression. None of these compounds had an effect on pltA expression whereas a previous study reported repression of both DAPG and pyoluteorin biosynthesis genes by salicylate.

1-Aminocyclopropane-1-carboxylic acid deamination (encoded by acdS) is another bacterial function that may be differentially expressed according to plant genotypes. Indeed, in vitro experiments demonstrated that some compounds present in root exudates tightly control acdS expression. First, ACC, the precursor of ethylene that is metabolized by AcdS, can positively regulate acdS expression. Second, leucine, by inhibiting oligomerization of the Lrp-type regulator AcdR, prevents transcription of acdS leading to a decrease of ACC deaminase activity in Pseudomonas putida UW4 and in Azospirillum lipoferum 4B. Finally, carbon sources can also influence acdS transcription.

As presented above, bacterial IAA biosynthesis mostly depends on tryptophan-related pathways. The main source of tryptophan for PGPR is root exudates. Measurement of tryptophan bioavailability from graminaceous roots (Avena barbata) indicated that this amino acid is abundant at the emergence of secondary roots. In the absence of exogenous tryptophan supply, bacterial IAA biosynthesis is insignificant. Next to being an IAA precursor, tryptophan also plays an important role in regulating positively the ipdC/ppdC gene. Other root-exuded amino acids like tyrosine and phenylalanine can also induce ipdC/ppdC expression. Besides amino acids, plant roots release compounds like vitamins (e.g., pyridoxine and nicotinic acid) and organic acids (e.g., phenylacetic acid and prephenic acid; ). All these compounds increase significantly IAA production in Azospirillum brasilense Sp245.

Metabolites present in root exudates can thus specifically modulate the expression of key genes involved in plant-beneficial functions. Consequently, specific physiological responses of the plant are dependent on the PGPR strain/plant cultivar combination.

REGULATION OF PGPR FUNCTIONS BY MICROBIAL SIGNALS

Plant growth-promoting rhizobacteria exchange several types of cell-to-cell communication signals between each other and with other rhizosphere-inhabiting bacteria and fungi, i.e., quorum-sensing (QS) signals that allow bacteria to monitor their density and to coordinate gene expression only when a quorum of cells is achieved and other bacterial signals that regulate gene expression independently of the cell density.

Quorum-sensing relies on the synthesis and perception of small diffusible molecules, such as N-acyl-homoserine lactones (AHLs). In fluorescent pseudomonads, colonization properties and biosynthesis of antimicrobial metabolites, such as phenazines, is often subjected to an AHL-based QS regulation. Production of pyrrolnitrin in Serratia plymuthica HRO-C48, a strain isolated from the rhizosphere of oilseed rape and able to protect crops against Verticillium wilt, is also under QS regulation. In S. plymuthica G3, an endophytic strain, QS positively regulates antifungal activity, production of exoenzymes, but negatively regulates IAA production. Among the genus Azospirillum, only a few strains belonging to the lipoferum species and isolated from rice, display the ability to produce AHL signals. In the rice endophyte Azospirillum lipoferum B518, AHL inactivation abolishes pectinase activity, increases siderophore synthesis and reduces IAA production (in stationary phase) but no effect is observed on cellulase activity and on the phytostimulatory effect. Moreover, a proteomic approach indicates that AHL-based QS regulation in Azospirillum is rather dedicated to control functions linked to rhizosphere competence and adaptation to plant roots.

Interestingly, several studies have shown that bacterial communication of a specific bacterial population could be jammed by other microbes; indeed, some soil bacteria can inactivate AHL (notably members of the genus Bacillus), whereas others can intercept AHL or can act as a physical barrier preventing their diffusion. Consequently, other members of the bacterial rhizosphere community can compromise expression of biocontrol traits in PGPR. Conversely, cross-talk between species using the same AHL signal or a structurally-related AHL can occur in natural habitats and was evidenced in the rhizosphere of wheat and tomato. Finally, plant compounds designated as AHL-mimics can also interfere with bacterial QS and may influence the expression of plant-beneficial functions. Some Pseudomonas fluorescens strains unable to synthetize AHLs but possessing the cognate receptor may even recognize a plant compound to trigger expression of genes involved in biocontrol properties.

Exometabolites produced by microbial populations including pathogenic fungal strains can also affect PGPR plant-beneficial properties. For instance, fusaric acid produced by Fusarium oxysporum represses the production of DAPG in the biocontrol strain Pseudomonas protegens CHA0. Next to their antifungal effect, some Pseudomonas-produced compounds can influence gene expression of biocontrol traits in pseudomonads. Indeed, in Pseudomonas protegens strains CHA0 and Pf-5, DAPG and pyoluteorin productions are influenced by positive autoregulation; moreover, DAPG and pyoluteorin mutually inhibit one another’s production. In order to determine if DAPG could act as a signal on other PGPR strains than those of the fluorescent Pseudomonas group, a differential fluorescence induction promoter-trapping approach based on flow cytometry was developed on Azospirillum. Using this approach DAPG was shown to enhance expression of a wide range of Azospirillum brasilense genes, including genes involved in phytostimulation. Four of them (i.e., ppdC, flgE, nirK, and nifX-nifB) were upregulated on roots in the presence of Pseudomonas fluorescens F113 compared with its DAPG-negative mutant. Accordingly, Pseudomonas fluorescens F113 but not its DAPG-negative mutant enhanced the phytostimulatory effect of Azospirillum brasilense Sp245 on wheat. Thus, DAPG can act as a signal by which some beneficial pseudomonads may stimulate plant-beneficial activities of Azospirillum PGPR. This finding is also relevant in the context of inoculation with microbial consortia, in which different types of PGPR may be combined. The number of studies investigating the efficacy of such combined inoculations is growing, with variations in the number of microorganisms and the nature of the combinations (PGPR strains only, PGPR and fungi, etc.;;;; ). Field inoculation of sorghum with fluorescent Pseudomonas strains alone or in combination with arbuscular mycorrhizal fungi showed a better effect when in presence of the latter. Field inoculation of maize with a consortium consisting of two PGPR (Azospirillum lipoferum CRT1 and Pseudomonas fluorescens F113) and one mycorrhizal strain (Rhizophagus irregularis/Glomus intraradices JJ291) showed an increase of root surface, root volume and number of roots, although data were not statistically significant compared to the single Rhizophagus inoculation. Modification of one member of this consortium (three different Azospirillum strains were tested) could lead to significant modification of maize growth. Further studies are needed to describe the synergistic effects between beneficial microorganisms at a molecular scale and to analyse the expression of plant-beneficial functions when consortia are used.

ECOLOGY OF PGPR POPULATIONS AND IMPACT ON ROOT SYSTEM FUNCTIONING

Many studies have deciphered the mechanisms of action of PGPR using one individual strain and one host plant. But in reality, as described above, PGPR strains are not acting individually in the rhizosphere but rather as part of bacterial communities, in which cell communication signals may coordinate the activities of all individual strains. Indeed, a vast array of PGPR populations displaying co-occurring plant-beneficial activities and that may share between each other antagonistic or synergistic effects are interacting with a same host plant (Figure 3). When analysing plant growth-promoting effects, it is thus important to integrate the complexity of the interactions between PGPR populations within the rhizo-microbiome. To do so, functional ecology approaches are needed, in which the relations between the size, diversity and activities of PGPR assemblages in the rhizosphere are taken into account. This is of particular importance when assessing the effect of various environmental factors, including that of plant genotype.

PGPR ECOLOGY IN THE RHIZOSPHERE: FROM INDIVIDUAL STRAINS TO FUNCTIONAL GROUPS

Plant growth-promoting rhizobacteria strains occur in various taxonomic groups, and these different taxonomic groups may be present simultaneously in a given soil. This suggests that taxonomically-contrasted PGPR strains may coexist in soil and colonize a same rhizosphere, along with all non-PGPR members of the bacterial community. This possibility has been documented repeatedly, especially when characterizing the taxonomic status of bacterial isolates selected based on their positive effect on plant growth or health, their ability to inhibit phytopathogens, or the occurrence of a particular gene or property of relevance for PGPR effect. In fact, this possibility seems to be the rule rather than the exception. PGPR populations contributing to a same type of function (i.e., ISR, nitrogen fixation, nutrient solubilization, plant development enhancement, etc.) belong to a same functional group. Functional group approaches can be implemented when specific genes are documented. For instance, nitrogen fixers can be assessed using the nifH gene, which encodes the dinitrogenase subunit of the nitrogenase. Its sequence is well conserved within the functional group and it is commonly used as marker to monitor the size and diversity of the diazotrophic community. Some of these PGPR functional groups are taxonomically narrow, such as the Pseudomonas DAPG producers. In contrast, others are much more diversified, and certain bacterial functional groups may also comprise both PGPR and non-PGPR strains. For instance, nitrogen fixers include PGPR as well as mutualistic symbionts and even a few pathogens.

When considering PGPR-plant relationship in fields, the co-occurrence of genetically contrasted PGPR strains from a same functional group in the rhizosphere has two consequences. First, the activity of a given PGPR functional group corresponds to the resulting contributions of all active individual cells from each type of bacterium within the functional group. If synergistic effects occur between the PGPR populations, the expected performance level for the PGPR function might be higher than if only one type of strain was involved. On this basis, knowing the size of the functional group will help understand the potential importance of the corresponding function. Indeed, for functions leading to enhanced nutrient availability to the plant, such as nitrogen fixation or phosphorus solubilization, the higher the better. For others where optimality matters, such as the production of auxinic signals, the performance level of the functional group will need fine-tuning to avoid production levels too small or too great. How this is ecologically regulated at the scale of the corresponding functional group is unknown, but it raises the possibility of co-evolutionary patterns. To bridge the gap between the potential of a plant-beneficial PGPR function and its actual implementation by PGPR strains, the regulatory effects need also to be taken into consideration. Some of these regulatory effects will be common to all members of the functional group. However, other regulatory effects may be relevant for a subset only of the functional group. For instance, zinc sulfate stimulates DAPG production in certain but not all genetic groups of Pseudomonas PGPR strains.

Second, the relationships amongst the different PGPR strains co-occurring in a same rhizosphere are important. Interactions will take place within a functional group, as illustrated above with QS regulation of phenazine production in fluorescent Pseudomonas PGPR. Interactions may also take place between different PGPR functional groups (Figure 3), integrating competitive and inhibitory effects, signal jamming and positive signaling, as well as more indirect processes such as root exudation modifications. These interactions have the potential to modulate spatial colonization patterns of PGPR on roots and to affect PGPR performance. This also suggests that members of different PGPR functional groups can function together, as consortia, with the possibility of synergistic effects or, contrariwise, antagonistic effects. These positive effects may be sought by implementing inoculation procedures in which different types of plant-beneficial microorganisms are used in combination, as highlighted above. Even in this context, interactions between the different microbial strains that are inoculated and indigenous microorganisms (including PGPR) probably matter.

IMPACT OF PLANT GENOTYPES ON PGPR FUNCTIONAL GROUPS

Plants at species, sub-species and variety levels exhibit substantial genetic and phenotypic diversity. In the rhizosphere, different plant genotypes will have a different impact on the number, diversity and activity of microorganisms. This has been shown when comparing different plant species or varieties within species. It entails differences noticeably in root system structure, root exudation profile, and nutrient acquisition. These effects have also been evidenced when considering microbial functional groups of PGPR or where PGPR predominate.

