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Use of Plant Growth-Promoting Bacteria for Biocontrol of Plant Diseases: Principles, Mechanisms of Action, and Future Prospects

Stéphane Compant, Brion Duffy, Jerzy Nowak, Christophe Clément, Essaïd Ait Barka
Stéphane Compant
1Laboratoire de Stress, Défenses et Reproduction des Plantes, Unité de Recherche Vignes et Vins de Champagne, UPRES EA 2069, UFR Sciences, Université de Reims Champagne-Ardenne, 51687 Reims Cedex 2, France
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Brion Duffy
2Agroscope FAW Wädenswil, Swiss Federal Research Institute for Fruit Production, Viticulture, and Horticulture, CH-8820 Wädenswil, Switzerland
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Jerzy Nowak
3Department of Horticulture, Virginia Polytechnic Institute and State University, 0327-301 Saunders Hall, Blacksburg, Virginia 24060
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Christophe Clément
1Laboratoire de Stress, Défenses et Reproduction des Plantes, Unité de Recherche Vignes et Vins de Champagne, UPRES EA 2069, UFR Sciences, Université de Reims Champagne-Ardenne, 51687 Reims Cedex 2, France
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Essaïd Ait Barka
1Laboratoire de Stress, Défenses et Reproduction des Plantes, Unité de Recherche Vignes et Vins de Champagne, UPRES EA 2069, UFR Sciences, Université de Reims Champagne-Ardenne, 51687 Reims Cedex 2, France
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  • For correspondence: ea.barka@univ-reims.fr
DOI: 10.1128/AEM.71.9.4951-4959.2005
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Pathogenic microorganisms affecting plant health are a major and chronic threat to food production and ecosystem stability worldwide. As agricultural production intensified over the past few decades, producers became more and more dependent on agrochemicals as a relatively reliable method of crop protection helping with economic stability of their operations. However, increasing use of chemical inputs causes several negative effects, i.e., development of pathogen resistance to the applied agents and their nontarget environmental impacts (44, 62). Furthermore, the growing cost of pesticides, particularly in less-affluent regions of the world, and consumer demand for pesticide-free food has led to a search for substitutes for these products. There are also a number of fastidious diseases for which chemical solutions are few, ineffective, or nonexistent (62). Biological control is thus being considered as an alternative or a supplemental way of reducing the use of chemicals in agriculture (44, 62, 136, 188).

There has been a large body of literature describing potential uses of plant associated bacteria as agents stimulating plant growth and managing soil and plant health (reviewed in references 63, 70, 143, 165, and 188). Plant growth-promoting bacteria (PGPB) (8) are associated with many, if not all, plant species and are commonly present in many environments. The most widely studied group of PGPB are plant growth-promoting rhizobacteria (PGPR) (82) colonizing the root surfaces and the closely adhering soil interface, the rhizosphere (82, 84). As reviewed by Kloepper et al. (84) or, more recently, by Gray and Smith (65), some of these PGPR can also enter root interior and establish endophytic populations. Many of them are able to transcend the endodermis barrier, crossing from the root cortex to the vascular system, and subsequently thrive as endophytes in stem, leaves, tubers, and other organs (10, 28, 65, 70). The extent of endophytic colonization of host plant organs and tissues reflects the ability of bacteria to selectively adapt to these specific ecological niches (65, 70). Consequently, intimate associations between bacteria and host plants can be formed (28, 70, 84) without harming the plant (70, 83, 84, 92, 191). Although, it is generally assumed that many bacterial endophyte communities are the product of a colonizing process initiated in the root zone (102, 165, 177, 188), they may also originate from other source than the rhizosphere, such as the phyllosphere, the anthosphere, or the spermosphere (70).

Despite their different ecological niches, free-living rhizobacteria and endophytic bacteria use some of the same mechanisms to promote plant growth and control phytopathogens (15, 46, 63, 70, 92, 165). The widely recognized mechanisms of biocontrol mediated by PGPB are competition for an ecological niche or a substrate, production of inhibitory allelochemicals, and induction of systemic resistance (ISR) in host plants to a broad spectrum of pathogens (15, 63, 66, 67, 97, 146) and/or abiotic stresses (reviewed in references 101 and 117). This review surveys the advances of plant-PGPB interaction research focusing on the principles and mechanisms of action of PGPB, both free-living and endophytic bacteria, and their use or potential use for the biological control of plant diseases.

COMPETITIVE ROOT COLONIZATION

Despite their potential as low-input practical agents of plant protection, application of PGPB has been hampered by inconsistent performance in field tests (167); this is usually attributed to their poor rhizosphere competence (153, 189). Rhizosphere competence of biocontrol agents comprises effective root colonization combined with the ability to survive and proliferate along growing plant roots over a considerable time period, in the presence of the indigenous microflora (95, 127, 189, 190). Given the importance of rhizosphere competence as a prerequisite of effective biological control, understanding root-microbe communication (6, 135), as affected by genetic (80, 118) and environmental (128) determinants in spatial (6) and temporal (23) contexts, will significantly contribute to improve the efficacy of these biocontrol agents.

Competition for root niches and bacterial determinants directly involves root colonization.The root surface and surrounding rhizosphere are significant carbon sinks (143). Photosynthate allocation to this zone can be as high as 40% (34). Thus, along root surfaces there are various suitable nutrient-rich niches attracting a great diversity of microorganisms, including phytopathogens. Competition for these nutrients and niches is a fundamental mechanism by which PGPB protect plants from phytopathogens (50). PGPB reach root surfaces by active motility facilitated by flagella and are guided by chemotactic responses (41, 42, 112, 162, 171, 172). Known chemical attractants present in root exudates include organic acids, amino acids, and specific sugars (188). Some exudates can also be effective as antimicrobial agents and thus give ecological niche advantage to organisms that have adequate enzymatic machinery to detoxify them (reviewed in reference 6). The quantity and composition of chemoattractants and antimicrobials exuded by plant roots are under genetic and environmental control (6). This implies that PGPB competence highly depends either on their abilities to take advantage of a specific environment or on their abilities to adapt to changing conditions. As an example, Azospirillum chemotaxis is induced by sugars, amino acids, and organic acids, but the degree of chemotactic response to each of these compounds differs among strains (142). PGPB may be uniquely equipped to sense chemoattractants, e.g., rice exudates induce stronger chemotactic responses of endophytic bacteria than from non-PGPB present in the rice rhizosphere (5).

Bacterial lipopolysaccharides (LPS), in particular the O-antigen chain, can also contribute to root colonization (35). However, the importance of LPS in this colonization might be strain dependent since the O-antigenic side chain of Pseudomonas fluorescens WCS374 does not contribute to potato root adhesion (43), whereas the O-antigen chain of P. fluorescens PCL1205 is involved in tomato root colonization (35). Furthermore, the O-antigenic aspect of LPS does not contribute to rhizoplane colonization of tomato by the plant beneficial endophytic bacterium P. fluorescens WCS417r but, interestingly, this bacterial determinant was involved in endophytic colonization of roots (57).

It has also been recently demonstrated that the high bacterial growth rate and ability to synthesize vitamin B1 and exude NADH dehydrogenases contribute to plant colonization by PGPB (35, 157). Another determinant of root colonization ability by bacteria is type IV pili, better known for its involvement in the adhesion of animal and human pathogenic bacteria to eukaryotic cells (69, 162, 163). The type IV pili also play a role in plant colonization by endophytic bacteria such as Azoarcus sp. (49, 162).

Root colonization and site-specific recombinase.Bacterial traits required for effective root colonization are subject to phase variation, a regulatory process for DNA rearrangements orchestrated by site-specific recombinase (36, 149, 174). In certain PGPB, efficient root colonization is linked to their ability to secrete a site-specific recombinase (36). Transfer of the site-specific recombinase gene from a rhizosphere-competent P. fluorescens into a rhizosphere-incompetent Pseudomonas strain enhanced its ability to colonize root tips (37).