Nitrogen-fixing bacteria are particularly important for plant nitrogen nutrition. The analysis of functional groups indicated that the size and/or composition of nitrogen-fixing bacteria is influenced by host plant features (Figure 3), both at plant species and variety levels. Analysis of nifH gene transcripts extracted from the rhizosphere showed that only a fraction of the community expresses nifH, and that the corresponding bacterial species differed according to the plant variety, pointing to an influence of plant genotype on the functioning of nitrogen-fixing bacteria. Similar findings were made with the functional group of phosphate solubilizers. Their selection by roots varies according to host plant species.

Other functional groups, such as those involved in plant protection from parasites, act mainly by competition or antagonism, even though direct ISR effects might also take place. For these microorganisms as well, plant genotype can have a major effect on microbial selection processes, as shown with fluorescent pseudomonads producing DAPG or hydrogen cyanide. Plant-genotype differences in rhizosphere ecology may also matter in terms of plant protection efficiency.

CONCLUSION

Plants have evolved different types of biotic interactions with soil microbial populations, ranging from commensalism to mutualism. Within this continuum of interactions, the plant-PGPR cooperation plays a major role by enhancing growth and health of widely diverse plants. Recent progress has helped to understand key features regarding the modes of action and ecology of plant-PGPR interactions, but major knowledge gaps remain. In terms of molecular signaling and functioning, whether PGPR fine-tune plant hormonal pathways similar to those induced by pathogens and symbionts and/or trigger yet-unknown specific pathways requires clarification.

Plant growth-promoting rhizobacteria are able to modulate RSA and in fine the vegetative growth and physiology of the whole plant. RSA effects have long been associated with the production of IAA by PGPR. Surprisingly, bacterial modulation of plant auxin distribution and IAA signal transduction pathways, independently of IAA production by PGPR, has also been revealed. It is obviously a step forward in our understanding of plant-PGPR cooperation but it does not fully clarify the bacterial functions and plant hormonal networks involved. Plant hormones regulate genes for the biosynthesis of other hormones or components of hormonal pathways. Consequently, it is possible that PGPR can affect these cross-talks too. It would explain why PGPR can have such pleiotropic effects on plants. One of the major current scientific challenges lying ahead is to understand how these different signaling pathways are integrated to coordinate plant growth and development, and how PGPR influence the plant hormonal network.

Distinct PGPR populations present in a same soil can express plant-beneficial properties in concert. As aforementioned, the relationships between plants and their rhizo-microbiome are complex and vary both according to plant genotypes and soil inhabiting populations (and thus local soil properties, more generally speaking). Next-generation sequencing technologies have started to reveal their taxonomic and functional diversity. They have begun to bring new knowledge on the ecology of PGPR functional groups. In the near future, it is expected that metatranscriptomics and metaproteomics will develop drastically, and will allow further progress on the understanding of the activity and ecological behavior of natural PGPR populations within the rhizosphere. However, given the heterogeneity in space and time of the rhizosphere habitat, samplings at different times and locations within the plant rhizosphere and within fields will be essential to better understand the ecology and performance of PGPR at plant and field plot scales. Nevertheless, despite being very reductionist, mechanistic functional studies using one PGPR and one plant are still useful to investigate the ways PGPR exert beneficial effects on plants. We think that the most important advances on plant-PGPR cooperation will be brought in the future by combining both ecology and functional biology approaches.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References 247

  1. 1.

    Ahn S. J. Shin R. Schachtman D. P. (2004 ). Expression of KT/KUP genes in Arabidopsis and the role of root hairs in K+ uptake. Plant Physiol. 134 1135–1145

    Not in our library10.1104/pp.103.034660

  2. 2.

    Aira M. Gómez-Brandón M. Lazcano C. Bååth E Domïnguez J. (2010 ). Plant genotype strongly modifies the structure and growth of maize rhizosphere microbial communities. Soil Biol. Biochem. 42 2276–2281

    Not in our library10.1016/j.soilbio.2010.08.029

  3. 3.

    Ait Barka E. Nowak J. Clement C. (2006 ). Enhancement of chilling resistance of inoculated grapevine plantlets with a plant growth-promoting rhizobacterium, Burkholderia phytofirmans strain PsJN. Appl. Environ. Microbiol. 72 7246–7252

    Not in our library10.1128/aem.01047-06

  4. 4.

    Almario J. Kyselková M. Kopecký J. Ságová-Marečková M. Muller D. Grundmann G. L. (2013a ). Assessment of the relationship between geologic origin of soil, rhizobacterial community composition and soil receptivity to tobacco black root rot in Savoie region (France). Plant Soil.

    Not in our library10.1007/s11104-013-1677-1671

  5. 5.

    Almario J. Prigent-Combaret C. Muller D Mënne-Loccoz Y. (2013b ). Effect of clay mineralogy on iron bioavailability and rhizosphere transcription of 2,4-diacetylphloroglucinol biosynthetic genes in biocontrol Pseudomonas protegens. Mol. Plant Microbe Interact. 26 566–574

    Not in our library10.1094/mpmi-11-12-0274-r

  6. 6.

    Aloni R. Aloni E. Langhans M. Ullrich C. I. (2006 ). Role of cytokinin and auxin in shaping root architecture: regulating vascular differentiation, lateral root initiation, root apical dominance and root gravitropism. Ann. Bot. 97 883–893

    Not in our library10.1093/aob/mcl027

  7. 7.

    Alonso J. M. Stepanova A. N. Leisse T. J. Kim C. J. Chen H. M. Shinn P. (2003 ). Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301 653–657

    Not in our library10.1126/science.1086391

  8. 8.

    Anderson A. J. Guerra D. (1985 ). Responses of bean to root colonization with Pseudomonas putida in a hydroponic system. Phytopathology 75 992–995

    Not in our library10.1094/phyto-75-992

  9. 9.

    Arkhipova T. N. Prinsen E. Veselov S. U. Martinenko E. V. Melentiev A. I. Kudoyarova G. R. (2007 ). Cytokinin producing bacteria enhance plant growth in drying soil. Plant Soil 292 305–315

    Not in our library10.1007/s11104-007-9233-5

  10. 10.

    Bacilio-Jiménez M. Aguilar-Flores S. Ventura-Zapata E. Perez-Campos E. Bouquelet S. Zenteno E. (2003 ). Chemical characterization of root exudates from rice (Oryza sativa) and their effects on the chemotactic response of endophytic bacteria. Plant Soil 249 271–277

    Not in our library10.1023/a:1022888900465

  11. 11.

    Badri D. V. Weir T. L. van der Lelie D. Vivanco J. M. (2009 ). Rhizosphere chemical dialogues: plant-microbe interactions. Curr. Opin. Biotechnol. 20 642–650

    Not in our library10.1016/j.copbio.2009.09.014

  12. 12.

    Baehler E. Bottiglieri M. Pechy-Tarr M. Maurhofer M. Keel C. (2005 ). Use of green fluorescent protein-based reporters to monitor balanced production of antifungal compounds in the biocontrol agent Pseudomonas fluorescens CHA0. J. Appl. Microbiol. 99 24–38

    Not in our library10.1111/j.1365-2672.2005.02597.x

  13. 13.

    Bais H. P. Weir T. L. Perry L. G. Gilroy S. Vivanco J. M. (2006 ). The role of root exudates in rhizosphere interactions with plants and other organisms. Annu. Rev. Plant Biol. 57 233–266

    Not in our library10.1146/annurev.arplant.57.032905.105159

  14. 14.

    Bakker P. A. Pieterse C. M van Loon L. C. (2007 ). Induced systemic resistance by fluorescent Pseudomonas spp. Phytopathology 97 239–243

    Not in our library10.1094/phyto-97-2-0239

  15. 15.

    Barea J. M. Pozo M. J. Azcón R Azcón-Aguilar C. (2005 ). Microbial co-operation in the rhizosphere. J. Exp. Bot. 56 1761–1778

    Not in our library10.1093/jxb/eri197

  16. 16.

    Barriuso J. Pereyra M. T. Lucas Garcia J. A. Megias M. Gutierrez Manero F. J. Ramos B. (2005 ). Screening for putative PGPR to improve establishment of the symbiosis Lactarius deliciosus-Pinus sp. Microb. Ecol. 50 82–89

    Not in our library10.1007/s00248-004-0112-9

  17. 17.

    Bashan Y. de-Bashan L. E. (2010 ). How the plant growth-promoting bacterium Azospirillum promotes plant growth – a critical assessment. Adv. Agron. 108 77–136

    Not in our library10.1016/s0065-2113(10)08002-8

  18. 18.

    Bauer H. Ache P. Lautner S. Fromm J. Hartung W. Al-Rasheid Khaled A. S. (2013 ). The stomatal response to reduced relative humidity requires guard cell-autonomous ABA synthesis. Curr. Biol. 1 53–57

    Not in our library10.1016/j.cub.2012.11.022

  19. 19.

    Bekri M. A. Desair J. Keijers V. Proost P. Searle-van Leeuwen M. Vanderleyden J. (1999 ). Azospirillum irakense produces a novel type of pectate lyase. J. Bacteriol. 181 2440–2447

    Not in our library10.1128/jb.181.8.2440-2447.1999

  20. 20.

    Benhamou N. Belanger R. R. Paulitz T. C. (1996 ). Pre-inoculation of Ri T-DNA-transformed pearoots with Pseudomonas fluorescens inhibits colonization by Pythium ultimum Trow: an ultrastructural and cytochemical study. Planta 199 105–117

    Not in our library10.1007/bf00196887

  21. 21.

    Benizri E. Baudoin E. Guckert A. (2001 ). Root colonization by inoculated plant growth promoting rhizobacteria. Biocontrol Sci. Technol. 11 557–574

    Not in our library10.1080/09583150120076120

  22. 22.

    Berg G. Smalla K. (2009 ). Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol. Ecol. 68 1–13

    Not in our library10.1111/j.1574-6941.2009.00654.x

  23. 23.

    Bergsma-Vlami M. Prins M. E. Raaijmakers J. M. (2005 ). Influence of plant species on population dynamics, genotypic diversity and antibiotic production in the rhizosphere by indigenous Pseudomonas spp. FEMS Microbiol. Ecol. 52 59–69

    Not in our library10.1016/j.femsec.2004.10.007

  24. 24.

    Berthomieu P. Conejero G. Nublat A. Brackenbury W. J. Lambert C. Savio C. (2003 ). Functional analysis of AtHKT1 in Arabidopsis shows that Na+ recirculation by the phloem is crucial for salt tolerance. EMBO J. 22 2004–2014

    Not in our library10.1093/emboj/cdg207

  25. 25.

    Bertin C. Yang X. H. Weston L. A. (2003 ). The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256 67–83

    Not in our library10.1023/a:1026290508166

  26. 26.

    Bertrand H. Nalin R. Bally R. Cleyet-Marel J. C. (2001 ). Isolation and identification of the most efficient plant growth-promoting bacteria associated with canola (Brassica napus). Biol. Fertil. Soils 33 152–156

    Not in our library10.1007/s003740000305

  27. 27.

    Bertrand H. Plassard C. Pinochet X. Touraine B. Normand P. Cleyet-Marel J. C. (2000 ). Stimulation of the ionic transport system in Brassica napus by a plant growth-promoting rhizobacterium (Achromobacter sp.). Can. J. Microbiol. 46 229–236

    Not in our library10.1139/cjm-46-3-229

  28. 28.