Utilization of root exudates and root mucilage by PGPB.Since root exudates are the primary source of nutrients for rhizosphere microorganisms (143, 176), rhizosphere competence implies that PGPB are well adapted to their utilization (96). Despite the fact that sugars have often been reported as the major carbon source in exudates, the ability to use specific sugars does not play a major role in tomato root colonization (96). Similarly, although amino acids are present in root exudates, the bioavailability of amino acids alone is considered insufficient to support root tip colonization by auxotrophic mutants of P. fluorescens WCS365 (158). In contrast, Simons et al. (158) reported that amino acid synthesis is required for root colonization by P. fluorescens WCS365, indicating that amino acid prototrophy is involved in rhizosphere competence. In addition, PGPB regulate the rate of uptake of polyamines such as putrescine, spermine, and spermidine, since their high titer could retard bacterial growth and reduce their ability to competitively colonize roots (87). Root mucilage also offers a utilizable carbon source for PGPB (85) to use for the competitive colonization.

BIOCONTROL ACTIVITY MEDIATED BY THE SYNTHESIS OF ALLELOCHEMICALS

Offensive PGPB colonization and defensive retention of rhizosphere niches are enabled by production of bacterial allelochemicals, including iron-chelating siderophores, antibiotics, biocidal volatiles, lytic enzymes, and detoxification enzymes (6, 63, 166).

Competition for iron and the role of siderophores.Iron is an essential growth element for all living organisms. The scarcity of bioavailable iron in soil habitats and on plant surfaces foments a furious competition (93). Under iron-limiting conditions PGPB produce low-molecular-weight compounds called siderophores to competitively acquire ferric ion (191). Although various bacterial siderophores differ in their abilities to sequester iron, in general, they deprive pathogenic fungi of this essential element since the fungal siderophores have lower affinity (94, 122). Some PGPB strains go one step further and draw iron from heterologous siderophores produced by cohabiting microorganisms (19, 92, 94, 137, 186, 191).

Siderophore biosynthesis is generally tightly regulated by iron-sensitive Fur proteins, the global regulators GacS and GacA, the sigma factors RpoS, PvdS, and FpvI, quorum-sensing autoinducers such as N-acyl homoserine lactone, and site-specific recombinases (31, 141). However, some data demonstrate that none of these global regulators is involved in siderophore production. Neither GacS nor RpoS significantly affected the level of siderophores synthesized by Enterobacter cloacae CAL2 and UW4 (148). RpoS is not involved in the regulation of siderophore production by Pseudomonas putida strain WCS358 (86). In addition, GrrA/GrrS, but not GacS/GacA, are involved in siderophore synthesis regulation in Serratia plymuthica strain IC1270, suggesting that gene evolution occurred in the siderophore-producing bacteria (123). A myriad of environmental factors can also modulate siderophores synthesis, including pH, the level of iron and the form of iron ions, the presence of other trace elements, and an adequate supply of carbon, nitrogen, and phosphorus (52).

Antibiosis.The basis of antibiosis as a biocontrol mechanism of PGPB has become increasingly better understood over the past two decades (191). A variety of antibiotics have been identified, including compounds such as amphisin, 2,4-diacetylphloroglucinol (DAPG), hydrogen cyanide, oomycin A, phenazine, pyoluteorin, pyrrolnitrin, tensin, tropolone, and cyclic lipopeptides produced by pseudomonads (33, 40, 114, 115, 138) and oligomycin A, kanosamine, zwittermicin A, and xanthobaccin produced by Bacillus, Streptomyces, and Stenotrophomonas spp. (72, 81, 103, 104, 110). Interestingly, some antibiotics produced by PGPB are finding new uses as experimental pharmaceuticals (45, 75, 192), and this group of bacteria may offer an untapped resource for compounds to deal with the alarming ascent of multidrug-resistant human pathogenic bacteria.

Regulatory cascades of these antibiotics involve GacA/GacS or GrrA/GrrS, RpoD, and RpoS, N-acyl homoserine lactone derivatives (15, 21, 68, 131) and positive autoregulation (17, 151). Antibiotic synthesis is tightly linked to the overall metabolic status of the cell, which in turn is dictated by nutrient availability and other environmental stimuli (167), such as major and minor minerals, type of carbon source and supply, pH, temperature, and other parameters (11, 51, 52, 61, 78, 103, 104, 124, 125). Trace elements, particularly zinc, and carbon source levels influence the genetic stability/instability of bacteria, affecting their ability to produce secondary metabolites (53). It is important to note that many strains produce pallet of secondary antimicrobial metabolites and that conditions favoring one compound may not favor another (52). Thus, the varied arsenal of biocontrol strains may enable antagonists to perform their ultimate objective of pathogen suppression under the widest range of environmental conditions. For example, in P. fluorescens CHA0 biosynthesis of DAPG is stimulated and pyoluteorin is repressed in the presence of glucose as a carbon source. As glucose is depleted, however, pyoluteorin becomes the more abundantly antimicrobial compound produced by this strain (52). This ensures a degree of flexibility for the antagonist when confronted with a different or a changeable environment. Biotic conditions can also influence antibiotic biosynthesis (51, 54, 68, 116, 128). For example bacterial metabolites salicylates and pyoluteorin can affect DAPG production by P. fluorescens CHA0 (151). Furthermore, plant growth and development also influence antiobiotic production, since biological activity of DAPG producers is not induced by the exudates of young plant roots but is induced by the exudates of older plants, which results in selective pressure against other rhizosphere microorganisms (129). Plant host genotype also plays a significant role in the disease-suppressive interaction of plant with a microbial biocontrol agent, as demonstrated by Smith et al. (160, 161).

Lytic enzyme production.A variety of microorganisms also exhibit hyperparasitic activity, attacking pathogens by excreting cell wall hydrolases (26). Chitinase produced by S. plymuthica C48 inhibited spore germination and germ-tube elongation in Botrytis cinerea (58). The ability to produce extracellular chitinases is considered crucial for Serratia marcescens to act as antagonist against Sclerotium rolfsii (121), and for Paenibacillus sp. strain 300 and Streptomyces sp. strain 385 to suppress Fusarium oxysporum f. sp. cucumerinum. It has been also demonstrated that extracellular chitinase and laminarinase synthesized by Pseudomonas stutzeri digest and lyse mycelia of F. solani (91). Although, chitinolytic activity appears less essential for PGPB such as S. plymutica IC14 when used to suppress S. sclerotiorum and B. cinerea, synthesis of proteases and other biocontrol traits are involved (77). The β-1,3-glucanase synthesized by Paenibacillus sp. strain 300 and Streptomyces sp. strain 385 lyse fungal cell walls of F. oxysporum f. sp. cucumerinum (159). B. cepacia synthesizes β-1,3-glucanase that destroys the integrity of R. solani, S. rolfsii, and Pythium ultimum cell walls (59). Similar to siderophores and antibiotics, regulation of lytic enzyme production (proteases and chitinases in particular) involves the GacA/GacS (30, 60, 111, 147) or GrrA/GrrS regulatory systems (123) and colony phase variation (97).

Detoxification and degradation of virulence factors.Another mechanism of biological control is the detoxification of pathogen virulence factors. For example, certain biocontrol agents are able to detoxify albicidin toxin produced by Xanthomonas albilineans (9, 183, 194, 195). The detoxification mechanisms include production of a protein that reversibly binds the toxin in both Klebsiella oxytoca (183) and Alcaligenes denitrificans (9), as well as an irreversible detoxification of albicidin mediated by an esterase that occurs in Pantoea dispersa (194, 195). Several different microorganisms, including strains of B. cepacia and Ralstonia solanacearum, can also hydrolyze fusaric acid, a phytotoxin produced by various Fusarium species (169, 170). More often though, pathogen toxins display a broad-spectrum activity and can suppress growth of microbial competitors, or detoxify antiobiotics produced by some biocontrol microorganisms, as a self-defense mechanism against biocontrol agents (55, 152).

Recently, it has been discovered that certain PGPB quench pathogen quorum-sensing capacity by degrading autoinducer signals, thereby blocking expression of numerous virulence genes (47, 48, 105, 106, 113, 173). Since most, if not all, bacterial plant pathogens rely upon autoinducer-mediated quorum-sensing to turn on gene cascades for their key virulence factors (e.g., cell-degrading enzymes and phytotoxins) (181), this approach holds tremendous potential for alleviating disease, even after the onset of infection, in a curative manner.