    Bharti N. Yadav D. Barnawal D. Maji D. Kalra A. (2013 ). Exiguobacterium oxidotolerans, a halotolerant plant growth promoting rhizobacteria, improves yield and content of secondary metabolites in Bacopa monnieri (L.) Pennell under primary and secondary salt stress. World J. Microbiol. Biotechnol. 29 379–387

    Not in our library10.1007/s11274-012-1192-1

  29. 29.

    Blaha D. Prigent-Combaret C. Mirza M. S Mënne-Loccoz Y. (2006 ). Phylogeny of the 1-aminocyclopropane-1-carboxylic acid deaminase-encoding gene acdS in phytobeneficial and pathogenic Proteobacteria and relation with strain biogeography. FEMS Microbiol. Ecol. 56 455–470

    Not in our library10.1111/j.1574-6941.2006.00082.x

  30. 30.

    Bleecker A. B. Kende H. (2000 ). Ethylene: a gaseous signal molecule in plants. Annu. Rev. Cell Dev. Biol. 16 1–18

    Not in our library10.1146/annurev.cellbio.16.1.1

  31. 31.

    Boddey R. M. Urquiaga S. Alves B. J. R. Reis V. (2003 ). Endophytic nitrogen fixation in sugarcane: present knowledge and future applications. Plant Soil 252 139–149

    Not in our library10.1023/a:1024152126541

  32. 32.

    Bottini R. Cassán F. Piccoli P. (2004 ). Gibberellin production by bacteria and its involvement in plant growth promotion and yield increase. Appl. Microbiol. Biotechnol. 65 497–503

    Not in our library10.1007/s00253-004-1696-1

  33. 33.

    Bouffaud M. L. Kyselkova M. Gouesnard B. Grundmann G. Muller D Mënne-Loccoz Y. (2012 ). Is diversification history of maize influencing selection of soil bacteria by roots? Mol. Ecol. 21 195–206

    Not in our library10.1111/j.1365-294x.2011.05359.x

  34. 34.

    Boyer M. Bally R. Perrotto S. Chaintreuil C Wisniewski-Dyé F. (2008 ). A quorum-quenching approach to identify quorum-sensing-regulated functions in Azospirillum lipoferum. Res. Microbiol. 159 699–708

    Not in our library10.1016/j.resmic.2008.08.003

  35. 35.

    Boyer M Wisniewski-Dyé F. (2009 ). Cell–cell signaling in bacteria: not simply a matter of quorum. FEMS Microbiol. Ecol. 70 1–19

    Not in our library10.1111/j.1574-6941.2009.00745.x

  36. 36.

    Brandl M. T. Lindow S. E. (1998 ). Contribution of indole-3-acetic acid production to the epiphytic fitness of Erwinia herbicola. Appl. Environ. Microbiol. 64 3256–3263

    Not in our library10.1128/aem.64.9.3256-3263.1998

  37. 37.

    Brazelton J. N. Pfeufer E. E. Sweat T. A. McSpadden Gardener B. B. Coenen C. (2008 ). 2,4-diacetylphloroglucinol alters plant root development. Mol. Plant Microbe. Interact. 21 1349–1358

    Not in our library10.1094/mpmi-21-10-1349

  38. 38.

    Brodhagen M. Henkels M. D. Loper J. E. (2004 ). Positive autoregulation and signaling properties of pyoluteorin, an antibiotic produced by the biological control organism Pseudomonas fluorescens Pf-5. Appl. Environ. Microbiol. 70 1758–1766

    Not in our library10.1128/aem.70.3.1758-1766.2004

  39. 39.

    Brusamarello-Santos L. C. C. Pacheco F. Aljanabi S. M. M. Monteiro R. A. Cruz L. M. Baura V. A. (2012 ). Differential gene expression of rice roots inoculated with the diazotroph Herbaspirillum seropedicae. Plant Soil 356 113–125

    Not in our library10.1007/s11104-011-1044-z

  40. 40.

    Bulgarelli D. Schlaeppi K. Spaepen S. Ver Loren van Themaat E. Schulze-Lefert P. (2013 ). Structure and functions of the bacterial microbiota of plants. Annu. Rev. Plant Biol. 64 807–838

    Not in our library10.1146/annurev-arplant-050312-120106

  41. 41.

    Burdman S. Volpin H. Kigel J. Kapulnik Y. Okon Y. (1996 ). Promotion of nod gene inducers and nodulation in common bean (Phaseolus vulgaris) roots inoculated with Azospirillum brasilense Cd. Appl. Environ. Microbiol. 62 3030–3033

    Not in our library10.1128/aem.62.8.3030-3033.1996

  42. 42.

    Cacciari I. Lippi D. Pietrosanti T. Pietrosanti W. (1989 ). Phytohormone-like substances produced by single and mixed diazotrophic cultures of Azospirillum and Arthrobacter. Plant Soil 115 151–153

    Not in our library10.1007/bf02220706

  43. 43.

    Cartieaux F. Thibaud M. C. Zimmerli L. Lessard P. Sarrobert C. David P. (2003 ). Transcriptome analysis of Arabidopsis colonized by a plant-growth promoting rhizobacterium reveals a general effect on disease resistance. Plant J. 36 177–188

    Not in our library10.1046/j.1365-313x.2003.01867.x

  44. 44.

    Casimiro I. Marchant A. Bhalerao R. P. Beeckman T. Dhooge S. Swarup R. (2001 ). Auxin transport promotes Arabidopsis lateral root initiation. Plant Cell 13 843–852

    Not in our library10.1105/tpc.13.4.843

  45. 45.

    Cassán F. Perrig D. Sgroy V. Masciarelli O. Penna C. Luna V. (2009 ). Azospirillum brasilense Az39 and Bradyrhizobium japonicum E109, inoculated singly or in combination, promote seed germination and early seedling growth in corn (Zea mays L.) and soybean (Glycine max L.). Eur. J. Soil Biol. 45 28–35

    Not in our library10.1016/j.ejsobi.2008.08.005

  46. 46.

    Chamam A. Sanguin H. Bellvert F. Meiffren G. Comte G. Wisniewski-Dyé F. (2013 ). Plant secondary metabolite profiling evidences strain-dependent effect in the Azospirillum-Oryza sativa association. Phytochemistry 87 65–77

    Not in our library10.1016/j.phytochem.2012.11.009

  47. 47.
    Root Exudation of Phytochemicals in Arabidopsis Follows Specific Patterns That Are Developmentally Programmed and Correlate with Soil Microbial Functions · 2013
    Corrected
  48. 48.

    Chen C. R. Condron L. M. Davis M. R. Sherlock R. R. (2002 ). Phosphorus dynamics in the rhizosphere of perennial ryegrass (Lolium perenne L.) and radiata pine (Pinus radiata D. Don.). Soil Biol. Biochem. 34 487–499

    Not in our library10.1016/s0038-0717(01)00207-3

  49. 49.

    Chin-A-Woeng T. F. van den Broek D. de Voer G. van der Drift K. M. Tuinman S. Thomas-Oates J. E. (2001 ). Phenazine-1-carboxamide production in the biocontrol strain Pseudomonas chlororaphis PCL1391 is regulated by multiple factors secreted into the growth medium. Mol. Plant Microbe. Interact. 14 969–979

    Not in our library10.1094/mpmi.2001.14.8.969

  50. 50.

    Coelho M. R. R. Marriel I. E. Jenkins S. N. Lanyon C. V. Seldin L O’Donnell A. G. (2009 ). Molecular detection and quantification of nifH gene sequences in the rhizosphere of sorghum (Sorghum bicolor) sown with two levels of nitrogen fertilizer. Appl. Soil Ecol. 42 48–53

    Not in our library10.1016/j.apsoil.2009.01.010

  51. 51.

    Cohen A. C. Bottini R. Piccoli P. N. (2008 ). Azospirillum brasilense Sp 245 produces ABA in chemically-defined culture medium and increases ABA content in Arabidopsis plants. Plant Growth Regul. 54 97–103

    Not in our library10.1007/s10725-007-9232-9

  52. 52.

    Comas L. H. Eissenstat D. M. (2009 ). Patterns in root trait variation among 25 co-existing North American forest species. New Phytol. 182 919–928

    Not in our library10.1111/j.1469-8137.2009.02799.x

  53. 53.

    Combes-Meynet E. Pothier J. F. Mënne-Loccoz Y. Prigent-Combaret C. (2011 ). The Pseudomonas secondary metabolite 2,4-diacetylphloroglucinol is a signal inducing rhizoplane expression of Azospirillum genes involved in plant-growth promotion. Mol. Plant Microbe. Interact. 24 271–284

    Not in our library10.1094/mpmi-07-10-0148

  54. 54.

    Compant S. Clément C Sessitsch A. (2010 ). Plant growth-promoting bacteria in the rhizo- and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol. Biochem. 42 669–678

    Not in our library10.1016/j.soilbio.2009.11.024

  55. 55.

    Contesto C. Desbrosses G. Lefoulon C. Bena G. Borel F. Galland M. (2008 ). Effects of rhizobacterial ACC deaminase activity on Arabidopsis indicate that ethylene mediates local root responses to plant growth-promoting rhizobacteria. Plant Sci. 1–2 178–189

    Not in our library10.1016/j.plantsci.2008.01.020

  56. 56.

    Contesto C. Milesi S. Mantelin S. Zancarini A. Desbrosses G. Varoquaux F. (2010 ). The auxin-signaling pathway is required for the lateral root response of Arabidopsis to the rhizobacterium Phyllobacterium brassicacearum. Planta 232 1455–1470

    Not in our library10.1007/s00425-010-1264-0

  57. 57.

    Costa R. Götz M. Mrotzek N. Lottmann J. Berg G. Smalla K. (2006 ). Effects of site and plant species on rhizosphere community structure as revealed by molecular analysis of microbial guilds. FEMS Microbiol. Ecol. 56 236–249

    Not in our library10.1111/j.1574-6941.2005.00026.x

  58. 58.

    Couillerot O. Combes-Meynet E. Pothier J. F. Bellvert F. Challita E. Poirier M. A. (2011 ). The role of the antimicrobial compound 2,4-diacetylphloroglucinol in the impact of biocontrol Pseudomonas fluorescens F113 on Azospirillum brasilense phytostimulators. Microbiology 157 1694–1705

    Not in our library10.1099/mic.0.043943-0

  59. 59.

    Couillerot O. Prigent-Combaret C. Caballero-Mellado J Mënne-Loccoz Y. (2009 ). Pseudomonas fluorescens and closely-related fluorescent pseudomonads as biocontrol agents of soil-borne phytopathogens. Lett. Appl. Microbiol. 48 505–512

    Not in our library10.1111/j.1472-765x.2009.02566.x

  60. 60.

    Couillerot O. Ramirez-Trujillo A. Walker V. von Felten A. Jansa J. Maurhofer M. (2012 ). Comparison of prominent Azospirillum strains in Azospirillum-Pseudomonas-Glomus consortia for promotion of maize growth. Appl. Microbiol. Biotechnol. 97 4639–4649

    Not in our library10.1007/s00253-012-4249-z

  61. 61.

    Creus C. M. Graziano M. Casanovas E. M. Pereyra M. A. Simontacchi M. Puntarulo S. (2005 ). Nitric oxide is involved in the Azospirillum brasilense-induced lateral root formation in tomato. Planta 221 297–303

    Not in our library10.1007/s00425-005-1523-7

  62. 62.