Although biocontrol activity of microorgansims involving synthesis of allelochemicals has been studied extensively with free-living rhizobacteria, similar mechanisms apply to endophytic bacteria (92), since they can also synthesize metabolites with antagonistic activity toward plant pathogens (24). For example, Castillo et al. (20) demonstrated that munumbicins, antibiotics produced by the endophytic bacterium Streptomyces sp. strain NRRL 30562 isolated from Kennedia nigriscans, can inhibit in vitro growth of phytopathogenic fungi, P. ultimum, and F. oxysporum. Subsequently, it has been reported that certain endophytic bacteria isolated from field-grown potato plants can reduce the in vitro growth of Streptomyces scabies and Xanthomonas campestris through production of siderophore and antibiotic compounds (154). Interestingly, the ability to inhibit pathogen growth by endophytic bacteria, isolated from potato tubers, decreases as the bacteria colonize the host plant's interior, suggesting that bacterial adaptation to this habitat occurs within their host and may be tissue type and tissue site specific (164). Aino et al. (1) have also reported that the endophytic P. fluorescens strain FPT 9601 can synthesize DAPG and deposit DAPG crystals around and in the roots of tomato, thus demonstrating that endophyte can produce antibiotics in planta.

INDIRECT PLANT GROWTH PROMOTION THROUGH INDUCED SYSTEMIC RESISTANCE

Biopriming plants with some PGPB can also provide systemic resistance against a broad spectrum of plant pathogens. Diseases of fungal, bacterial, and viral origin, and in some instances even damage caused by insects and nematodes, can be reduced after application of PGPB (79, 135, 139, 146, 165).

Induced systemic resistance.Certain bacteria trigger a phenomenon known as ISR phenotypically similar to systemic acquired resistance (SAR). SAR develops when plants successfully activate their defense mechanism in response to primary infection by a pathogen, notably when the latter induces a hypersensitive reaction through which it becomes limited in a local necrotic lesion of brown, desiccated tissue (175). As SAR, ISR is effective against different types of pathogens but differs from SAR in that the inducing PGPB does not cause visible symptoms on the host plant (175). PGPB-elicited ISR was first observed on carnation (Dianthus caryophillus) with reduced susceptibility to wilt caused by Fusarium sp. (178) and on cucumber (Cucumis sativus) with reduced susceptibility to foliar disease caused by Colletotrichum orbiculare (187). Manifestation of ISR is dependent on the combination of host plant and bacterial strain (80, 175). Most reports of PGPB-mediated ISR involve free-living rhizobacterial strains, but endophytic bacteria have also been observed to have ISR activity. For example, ISR was triggered by P. fluorescens EP1 against red rot caused by Colletotrichum falcatum on sugarcane (182), Burkholderia phytofirmans PsJN against Botrytis cinerea on grapevine (2, 3) and Verticllium dahliae on tomato (156), P. denitrificans 1-15 and P. putida 5-48 against Ceratocystis fagacearum on oak (18), P. fluorescens 63-28 against F. oxysporum f. sp. radicis-lycopersici on tomato (109) and Pythium ultimum and F. oxysporum f. sp. pisi on pea roots (12), and Bacillus pumilus SE34 against F. oxysporum f. sp. pisi on pea roots (13) and F. oxysporum f. sp. vasinfectum on cotton roots (29).

Determinants of ISR.The ability to act as bioprotectants via ISR has been demonstrated for both rhizobacteria and bacterial endophytes, and considerable progress has been made in elucidating the mechanisms of plant-PGPB-pathogen interaction. Several bacterial traits (i.e., flagellation and production of siderophores and lipopolysaccharides) have been proposed to trigger ISR (73, 88, 90, 175, 179), but there is no compelling evidence for an overall ISR signal produced by bacteria (67). It has recently been reported that volatile organic compounds may play a key role in this process (135, 145). For example, volatiles secreted by B. subtilis GBO3 and B. amyloquefaciens IN937a were able to activate an ISR pathway in Arabidopsis seedlings challenged with the soft-rot pathogen Erwinia carotovora subsp. carotovora (144). A major distinction often drawn between ISR and SAR is the dependence of the latter on the accumulation of salicylic acid (SA) (128). Some PGPB do trigger an SA-dependent signaling pathway by producing nanogram amounts of SA in the rhizosphere (38, 39). However, the majority of PGPB that activate ISR appear to do so via a SA-independent pathway involving jasmonate and ethylene signals (128, 133). ISR is associated with an increase in sensitivity to these hormones rather than an increase in their production, which might lead to the activation of a partially different set of defense genes (71, 134).