    Curzi M. J. Ribaudo C. M. Trinchero G. D. Cura J. A. Pagano E. A. (2008 ). Changes in the content of organic and amino acids and ethylene production of rice plants in response to the inoculation with Herbaspirillum seropedicae. J. Plant Interact. 3 163–173

    Not in our library10.1080/17429140802255167

  63. 63.

    Czarnota M. A. Rimando A. M. Weston L. A. (2003 ). Evaluation of root exudates of seven sorghum accessions. J. Chem. Ecol. 29 2073–2083

    Not in our library10.1023/a:1025634402071

  64. 64.

    Dardanelli M. S. Manyani H. Gonzalez-Barroso S. Rodriguez-Carvajal M. A. Gil-Serrano A. M. Espuny M. R. (2010 ). Effect of the presence of the plant growth promoting rhizobacterium (PGPR) Chryseobacterium balustinum Aur9 and salt stress in the pattern of flavonoids exuded by soybean roots. Plant Soil 328 483–493

    Not in our library10.1007/s11104-009-0127-6

  65. 65.

    de Garcïa Salamone I. E. Hynes R. K. Nelson L. M. (2001 ). Cytokinin production by plant growth promoting rhizobacteria and selected mutants. Can. J. Microbiol. 47 404–411

    Not in our library10.1139/w01-029

  66. 66.

    De Maeyer K. D’Aes J. Hua G. K. Perneel M. Vanhaecke L. Noppe H. (2011 ). N-Acylhomoserine lactone quorum-sensing signaling in antagonistic phenazine-producing Pseudomonas isolates from the red cocoyam rhizosphere. Microbiology 157 459–472

    Not in our library10.1099/mic.0.043125-0

  67. 67.

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

    Not in our library10.1016/j.chom.2011.09.005

  68. 68.

    De Smet I. Zhang H. Inzé D. Beeckman T. (2006 ). A novel role for abscisic acid emerges from underground. Trends Plant Sci. 11 434–439

    Not in our library10.1016/j.tplants.2006.07.003

  69. 69.

    Desoignies N. Schramme F. Ongena M. Legreve A. (2012 ). Systemic resistance induced by Bacillus lipopeptides in Beta vulgaris reduces infection by the rhizomania disease vector Polymyxa betae. Mol. Plant Pathol. 14 416–421

    Not in our library10.1111/mpp.12008

  70. 70.

    de Werra P. Huser A. Tabacchi R. Keel C. Maurhofer M. (2011 ). Plant- and microbe-derived compounds affect the expression of genes encoding antifungal compounds in a pseudomonad with biocontrol activity. Appl. Environ. Microbiol. 77 2807–2812

    Not in our library10.1128/aem.01760-10

  71. 71.

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

    Not in our library10.1038/nrmicro954

  72. 72.

    Dobbelaere S. Croonenborghs A. Thys A. Vande Broek A. Vanderleyden J. (1999 ). Phytostimulatory effect of Azospirillum brasilense wild type and mutant strains altered in IAA production on wheat. Plant Soil 212 153–162

    Not in our library10.1023/a:1004658000815

  73. 73.

    Dobbelaere S. Vanderleyden J. Okon Y. (2003 ). Plant growth-promoting effects of diazotrophs in the rhizosphere. Crit. Rev. Plant Sci. 22 107–149

    Not in our library10.1080/713610853

  74. 74.

    Dodd I. C. Zinovkina N. Y. Safronova V. I. Belimov A. A. (2010 ). Rhizobacterial mediation of plant hormone status. Ann. Appl. Biol. 157 361–379

    Not in our library10.1111/j.1744-7348.2010.00439.x

  75. 75.

    Doornbos R. F. van Loon L. C Bakker P. A. H. M. (2012 ). Impact of root exudates and plant defense signaling on bacterial communities in the rhizosphere. A review. Agron. Sustain. Dev. 32 227–243

    Not in our library10.1007/s13593-011-0028-y

  76. 76.

    Drogue B. Combes-Meynet E. Mënne-Loccoz Y. Wisniewski-Dyé F. Prigent-Combaret C. (2013 ). “Control of the cooperation between plant growth-promoting rhizobacteria and crops by rhizosphere signals,” in Vol. 1 and 2 Molecular Microbial Ecology of the Rhizosphere ed. de Bruijn F. J. (NJ, USA: John Wiley & Sons, Inc.) 281–294

    Not in our library10.1002/9781118297674.ch27

  77. 77.

    Drogue B. Dore H. Borland S. Wisniewski-Dyé F. Prigent-Combaret C. (2012 ). Which specificity in cooperation between phytostimulating rhizobacteria and plants? Res. Microbiol. 163 500–510

    Not in our library10.1016/j.resmic.2012.08.006

  78. 78.

    Dubrovsky J. G. Esther Puente M. Bashan Y. (1994 ). Arabidopsis thaliana as a model system for the study of the effect of inoculation by Azospirillum brasilense Sp-245 on root-hair growth. Soil Biol. Biochem. 26 1657–1664

    Not in our library10.1016/0038-0717(94)90318-2

  79. 79.

    Duffy B. K Défago G. (1999 ). Environmental factors modulating antibiotic and siderophore biosynthesis by Pseudomonas fluorescens biocontrol strains. Appl. Environ. Microbiol. 65 2429–2438

    Not in our library10.1128/aem.65.6.2429-2438.1999

  80. 80.

    Dutta S. Podile A. R. (2010 ). Plant growth promoting rhizobacteria (PGPR): the bugs to debug the root zone. Crit. Rev. Microbiol. 36 232–244

    Not in our library10.3109/10408411003766806

  81. 81.

    El Zemrany H. Cortet J. Lutz M. P. Chabert A. Baudoin E. Haurat J. (2006 ). Field survival of the phytostimulator Azospirillum lipoferum CRT1 and functional impact on maize crop, biodegradation of crop residues, and soil faunal indicators in a context of decreasing nitrogen fertilisation. Soil Biol. Biochem. 38 1712–1726

    Not in our library10.1016/j.soilbio.2005.11.025

  82. 82.

    El Zemrany H. Czarnes S. Hallett P. D. Alamercery S. Bally R. Jocteur-Monrozier L. (2007 ). Early changes in root characteristics of maize (Zea mays) following seed inoculation with the PGPR Azospirillum lipoferum CRT1. Plant Soil 291 109–118

    Not in our library10.1007/s11104-006-9178-0

  83. 83.

    Fernandez O. Theocharis A. Bordiec S. Feil R. Jacquens L. Clement C. (2012 ). Burkholderia phytofirmans PsJN acclimates grapevine to cold by modulating carbohydrate metabolism. Mol. Plant Microbe. Interact. 25 496–504

    Not in our library10.1094/mpmi-09-11-0245

  84. 84.

    Fester T. Maier W. Strack D. (1999 ). Accumulation of secondary compounds in barley and wheat roots in response to inoculation with an arbuscular mycorrhizal fungus and co-inoculation with rhizosphere bacteria. Mycorrhiza 8 241–246

    Not in our library10.1007/s005720050240

  85. 85.

    Frapolli M. Défago G Mënne-Loccoz Y. (2010 ). Denaturing gradient gel electrophoretic analysis of dominant 2,4-diacetylphloroglucinol biosynthetic phlD alleles in fluorescent Pseudomonas from soils suppressive or conducive to black root rot of tobacco. Soil Biol. Biochem. 42 649–656

    Not in our library10.1016/j.soilbio.2010.01.005

  86. 86.

    Frapolli M. Pothier J. F. Défago G Mënne-Loccoz Y. (2012 ). Evolutionary history of synthesis pathway genes for phloroglucinol and cyanide antimicrobials in plant-associated fluorescent pseudomonads. Mol. Phylogenet. Evol. 63 877–890

    Not in our library10.1016/j.ympev.2012.02.030

  87. 87.

    Frébort I. Kowalska M. Hluska T. Frébortová J. Galuszka P. (2011 ). Evolution of cytokinin biosynthesis and degradation. J. Exp. Bot. 62 2431–2452

    Not in our library10.1093/jxb/err004

  88. 88.

    Fulchieri M. Lucangeli C. Bottini R. (1993 ). Inoculation with Azospirillum lipoferum affects growth and gibberellin status of corn seedling roots. Plant Cell Physiol. 34 1305–1309

    Not in our library

  89. 89.

    Fuqua W. C. Winans S. C. Greenberg E. P. (1994 ). Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J. Bacteriol. 176 269–275

    Not in our library10.1128/jb.176.2.269-275.1994

  90. 90.

    Galland M. Gamet L. Varoquaux F. Touraine B. Desbrosses G. (2012 ). The ethylene pathway contributes to root hair elongation induced by the beneficial bacteria Phyllobacterium brassicacearum STM196. Plant Sci. 190 74–81

    Not in our library10.1016/j.plantsci.2012.03.008

  91. 91.

    Gans J. Wolinsky M. Dunbar J. (2005 ). Computational improvements reveal great bacterial diversity and high metal toxicity in soil. Science 309 1387–1390

    Not in our library10.1126/science.1112665

  92. 92.

    Garcïa-Gutiérrez L. Zeriouh H. Romero D. Cubero J. de Vicente A Pérez-Gracia A. (2013 ). The antagonistic strain Bacillus subtilis UMAF6639 also confers protection to melon plants against cucurbit powdery mildew by activation of jasmonate- and salicylic acid-dependent defence responses. Microb. Biotechnol. 6 264–74

    Not in our library10.1111/1751-7915.12028

  93. 93.

    Germida J. Siciliano S. (2001 ). Taxonomic diversity of bacteria associated with the roots of modern, recent and ancient wheat cultivars. Biol. Fertil. Soil 33 410–415

    Not in our library10.1007/s003740100343

  94. 94.

    Glick B. R. (2005 ). Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase. FEMS Microbiol. Lett. 251 1–7

    Not in our library10.1016/j.femsle.2005.07.030

  95. 95.

    Glick B. R. Cheng Z. Czarny J. Duan J. (2007 ). Promotion of plant growth by ACC deaminase-producing soil bacteria. Eur. J. Plant Pathol. 119 329–339

    Not in our library10.1007/s10658-007-9162-4

  96. 96.

    Gomes N. C. M. Cleary D. F. R. Pinto F. N. Egas C. Almeida A. Cunha A. (2010 ). Taking root: Enduring effect of rhizosphere bacterial colonization in mangroves. PLoS ONE 5:e14065

    Not in our library10.1371/journal.pone.0014065

  97. 97.

    Grayston S. J. Wang S. Campbell C. D. Edwards A. C. (1998 ). Selective influence of plant species on microbial diversity in the rhizosphere. Soil Biol. Biochem. 30 369–378

    Not in our library10.1016/s0038-0717(97)00124-7

  98. 98.

    Gutiérrez-Mañero F. J. Ramos-Solano B. Probanza A. Mehouachi J. Tadeo F. R. Talon M. (2001 ). The plant-growth promoting rhizobacteria Bacillus pumilus and Bacillus licheniformis produce high amounts of physiologically active gibberellins. Physiol. Plant. 111 206–211

    Not in our library10.1034/j.1399-3054.2001.1110211.x

  99. 99.

    Hartmann A. Schmid M. Tuinen D. Berg G. (2009 ). Plant-driven selection of microbes. Plant Soil 321 235–257

    Not in our library10.1007/s11104-008-9814-y

  100. 100.

    Hemashenpagam N. Selvaraj T. (2011 ). Effect of arbuscular mycorrhizal (AM) fungus and plant growth promoting rhizomicroorganisms (PGPR's) on medicinal plant Solanum viarum seedlings. J. Environ. Biol. 32 579–583

    Not in our library

  101. 101.

    Herridge D. F. Peoples M. B. Boddey R. M. (2008 ). Global inputs of biological nitrogen fixation in agricultural systems. Plant Soil 311 1–18

    Not in our library10.1007/s11104-008-9668-3

  102. 102.

    Heulin T. Guckert A. Balandreau J. (1987 ). Stimulation of root exudation of rice seedlings by Azospirillum strains – carbon budget under gnotobiotic conditions. Biol. Fertil. Soil 4 9–14

    Not in our library

  103. 103.

    Hontzeas N. Zoidakis J. Glick B. R. Abu-Omar M. M. (2004 ). Expression and characterization of 1-aminocyclopropane-1-carboxylate deaminase from the rhizobacterium Pseudomonas putida UW4: a key enzyme in bacterial plant growth promotion. Biochim. Biophys. Acta 1703 11–19

    Not in our library10.1016/j.bbapap.2004.09.015

  104. 104.

    Hsu S.-F. Buckley D. H. (2009 ). Evidence for the functional significance of diazotroph community structure in soil. ISME J. 3 124–136

    Not in our library10.1038/ismej.2008.82

  105. 105.

    Hussain A. Hasnain S. (2009 ). Cytokinin production by some bacteria: its impact on cell division in cucumber cotyledons. Afr. J. Microbiol. Res. 3 704–712

    Not in our library

  106. 106.
    Induced Systemic Resistance in Arabidopsis thaliana in Response to Root Inoculation with Pseudomonas fluorescens CHA0 · 2003
    Not checked
  107. 107.

    Imsande J. Touraine B. (1994 ). N demand and the regulation of nitrate uptake. Plant Physiol. 105 3–7

    Not in our library10.1104/pp.105.1.3

  108. 108.

    İnceoǧlu O. Falcão Salles J. van Overbeek L van Elsas J. D. (2010 ). Effects of plant genotype and growth stage on the betaproteobacterial communities associated with different potato cultivars in two fields. Appl. Environ. Microbiol. 76 3675–3684

    Not in our library10.1128/aem.00040-10

  109. 109.

    Jaeger C. H. III Lindow S. E. Miller W. Clark E. Firestone M. K. (1999 ). Mapping of sugar and amino acid availability in soil around roots with bacterial sensors of sucrose and tryptophan. Appl. Environ. Microbiol. 65 2685–2690

    Not in our library10.1128/aem.65.6.2685-2690.1999

  110. 110.

    Jaleel C. A. Manivannan P. Sankar B. Kishorekumar A. Gopi R. Somasundaram R. (2007 ). Pseudomonas fluorescens enhances biomass yield and ajmalicine production in Catharanthus roseus under water deficit stress. Colloids Surf. B Biointerfaces 60 7–11

    Not in our library10.1016/j.colsurfb.2007.05.012

  111. 111.

    Jamali F. Sharifi-Tehrani A. Lutz M. Maurhofer M. (2009 ). Influence of host plant genotype, presence of a pathogen, and coinoculation with Pseudomonas fluorescens strains on the rhizosphere expression of hydrogen cyanide- and 2,4-diacetylphloroglucinol biosynthetic genes in P. fluorescens biocontrol strain CHA0. Microb. Ecol. 57 267–275

    Not in our library10.1007/s00248-008-9471-y

  112. 112.

    Jha Y. Subramanian R. B. Patel S. (2011 ). Combination of endophytic and rhizospheric plant growth promoting rhizobacteria in Oryza sativa shows higher accumulation of osmoprotectant against saline stress. Acta Physiol. Plant 33 797–802

    Not in our library10.1007/s11738-010-0604-9

  113. 113.

    Jing Y. D. He Z. L. Yang X. E. (2007 ). Role of soil rhizobacteria in phytoremediation of heavy metal contaminated soils. J. Zhejiang Univ. Sci. B 8 192–207

    Not in our library10.1631/jzus.2007.b0192

  114. 114.

    Kaeppler S. M. Parke J. L. Mueller S. M. Senior L. Stuber C. Tracy W. F. (2000 ). Variation among maize inbred lines and detection of quantitative trait loci for growth at low phosphorus and responsiveness to arbuscular mycorrhizal fungi. Crop Sci. 40 358–364

    Not in our library10.2135/cropsci2000.402358x

  115. 115.

    Kamilova F. Kravchenko L. V. Shaposhnikov A. I. Azarova T. Makarova N. Lugtenberg B. (2006 ). Organic acids, sugars and L-tryptophane in exudates of vegetables growing on stonewool and their effects on activities of rhizosphere bacteria. Mol. Plant Microbe Interact. 9 250–256

    Not in our library10.1094/mpmi-19-0250

  116. 116.

    Kechid M. Desbrosses G. Rokhsi W. Varoquaux F. Djekoun A. Touraine B. (2013 ). The NRT2.5 and NRT2.6 genes are involved in growth promotion of Arabidopsis by the PGPR strain Phyllobacterium brassicacearum STM196. New Phytol. 198 514–524

    Not in our library10.1111/nph.12158

  117. 117.

    Knauth S. Hurek T. Brar D. Reinhold-Hurek B. (2005 ). Influence of different Oryza cultivars on expression of nifH gene pools in roots of rice. Environ. Microbiol. 7 1725–1733

    Not in our library10.1111/j.1462-2920.2005.00841.x

  118. 118.

    Kotur Z. Mackenzie N. Ramesh S. Tyerman S. D. Kaiser B. N. Glass A. D. (2012 ). Nitrate transport capacity of the Arabidopsis thaliana NRT2 family members and their interactions with AtNAR2.1. New Phytol. 194 724–731

    Not in our library10.1111/j.1469-8137.2012.04094.x

  119. 119.

    Kovats K. Binder A. Hohl H. R. (1991 ). Cytology of induced systemic resistance of tomato to Phytophthora infestans. Planta 183 491–496

    Not in our library10.1007/bf00194269

  120. 120.

    Kumar V. Sarma M. V. Saharan K. Srivastava R. Kumar L. Sahai V. (2012 ). Effect of formulated root endophytic fungus Piriformospora indica and plant growth promoting rhizobacteria fluorescent pseudomonads R62 and R81 on Vigna mungo. World J. Microbiol. Biotechnol. 28 595–603

    Not in our library10.1007/s11274-011-0852-x

  121. 121.

    Kyselková M. Kopecký J. Frapolli M. Défago G. Ságová-Marečková M. Grundmann G. L. (2009 ). Comparison of rhizobacterial community composition in soil suppressive or conducive to tobacco black root rot disease. ISME J. 3 1127–1138

    Not in our library10.1038/ismej.2009.61

  122. 122.

    Lanteri M. L. Laxalt A. M. Lamattina L. (2008 ). Nitric oxide triggers phosphatidic acid accumulation via phospholipase D during auxin-induced adventitious root formation in cucumber. Plant Physiol. 147 188–198

    Not in our library10.1104/pp.107.111815

  123. 123.

    Lanteri M. L. Pagnussat G. C. Lamattina L. (2006 ). Calcium and calcium-dependent protein kinases are involved in nitric oxide- and auxin-induced adventitious root formation in cucumber. J. Exp. Bot. 57 1341–1351

    Not in our library10.1093/jxb/erj109

  124. 124.

    Lappartient A. G. Touraine B. (1996 ). Demand-driven control of root ATP sulfurylase activity and SO42− uptake in intact canola (the role of phloem-translocated glutathione). Plant Physiol. 111 147–157

    Not in our library10.1104/pp.111.1.147

  125. 125.

    Lappartient A. G. Vidmar J. J. Leustek T. Glass A. D. Touraine B. (1999 ). Inter-organ signaling in plants: regulation of ATP sulfurylase and sulfate transporter genes expression in roots mediated by phloem-translocated compound. Plant J. 18 89–95

    Not in our library10.1046/j.1365-313x.1999.00416.x

  126. 126.

    Lauter F. R. Ninnemann O. Bucher M. Riesmeier J. W. Frommer W. B. (1996 ). Preferential expression of an ammonium transporter and of two putative nitrate transporters in root hairs of tomato. Proc. Natl. Acad. Sci. U.S.A. 93 8139–8144

    Not in our library10.1073/pnas.93.15.8139

  127. 127.

    Lavania M. Chauhan P. S. Chauhan S. V. Singh H. B. Nautiyal C. S. (2006 ). Induction of plant defense enzymes and phenolics by treatment with plant growth-promoting rhizobacteria Serratia marcescens NBRI1213. Curr. Microbiol. 52 363–368

    Not in our library10.1007/s00284-005-5578-2

  128. 128.

    Lee K. H. Larue T. A. (1992 ). Ethylene as a possible mediator of light- and nitrate-induced inhibition of nodulation of Pisum sativum L. cv Sparkle. Plant Physiol. 100 1334–1338

    Not in our library10.1104/pp.100.3.1334

  129. 129.

    Li J. Glick B. R. (2001 ). Transcriptional regulation of the Enterobacter cloacae UW4 1-aminocyclopropane-1-carboxylate (ACC) deaminase gene (acdS). Can. J. Microbiol. 47 359–367

    Not in our library10.1139/cjm-47-4-359

  130. 130.

    Lipton D. S. Blanchar R. W. Blevins D. G. (1987 ). Citrate, malate and succinate concentration in exudates from P-sufficient and P-stresses Medicago sativa L. seedlings. Plant Physiol. 85 315–317

    Not in our library10.1104/pp.85.2.315

  131. 131.

    Liu X. Bimerew M. Ma Y. Muller H. Ovadis M. Eberl L. (2007 ). Quorum-sensing signaling is required for production of the antibiotic pyrrolnitrin in a rhizospheric biocontrol strain of Serratia plymuthica. FEMS Microbiol. Lett. 270 299–305

    Not in our library10.1111/j.1574-6968.2007.00681.x

  132. 132.

    Liu X. Jia J. Popat R. Ortori C. A. Li J. Diggle S. P. (2011 ). Characterisation of two quorum sensing systems in the endophytic Serratia plymuthica strain G3: differential control of motility and biofilm formation according to life-style. BMC Microbiol. 11:26.

    Not in our library10.1186/1471-2180-11-26

  133. 133.

    Lugtenberg B. J. Kamilova F. (2009 ). Plant-growth-promoting rhizobacteria. Annu. Rev. Microbiol. 63 541–556

    Not in our library10.1146/annurev.micro.62.081307.162918

  134. 134.

    Lynch J. M. Whipps J. M. (1990 ). Substrate flow in the rhizosphere. Plant Soil 129 1–10

    Not in our library10.1007/bf00011685

  135. 135.

    Maketon C. Fortuna A. M. Okubara P. A. (2012 ). Cultivar-dependent transcript accumulation in wheat roots colonized by Pseudomonas fluorescens Q8r1-96 wild type and mutant strains. Biol. Control 60 216–224

    Not in our library10.1016/j.biocontrol.2011.11.002

  136. 136.