Defense mechanisms of ISR-mediated by PGPB.PGPB-triggered ISR fortifies plant cell wall strength and alters host physiology and metabolic responses, leading to an enhanced synthesis of plant defense chemicals upon challenge by pathogens and/or abiotic stress factors (117, 139). After inoculation of tomato with endophytic P. fluorescens WCS417r, a thickening of the outer tangential and outermost part of the radial side of the first layer of cortical cell walls occurred when epidermal or hypodermal cells were colonized (57). In Burkholderia phytofirmans PsJN-grapevine interaction, a host defense reaction coinciding with phenolic compound accumulation and a strengthening of cell walls in the exodermis and in several cortical cell layers was also observed during endophytic colonization of the bacterium (28). The type of bacterized plant response induced after challenge with a pathogen resulted in the formation of structural barriers, such as thickened cell wall papillae due to the deposition of callose and the accumulation of phenolic compounds at the site of pathogen attack (13, 14, 109). Biochemical or physiological changes in plants (139) include induced accumulation of pathogenesis-related proteins (PR proteins) such as PR-1, PR-2, chitinases, and some peroxidases (76, 100, 109, 126, 139, 182). However, certain PGPB do not induce PR proteins (73, 132, 139, 180) but rather increase accumulation of peroxidase, phenylalanine ammonia lyase, phytoalexins, polyphenol oxidase, and/or chalcone synthase (25, 120, 139, 178). Recent evidence indicates that induction of some of these plant defense compounds (e.g., chalcone synthase) may be triggered by the same N-acyl homoserine lactones that bacteria use for intraspecific signaling (99). The revelation that some PGPB genes involved in antibiotic biosynthesis (e.g., phlD) are highly homologous with some plant genes involved in defense (e.g., chalcone synthase) (4, 7) raises the intriguing but as yet unexplored possibility that the products of these DeVriesien-like pangens may have interspecies activity benefiting plant protection, in addition to their currently known functions.

CONCLUSIONS AND FUTURE PROSPECTS TO MAKE BETTER USE OF PGPB

Research into the mechanisms of plant growth promotion by PGPB have provided a greater understanding of the multiple facets of disease suppression by these biocontrol agents. Still, most of the focus has been on free-living rhizobacterial strains, especially to Pseudomonas and Bacillus. Much remains to be learned from nonsymbiotic endophytic bacteria that have unique associations and apparently a more pronounced growth-enhancing effect on host plants (6, 22, 29, 135).

Revelations about the mechanisms of PGPB action open new doors to design strategies for improving the efficacy of biocontrol agents (107, 108, 184). Identification of key antimicrobials produced by superior agents, such as 2,4-diacetylphloroglucinol, can be exploited for streamlining strain discovery by targeting selection of new isolates that carry relevant biosynthetic genes (193). Determination of the role of edaphic parameters favorable for disease suppression, particularly those that stimulate antibiotic production and activity, can be exploited by targeting inoculants for soils that are more likely to support biocontrol. For example, amending soils or growth substrates with minerals such as zinc or priming inoculants with media amendments during fermentation (51, 53, 125) can be very effective. Similarly, modulation of the rhizosphere bacteria consortia can be accomplished by soil aeration, hydrogenation, and delivery of molasses, sugars and by appropriate crop rotations (reviewed in reference 188).

Identifying different mechanisms of action facilitate the combination of strains, bacteria with bacteria or bacteria with fungi, to hit pathogens with a broader spectrum of microbial weapons (32, 56, 80, 89, 98, 119, 130, 140, 150). Along this same line, biotechnology can be applied to further improve strains that have prized qualities (e.g., formulation ease, stability, or otherwise exceptionally suited to plant colonization) by creating transgenic strains that combine multiple mechanisms of action (27, 74, 168). For example, transforming the 1-aminocyclopropane-1-carboxylic acid deaminase gene, which directly stimulates plant growth by cleaving the immediate precursor of plant ethylene (64) into P. fluorescens CHAO, not only increases plant growth but can also increase biocontrol properties of PGPB (185). Continued work with endophytic bacteria also holds potential for developing biocontrol agents that may be self-perpetuating by colonizing hosts and being transferred to progeny much as is the case with associative nitrogen-fixing PGPB on sugarcane (16) or the nonsymbiotic endophyte bacterium Burkholderia phytofirmans PsJN (117, 155).