    Malhotra M. Srivastava S. (2006 ). Targeted engineering of Azospirillum brasilense SM with indole acetamide pathway for indoleacetic acid over-expression. Can. J. Microbiol. 52 1078–1084

    Not in our library10.1139/w06-071

  137. 137.

    Malhotra M. Srivastava S. (2008 ). An ipdC gene knock-out of Azospirillum brasilense strain SM and its implications on indole-3-acetic acid biosynthesis and plant growth promotion. Antonie Van Leeuwenhoek 93 425–433

    Not in our library10.1007/s10482-007-9207-x

  138. 138.

    Manero F. J. Algar E. Martin Gomez M. S. Saco Sierra M. D. Solano B. R. (2003 ). Elicitation of secondary metabolism in Hypericum perforatum by rhizosphere bacteria and derived elicitors in seedlings and shoot cultures. Pharm. Biol. 50 1201–1209

    Not in our library10.3109/13880209.2012.664150

  139. 139.

    Mantelin S. Desbrosses G. Larcher M. Tranbarger T. J. Cleyet-Marel J. C. Touraine B. (2006 ). Nitrate-dependent control of root architecture and N nutrition are altered by a plant growth-promoting Phyllobacterium sp. Planta 223 591–603

    Not in our library10.1007/s00425-005-0106-y

  140. 140.

    Mantelin S. Touraine B. (2004 ). Plant growth-promoting bacteria and nitrate availability: impacts on root development and nitrate uptake. J. Exp. Bot. 55 27–34

    Not in our library10.1093/jxb/erh010

  141. 141.

    Mårtensson L. Dïez B. Wartiainen I. Zheng W. El-Shehawy R. Rasmussen U. (2009 ). Diazotrophic diversity, nifH gene expression and nitrogenase activity in a rice paddy field in Fujian, China. Plant Soil 325 207–218

    Not in our library10.1007/s11104-009-9970-8

  142. 142.

    Masson-Boivin C. Giraud E. Perret X. Batut J. (2009 ). Establishing nitrogen-fixing symbiosis with legumes: how many rhizobium recipes? Trends Microbiol. 17 458–466

    Not in our library10.1016/j.tim.2009.07.004

  143. 143.

    Mazzola M. Funnell D. L. Raaijmakers J. M. (2004 ). Wheat cultivar-specific selection of 2,4-diacetylphloroglucinol-producing fluorescent Pseudomonas species from resident soil populations. Microb. Ecol. 48 338–348

    Not in our library10.1007/s00248-003-1067-y

  144. 144.

    Mazzola M. Gu Y. H. (2002 ). Wheat genotype-specific induction of soil microbial communities suppressive to disease incited by Rhizoctonia solani anastomosis group (AG)-5 and AG-8. Phytopathology 92 1300–1307

    Not in our library10.1094/phyto.2002.92.12.1300

  145. 145.

    Micallef S. A. Shiaris M. P Colón-Carmona A. (2009 ). Influence of Arabidopsis thaliana accessions on rhizobacterial communities and natural variation in root exudates. J. Exp. Bot. 60 1729–1742

    Not in our library10.1093/jxb/erp053

  146. 146.

    Miché L. Battistoni F. Gemmer S. Belghazi M. Reinhold-Hurek B. (2006 ). Upregulation of jasmonate-inducible defense proteins and differential colonization of roots of Oryza sativa cultivars with the endophyte Azoarcus sp. Mol. Plant Microbe Interact. 19 502–511

    Not in our library10.1094/mpmi-19-0502

  147. 147.

    Miller S. H. Browne P. Prigent-Combaret C. Combes-Meynet E. Morrissey J. P O’Gara F. (2009 ). Biochemical and genomic comparison of inorganic phosphate solubilisation in Pseudomonas species. Environ. Microbiol. Rep. 2 403–411

    Not in our library10.1111/j.1758-2229.2009.00105.x

  148. 148.

    Minorsky P. V. (2008 ). On the inside. Plant Physiol. 146 323–324

    Not in our library10.1104/pp.104.900246

  149. 149.
    Aerobic Nitric Oxide Production by Azospirillum brasilense Sp245 and Its Influence on Root Architecture in Tomato · 2008
    Not checked
  150. 150.

    Moubayidin L. Di Mambro R. Sabatini S. (2009 ). Cytokinin-auxin crosstalk. Trends Plant Sci. 14 557–562

    Not in our library10.1016/j.tplants.2009.06.010

  151. 151.

    Nazoa P. Vidmar J. J. Tranbarger T. J. Mouline K. Damiani I. Tillard P. (2003 ). Regulation of the nitrate transporter gene AtNRT2.1 in Arabidopsis thaliana: responses to nitrate, amino acids and developmental stage. Plant Mol. Biol. 52 689–703

    Not in our library10.1023/a:1024899808018

  152. 152.

    Niranjan Raj S. Lavanya S. N. Amruthesh K. N. Niranjana S. R. Reddy M. S. Shetty H. S. (2012 ). Histo-chemical changes induced by PGPR during induction of resistance in pearl millet against downy mildew disease. Biol. Control 60 90–102

    Not in our library10.1016/j.biocontrol.2011.10.011

  153. 153.

    Notz R. Maurhofer M. Dubach H. Haas D Défago G. (2002 ). Fusaric acid-producing strains of Fusarium oxysporum alter 2,4-diacetylphloroglucinol biosynthetic gene expression in Pseudomonas fluorescens CHA0 in vitro and in the rhizosphere of wheat. Appl. Environ. Microbiol. 68 2229–2235

    Not in our library10.1128/aem.68.5.2229-2235.2002

  154. 154.

    Notz R. Maurhofer M. Schnider-Keel U. Duffy B. Haas D Défago G. (2001 ). Biotic factors affecting expression of the 2,4-diacetylphloroglucinol biosynthesis gene phlA in Pseudomonas fluorescens biocontrol strain CHA0 in the rhizosphere. Phytopathology 91 873–881

    Not in our library10.1094/phyto.2001.91.9.873

  155. 155.

    Odum E. P. Barrett G. W. (2005 ). Fundamentals of Ecology, 5th Edn. Belmont, USA: Thomson Brooks/Cole

    Not in our library

  156. 156.

    Okubara P. A. Call D. R. Kwak Y. S. Skinner D. Z. (2010 ). Induction of defense gene homologues in wheat roots during interactions with Pseudomonas fluorescens. Biol. Control 55 118–125

    Not in our library10.1016/j.biocontrol.2010.07.009

  157. 157.

    Ona O. Van Impe J. Prinsen E. Vanderleyden J. (2005 ). Growth and indole-3-acetic acid biosynthesis of Azospirillum brasilense Sp245 is environmentally controlled. FEMS Microbiol. Lett. 246 125–132

    Not in our library10.1016/j.femsle.2005.03.048

  158. 158.

    Orr C. H. James A. Leifert C. Cooper J. M. Cummings S. P. (2011 ). Diversity and activity of free-living nitrogen-fixing bacteria and total bacteria in organic and conventionally managed soils. Appl. Environ. Microbiol. 77 911–919

    Not in our library10.1128/aem.01250-10

  159. 159.

    Overvoorde P. Fukaki H. Beeckman T. (2011 ). Auxin control of root development. Cold Spring Harb. Perspect. Biol. 2 a001537

    Not in our library10.1101/cshperspect.a001537

  160. 160.

    Parniske M. (2008 ). Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat. Rev. Microbiol. 6 763–775

    Not in our library10.1038/nrmicro1987

  161. 161.

    Patten C. L. Glick B. R. (2002 ). Role of Pseudomonas putida indoleacetic acid in development of the host plant root system. Appl. Environ. Microbiol. 68 3795–3801

    Not in our library10.1128/aem.68.8.3795-3801.2002

  162. 162.

    Penrose D. M. Moffatt B. A. Glick B. R. (2001 ). Determination of 1-aminocycopropane-1-carboxylic acid (ACC) to assess the effects of ACC deaminase-containing bacteria on roots of canola seedlings. Can. J. Microbiol. 47 77–80

    Not in our library10.1139/w00-128

  163. 163.

    Perin L. Martínez-Aguilar L. Castro-González R. Estrada-de los Santos P. Cabellos-Avelar T. Guedes H. V. (2006 ). Diazotrophic Burkholderia species associated with field-grown maize and sugarcane. Appl. Environ. Microbiol. 72 3103–3110

    Not in our library10.1128/aem.72.5.3103-3110.2006

  164. 164.

    Perrig D. Boiero M. L. Masciarelli O. A. Penna C. Ruiz O. A. Cassán F. D. (2007 ). Plant-growth-promoting compounds produced by two agronomically important strains of Azospirillum brasilense, and implications for inoculant formulation. Appl. Microbiol. Biotechnol. 75 1143–1150

    Not in our library10.1007/s00253-007-0909-9

  165. 165.

    Phillips D. A. Fox T. C. King M. D. Bhuvaneswari T. V. Teuber L. R. (2004 ). Microbial products trigger amino acid exudation from plant roots. Plant Physiol. 136 2887–2894

    Not in our library10.1104/pp.104.044222

  166. 166.

    Picard C. Bosco M. (2006 ). Heterozygosis drives maize hybrids to select elite 2,4-diacetylphloroglucinol-producing Pseudomonas strains among resident soil populations. FEMS Microbiol. Ecol. 58 193–204

    Not in our library10.1111/j.1574-6941.2006.00151.x

  167. 167.

    Picard C. Frascaroli E. Bosco M. (2004 ). Frequency and biodiversity of 2,4-diacetylphloroglucinol-producing rhizobacteria are differentially affected by the genotype of two maize inbred lines and their hybrid. FEMS Microbiol. Ecol. 49 207–215

    Not in our library10.1016/j.femsec.2004.03.016

  168. 168.

    Piccoli P. Bottini R. (1994 ). Effects of C/N ratio, N-content, pH, and incubation time on growth and gibberellin production by Azospirillum lipoferum. Symbiosis 17 229–236

    Not in our library

  169. 169.

    Pierson E. A. Wood D. W. Cannon J. A. Blachere F. M Pierson L. S. III (1998 ). Interpopulation signaling via N-acyl-homoserine lactones among bacteria in the wheat rhizosphere. Mol. Plant Microbe Interact. 11 1078–1084

    Not in our library10.1094/mpmi.1998.11.11.1078

  170. 170.

    Pierson L. S. III Keppenne V. D. Wood D. W. (1994 ). Phenazine antibiotic biosynthesis in Pseudomonas aureofaciens 30-84 is regulated by PhzR in response to cell density. J. Bacteriol. 176 3966–3974

    Not in our library10.1128/jb.176.13.3966-3974.1994

  171. 171.

    Pieterse C. M. Leon-Reyes A. Van der Ent S Van Wees S. C. (2009 ). Networking by small-molecule hormones in plant immunity. Nat. Chem. Biol. 5 308–316

    Not in our library10.1038/nchembio.164

  172. 172.

    Pieterse C. M. Van Pelt J. A. Ton J. Parchmann S. Mueller M. J. Buchala A. J. (2000 ). Rhizobacteria-mediated induced systemic resistance (ISR) in Arabidopsis requires sensitivity to jasmonate and ethylene but is not accompanied by an increase in their production. Physiol. Mol. Plant Pathol. 57 123–134

    Not in our library10.1006/pmpp.2000.0291

  173. 173.

    Pieterse C. M. van Wees S. C. Hoffland E. van Pelt J. A van Loon L. C. (1996 ). Systemic resistance in Arabidopsis induced by biocontrol bacteria is independent of salicylic acid accumulation and pathogenesis-related gene expression. Plant Cell 8 1225–1237

    Not in our library10.1105/tpc.8.8.1225

  174. 174.

    Pieterse C. M. van Wees S. C. van Pelt J. A. Knoester M. Laan R. Gerrits H. (1998 ). A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10 1571–1580

    Not in our library10.1105/tpc.10.9.1571

  175. 175.

    Poly F. Jocteur-Monrozier L. Bally R. (2001 ). Improvement in the RFLP procedure for studying the diversity of nifH genes in communities of nitrogen fixers in soil. Res. Microbiol. 152 95–103

    Not in our library10.1016/s0923-2508(00)01172-4

  176. 176.

    Pothier J. F. Prigent-Combaret C. Haurat J. Mënne-Loccoz Y Wisniewski-Dyé F. (2008 ). Duplication of plasmid-borne nitrite reductase gene nirK in the wheat-associated plant growth-promoting rhizobacterium Azospirillum brasilense Sp245. Mol. Plant Microbe Interact. 21 831–842

    Not in our library10.1094/mpmi-21-6-0831

  177. 177.

    Pothier J. F. Wisniewski-Dyé F. Weiss-Gayet M. Mënne-Loccoz Y. Prigent-Combaret C. (2007 ). Promoter-trap identification of wheat seed extract-induced genes in the plant-growth-promoting rhizobacterium Azospirillum brasilense Sp245. Microbiology 153 3608–3622

    Not in our library10.1099/mic.0.2007/009381-0

  178. 178.

    Pozo M. J. Van Der Ent S. Van Loon L. C. Pieterse C. M. (2008 ). Transcription factor MYC2 is involved in priming for enhanced defense during rhizobacteria-induced systemic resistance in Arabidopsis thaliana. New Phytol. 180 511–523

    Not in our library10.1111/j.1469-8137.2008.02578.x

  179. 179.

    Prigent-Combaret C. Blaha D. Pothier J. F. Vial L. Poirier M. A. Wisniewski-Dyé F. (2008 ). Physical organization and phylogenetic analysis of acdR as leucine-responsive regulator of the 1-aminocyclopropane-1-carboxylate deaminase gene acdS in phytobeneficial Azospirillum lipoferum 4B and other proteobacteria. FEMS Microbiol. Ecol. 65 202–219

    Not in our library10.1111/j.1574-6941.2008.00474.x

  180. 180.

    Ramaekers L. Remans R. Rao I. M. Blair M. W. Vanderleyden J. (2010 ). Strategies for improving phosphorus acquisition efficiency of crop plants. Field Crops Res. 117 169–176

    Not in our library10.1016/j.fcr.2010.03.001

  181. 181.

    Ramos-Solano B. Algar E. Garcia-Villaraco A. Garcia-Cristobal J. Garcia J. A. L. Gutierrez-Manero F. J. (2010 ). Biotic elicitation of isoflavone metabolism with plant growth promoting rhizobacteria in early stages of development in Glycine max var. Osumi. J. Agric. Food Chem. 58 1484–1492

    Not in our library10.1021/jf903299a

  182. 182.

    Raynaud X. Jaillard B. Leadley P. W. (2008 ). Plants may alter competition by modifying nutrient bioavailability in rhizosphere: a modeling approach. Am. Nat. 171 44–58

    Not in our library10.1086/523951

  183. 183.

    Remans R. Beebe S. Blair M. Manrique G. Tovar E. Rao I. M. (2008 ). Physiological and genetic analysis of root responsiveness to auxin-producing plant growth-promoting bacteria in common bean (Phaseolus vulgaris L.). Plant Soil 302 149–161

    Not in our library10.1007/s11104-007-9462-7

  184. 184.

    Ribaudo C. M. Krumpholz E. M. Cassán F. D. Bottini R. Cantore M. L. Cura J. A. (2006 ). Azospirillum sp. promotes root hair development in tomato plants through a mechanism that involves ethylene. J. Plant Growth Reg. 25 175–185

    Not in our library10.1007/s00344-005-0128-5

  185. 185.

    Richardson A. E. Baréa J. M. McNeill A. M. Prigent-Combaret C. (2009 ). Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321 305–339

    Not in our library10.1007/s11104-009-9895-2

  186. 186.

    Richardson A. E. Simpson R. J. (2011 ). Soil microorganisms mediating phosphorus availability update on microbial phosphorus. Plant Physiol. 156 989–996

    Not in our library10.1104/pp.111.175448

  187. 187.

    Riefler M. Novak O. Strnad M Schmülling T. (2006 ). Arabidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development, and cytokinin metabolism. Plant Cell 18 40–54

    Not in our library10.1105/tpc.105.037796

  188. 188.
    Combination of Fluorescent Reporters for Simultaneous Monitoring of Root Colonization and Antifungal Gene Expression by a Biocontrol Pseudomonad on Cereals with Flow Cytometry · 2010
    Not checked
  189. 189.

    Roesch L. F. W. Camargo F. A. O. Bento F. M. Triplett E. W. (2007 ). Biodiversity of diazotrophic bacteria within the soil, root and stem of field-grown maize. Plant Soil 302 91–104

    Not in our library10.1007/s11104-007-9458-3

  190. 190.

    Rothballer M. Schmid M. Fekete A. Hartmann A. (2005 ). Comparative in situ analysis of ipdC-gfpmut3 promoter fusions of Azospirillum brasilense strains Sp7 and Sp245. Environ. Microbiol. 7 1839–1846

    Not in our library10.1111/j.1462-2920.2005.00848.x

  191. 191.

    Rus A. Yokoi S. Sharkhuu A. Reddy M. Lee B. H. Matsumoto T. K. (2001 ). AtHKT1 is a salt tolerance determinant that controls Na+ entry into plant roots. Proc. Natl. Acad. Sci. U.S.A. 98 14150–14155

    Not in our library10.1073/pnas.241501798

  192. 192.

    Ryan A. D. Kinkel L. L. Schottel J. L. (2004 ). Effect of pathogen isolate, potato cultivar, and antagonist strain on potato scab severity and biological control. Biol. Sci. Technol. 14 301–311

    Not in our library

  193. 193.

    Ryu C. M. Farag M. A. Hu C. H. Reddy M. S. Wei H. X. Pare P. W. (2003 ). Bacterial volatiles promote growth in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 100 4927–4932

    Not in our library10.1073/pnas.0730845100

  194. 194.

    Saharan B. S. Nehra V. (2011 ). Plant growth promoting rhizobacteria: a critical review. Life Sci. Med. Res. 21 1–30

    Not in our library

  195. 195.

    Salamini F. Ozkan H. Brandolini A. Schafer-Pregl R. Martin W. (2002 ). Genetics and geography of wild cereal domestication in the near east. Nat. Rev. Genet. 3 429–441

    Not in our library10.1038/nrg817

  196. 196.

    Scheres B. Benfey P. Dolan L. (2002 ). Root development. Arabidopsis Book 1 e0101

    Not in our library10.1199/tab.0101

  197. 197.

    Sekar C. Prasad N. N. Sundaram M. D. (2000 ). Enhancement of polygalacturonase activity during auxin induced para nodulation and endorhizosphere colonization of Azospirillum in rice roots. Indian J. Exp. Biol. 38 80–83

    Not in our library

  198. 198.

    Selvaraj T. Rajeshkumar S. Nisha M. C. Wondimu L. Tesso M. (2008 ). Effect of Glomus mosseae and plant growth promoting rhizomicroorganisms (PGPR's) on growth, nutrients and content of secondary metabolites in Begonia malabarica Lam. Maejo Int. J. Sci. Technol. 2 516–525

    Not in our library

  199. 199.

    Shaw L. J. Morris P. Hooker J. E. (2006 ). Perception and modification of plant flavonoid signals by rhizosphere microorganisms. Environ. Microbiol. 8 1867–1880

    Not in our library10.1111/j.1462-2920.2006.01141.x

  200. 200.

    Shukla K. P. Sharma S. Singh N. K. Singh V. Tiwari K. Singh S. (2011 ). Nature and role of root exudates: efficacy in bioremediation. Afr. J. Biotechnol. 10 9717–9724

    Not in our library

  201. 201.

    Silverman F. P. Assiamah A. A. Bush D. S. (1998 ). Membrane transport and cytokinin action in root hairs of Medicago sativa. Planta 205 23–31

    Not in our library10.1007/s004250050292

  202. 202.

    Smith K. P. Goodman R. M. (1999 ). Host variation for interactions with beneficial plant-associated microbes. Annu. Rev. Phytopathol. 37 473–491

    Not in our library10.1146/annurev.phyto.37.1.473

  203. 203.

    Somers E. Ptacek D. Gysegom P. Srinivasan M. Vanderleyden J. (2005 ). Azospirillum brasilense produces the auxin-like phenylacetic acid by using the key enzyme for indole-3-acetic acid biosynthesis. Appl. Environ. Microbiol. 71 1803–1810

    Not in our library10.1128/aem.71.4.1803-1810.2005

  204. 204.

    Sondergaard T. E. Schulz A. Palmgren M. G. (2004 ). Energization of transport processes in plants. Roles of the plasma membrane H+-ATPase. Plant Physiol. 136 2475–2482

    Not in our library10.1104/pp.104.048231

  205. 205.

    Spaepen S. Vanderleyden J. Remans R. (2007a ). Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol. Rev. 31 425–448

    Not in our library10.1111/j.1574-6976.2007.00072.x

  206. 206.

    Spaepen S. Versees W. Gocke D. Pohl M. Steyaert J. Vanderleyden J. (2007b ). Characterization of phenylpyruvate decarboxylase, involved in auxin production of Azospirillum brasilense. J. Bacteriol. 189 7626–7633

    Not in our library10.1128/jb.00830-07

  207. 207.

    Srivastava S. Chaudhry V. Mishra A. Chauhan P. S. Rehman A. Yadav A. (2012 ). Gene expression profiling through microarray analysis in Arabidopsis thaliana colonized by Pseudomonas putida MTCC5279, a plant growth promoting rhizobacterium. Plant Signal. Behav. 7 235–245

    Not in our library10.4161/psb.18957

  208. 208.

    Steidle A. Sigl K. Schuhegger R. Ihring A. Schmid M. Gantner S. (2001 ). Visualization of N-acylhomoserine lactone-mediated cell–cell communication between bacteria colonizing the tomato rhizosphere. Appl. Environ. Microbiol. 67 5761–5770

    Not in our library10.1128/aem.67.12.5761-5770.2001

  209. 209.

    Stepanova A. N. Alonso J. M. (2009 ). Ethylene signaling and response: where different regulatory modules meet. Curr. Opin. Plant Biol. 12 548–555

    Not in our library10.1016/j.pbi.2009.07.009

  210. 210.

    Strömberg A. Brishammar S. (1993 ). A histological evaluation of induced resistance to Phytophthora infestans (Mont.) de Bary in potato leaves. J. Phytopathol. 137 15–25

    Not in our library10.1111/j.1439-0434.1993.tb01321.x

  211. 211.

    Subramoni S. Gonzalez J. F. Johnson A. Pechy-Tarr M. Rochat L. Paulsen I. (2011 ). Bacterial subfamily of LuxR regulators that respond to plant compounds. Appl. Environ. Microbiol. 77 4579–4588

    Not in our library10.1128/aem.00183-11

  212. 212.

    Suzuki S. He Y. Oyaizu H. (2003 ). Indole-3-acetic acid production in Pseudomonas fluorescens HP72 and its association with suppression of creeping bentgrass brown patch. Curr. Microbiol. 47 138–143

    Not in our library10.1007/s00284-002-3968-2

  213. 213.

    Tak H. I. Ahmad F. Babalola O. O. (2013 ). “Advances in the application of plant growth-promoting rhizobacteria in phytoremediation of heavy metals,” in Vol. 223, Reviews of Environmental Contamination and Toxicology ed. Whitacre D. M. (New York: Springer Science Business Media) 33–52

    Not in our library10.1007/978-1-4614-5577-6_2

  214. 214.

    Teplitski M. Robinson J. B. Bauer W. D. (2000 ). Plants secrete substances that mimic bacterial N-acyl homoserine lactone signal activities and affect population density-dependent behaviors in associated bacteria. Mol. Plant Microbe Interact. 13 637–648

    Not in our library10.1094/mpmi.2000.13.6.637

  215. 215.

    Theocharis A. Bordiec S. Fernandez O. Paquis S. Dhondt-Cordelier S. Baillieul F. (2012 ). Burkholderia phytofirmans PsJN primes Vitis vinifera L. and confers a better tolerance to low nonfreezing temperatures. Mol. Plant Microbe Interact. 25 241–249

    Not in our library10.1094/mpmi-05-11-0124

  216. 216.

    Thuler D. S. Floh E. I. Handro W. Barbosa H. R. (2003 ). Plant growth regulators and amino acids released by Azospirillum sp. in chemically defined media. Lett. Appl. Microbiol. 37 174–178

    Not in our library10.1046/j.1472-765x.2003.01373.x

  217. 217.

    Timmusk S. Nicander B. Granhall U. Tillberg E. (1999 ). Cytokinin production by Paenibacillus polymyxa. Soil Biol. Biochem. 31 1847–1852

    Not in our library10.1016/s0038-0717(99)00113-3

  218. 218.

    Touraine B. (2004 ). “Nitrate uptake by roots – transporters and root development,” in Nitrogen Acquisition and Assimilation in Higher Plants eds De Kok L. J. Stulen I. (Dordrecht: Kluwer Academic Publishers) 1–34

    Not in our library10.1007/978-1-4020-2728-4_1

  219. 219.

    Turk K. A. Rees A. P. Zehr J. P. Pereira N. Swift P. Shelley R. (2011 ). Nitrogen fixation and nitrogenase (nifH) expression in tropical waters of the eastern North Atlantic. ISME J. 5 1201–1212

    Not in our library10.1038/ismej.2010.205

  220. 220.

    Ulmasov T. Murfett J. Hagen G. Guilfoyle T. J. (1997 ). Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9 1963–1971

    Not in our library10.1105/tpc.9.11.1963

  221. 221.

    Upadhyay S. K. Singh D. P. Saikia R. (2009 ). Genetic diversity of plant growth promoting rhizobacteria isolated from rhizospheric soil of wheat under saline condition. Curr. Microbiol. 59 489–496

    Not in our library10.1007/s00284-009-9464-1

  222. 222.

    van de Mortel J. E. de Vos R. C. Dekkers E. Pineda A. Guillod L. Bouwmeester K. (2012 ). Metabolic and transcriptomic changes induced in Arabidopsis by the rhizobacterium Pseudomonas fluorescens SS101. Plant Physiol. 160 2173–2188

    Not in our library10.1104/pp.112.207324

  223. 223.

    Vandeputte O. M. Kiendrebeogo M. Rajaonson S. Diallo B. Mol A. El Jaziri M. (2010 ). Identification of catechin as one of the flavonoids from Combretum albiflorum bark extract that reduces the production of quorum-sensing-controlled virulence factors in Pseudomonas aeruginosa PAO1. Appl. Environ. Microbiol. 76 243–253

    Not in our library10.1128/aem.01059-09

  224. 224.

    Van der Ent S. Verhagen B. W. Van Doorn R. Bakker D. Verlaan M. G. Pel M. J. (2008 ). MYB72 is required in early signaling steps of rhizobacteria-induced systemic resistance in Arabidopsis. Plant Physiol. 146 1293–1304

    Not in our library10.1104/pp.107.113829

  225. 225.

    van Overbeek L. van Elsas J. D. (2008 ). Effects of plant genotype and growth stage on the structure of bacterial communities associated with potato (Solanum tuberosum L.). FEMS Microbiol. Ecol. 64 283–296

    Not in our library10.1111/j.1574-6941.2008.00469.x

  226. 226.

    Vargas L. Gurjao de Carvalho T. L. Gomes Ferreira P. C. Baldani V. L. Baldani J. I. Hemerly A. S. (2012 ). Early responses of rice (Oryza sativa L.) seedlings to inoculation with beneficial diazotrophic bacteria are dependent on plant and bacterial genotypes. Plant Soil 356 127–137

    Not in our library10.1007/s11104-012-1274-8

  227. 227.

    Vaughan D. A. Lu B.-R. Tomooka N. (2008 ). The evolving story of rice evolution. Plant Sci. 174 394–408

    Not in our library10.1016/j.plantsci.2008.01.016

  228. 228.

    Veresoglou S. D. Menexes G. (2010 ). Impact of inoculation with Azospirillum spp. on growth properties and seed yield of wheat: a meta-analysis of studies in the ISI Web of Science from 1981 to 2008. Plant Soil 337 469–480

    Not in our library10.1007/s11104-010-0543-7

  229. 229.

    Verhagen B. W. Glazebrook J. Zhu T. Chang H. S. van Loon L. C. Pieterse C. M. (2004 ). The transcriptome of rhizobacteria-induced systemic resistance in Arabidopsis. Mol. Plant Microbe Interact. 17 895–908

    Not in our library10.1094/mpmi.2004.17.8.895

  230. 230.

    Vessey J. K. (2003 ). Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255 571–586

    Not in our library10.1023/a:1026037216893

  231. 231.

    Vial L. Cuny C. Gluchoff-Fiasson K. Comte G. Oger P. M. Faure D. (2006 ). N-acyl-homoserine lactone-mediated quorum-sensing in Azospirillum: an exception rather than a rule. FEMS Microbiol. Ecol. 58 155–168

    Not in our library10.1111/j.1574-6941.2006.00153.x

  232. 232.

    von Wiren N. Lauter F. R. Ninnemann O. Gillissen B. Walch-Liu P. Engels C. (2000 ). Differential regulation of three functional ammonium transporter genes by nitrogen in root hairs and by light in leaves of tomato. Plant J. 21 167–175

    Not in our library10.1046/j.1365-313x.2000.00665.x

  233. 233.

    Walker V. Bertrand C. Bellvert F. Mënne-Loccoz Y. Bally R. Comte G. (2011 ). Host plant secondary metabolite profiling shows a complex, strain-dependent response of maize to plant growth-promoting rhizobacteria of the genus Azospirillum. New Phytol. 189 494–506

    Not in our library10.1111/j.1469-8137.2010.03484.x

  234. 234.

    Walker V. Couillerot O. Von Felten A. Bellvert F. Jansa J. Maurhofer M. (2012 ). Variation of secondary metabolite levels in maize seedling roots induced by inoculation with Azospirillum, Pseudomonas and Glomus consortium under field conditions. Plant Soil 356 151–163

    Not in our library10.1007/s11104-011-0960-2

  235. 235.
    Microarray Analysis of the Gene Expression Profile Induced by the Endophytic Plant Growth-Promoting Rhizobacteria, Pseudomonas fluorescens FPT9601-T5 in Arabidopsis · 2005
    Not checked
  236. 236.

    Weller D. M. Mavrodi D. V. van Pelt J. A. Pieterse C. M. van Loon L. C. Bakker P. A. (2012 ). Induced systemic resistance in Arabidopsis thaliana against Pseudomonas syringae pv. tomato by 2,4-diacetylphloroglucinol-producing Pseudomonas fluorescens. Phytopathology 102 403–412

    Not in our library10.1094/phyto-08-11-0222

  237. 237.

    Wright J. P. Jones C. G. (2006 ). The concept of organisms as ecosystem engineers ten years on: progress, limitations, and challenges. BioScience 56 203–209

    Not in our library10.1641/0006-3568(2006)056[0203:tcooae]2.0.co;2

  238. 238.

    Wu L. Ma K. Lu Y. (2009 ). Prevalence of betaproteobacterial sequences in nifH gene pools associated with roots of modern rice cultivars. Microb. Ecol. 57 58–68

    Not in our library10.1007/s00248-008-9403-x

  239. 239.

    Yang S. F. Hoffman N. E. (1984 ). Ethylene biosynthesis and its regulation in higher plants. Annu. Rev. Plant Physiol. 35 155–189

    Not in our library10.1146/annurev.pp.35.060184.001103

  240. 240.

    Yaxley J. R. Ross J. J. Sherriff L. J. Reid J. B. (2001 ). Gibberellin biosynthesis mutations and root development in pea. Plant Physiol. 125 627–633

    Not in our library10.1104/pp.125.2.627

  241. 241.

    Zakharova E. A. Iosipenko A. D. Ignatov V. V. (2000 ). Effect of water-soluble vitamins on the production of indole-3-acetic acid by Azospirillum brasilense. Microbiol. Res. 155 209–214

    Not in our library10.1016/s0944-5013(00)80034-8

  242. 242.

    Zamioudis C. Mastranesti P. Dhonukshe P. Blilou I. Pieterse C. M. (2013 ). Unraveling root developmental programs initiated by beneficial Pseudomonas spp. bacteria. Plant Physiol. 162 304–318

    Not in our library10.1104/pp.112.212597

  243. 243.

    Zhang H. Kim M. S. Krishnamachari V. Payton P. Sun Y. Grimson M. (2007 ). Rhizobacterial volatile emissions regulate auxin homeostasis and cell expansion in Arabidopsis. Planta 226 839–851

    Not in our library10.1007/s00425-007-0530-2

  244. 244.

    Zhang H. Kim M. S. Sun Y. Dowd S. E. Shi H Paré P. W. (2008 ). Soil bacteria confer plant salt tolerance by tissue-specific regulation of the sodium transporter HKT1. Mol. Plant Microbe Interact. 21 737–744

    Not in our library10.1094/mpmi-21-6-0737

  245. 245.

    Zhang H. Murzello C. Sun Y. Kim M. S. Xie X. Jeter R. M. (2010 ). Choline and osmotic-stress tolerance induced in Arabidopsis by the soil microbe Bacillus subtilis (GB03). Mol. Plant Microbe Interact. 23 1097–1104

    Not in our library10.1094/mpmi-23-8-1097

  246. 246.

    Zhang H. Sun Y. Xie X. Kim M. S. Dowd S. E. Pare P. W. (2009 ). A soil bacterium regulates plant acquisition of iron via deficiency-inducible mechanisms. Plant J. 58 568–577

    Not in our library10.1111/j.1365-313x.2009.03803.x

  247. 247.

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

    Not in our library10.1016/j.envint.2006.12.005

Cited by papers we hold 20

Reads

Read by people on this page

None yet.

Checked or read by AI through naulon

None yet.

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.

Are you an author?

Is this your paper?

Claim it to add your note and be paid when agents cite it. Free.