ACKNOWLEDGMENTS

This study was supported by a grant from Europôl-Agro (Reims, France). Additional support for B. Duffy was provided by the Swiss Federal Office of Agriculture (project 04.24.3.3).

  • Copyright © 2005 American Society for Microbiology

REFERENCES

  1. 1.↵
    Aino, M., Y. Maekawa, S. Mayama, and H. Kato. 1997. Biocontrol of bacterial wilt of tomato by producing seedlings colonized with endophytic antagonistic pseudomonads, p. 120-123. In A. Ogoshi, K. Kobayashi, Y. Homma, F. Kodama, N. Kondo, and S. Akino (ed.), Plant growth promoting rhizobacteria: present status and future prospects. Nakanishi Printing, Sapporo, Japan.
  2. 2.↵
    Ait Barka, E., A. Belarbi, C. Hachet, J. Nowak, and J. C. Audran. 2000. Enhancement of in vitro growth and resistance to gray mould of Vitis vinifera cocultured with plant growth-promoting rhizobacteria. FEMS Microbiol. Lett.186:91-95.
    OpenUrlCrossRefPubMed
  3. 3.↵
    Ait Barka, E., S. Gognies, J. Nowak, J. C. Audran, and A. Belarbi. 2002. Inhibitory effect of endophyte bacteria on Botrytis cinerea and its influence to promote the grapevine growth. Biol. Control.24:135-142.
    OpenUrlCrossRefWeb of Science
  4. 4.↵
    Austin, M. B., and A. J. P. Noel. 2003. The chalcone synthase superfamily of type III polyketide synthases. Nat. Prod. Rep.20:79-110.
    OpenUrlCrossRefPubMedWeb of Science
  5. 5.↵
    Bacilio-Jiménez, M., S. Aguilar-Flores, E. Ventura-Zapata, E. Pérez-Campos, S. Bouquelet, and E. Zenteno. 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.
    OpenUrlCrossRef
  6. 6.↵
    Bais, H. P., S. W. Park, T. L. Weir, R. M. Callaway, and J. M. Vivanco. 2004. How plants communicate using the underground information superhighway. Trends Plant Sci.9:26-32.
    OpenUrlCrossRefPubMedWeb of Science
  7. 7.↵
    Bangera, M. G., and L. S. Thomashow. 1999. Identification, and characterization and of gene cluster for synthesis of the polyketide antibiotic 2,4-diacetylphloroglucinol from Pseudomonas fluorescens Q2-87. J. Bacteriol.181:3155-3163.
    OpenUrlAbstract/FREE Full Text
  8. 8.↵
    Bashan, Y., and G. Holguin. 1998. Proposal for the division of plant growth-promoting rhizobacteria into two classifications: biocontrol-PGPB (plant growth-promoting bacteria) and PGPB. Soil Biol. Biochem.30:1225-1228.
    OpenUrlCrossRef
  9. 9.↵
    Basnayake, W. V. S., and R. G. Birch. 1995. A gene from Alcaligenes denitrificans that confers albicidin resistance by reversible antibiotic binding. Microbiology141:551-560.
    OpenUrlCrossRefPubMedWeb of Science
  10. 10.↵
    Bell, C. R., G. A. Dickie, W. L. G. Harvey, and J. W. Y. F. Chan. 1995. Endophytic bacteria in grapevine. Can. J. Microbiol.41:46-53.
    OpenUrl
  11. 11.↵
    Bender, C. L., V. Rangaswamy, and J. Loper. 1999. Polyketide production by plant-associated pseudomonads. Annu. Rev. Phytopathol.37:175-196.
    OpenUrlCrossRefPubMedWeb of Science
  12. 12.↵
    Benhamou, N., R. R. Belanger, and T. C. Paulitz. 1996. Induction of differential host responses by Pseudomonas fluorescens in Ri T-DNA-transformed pea roots after challenge with Fusarium oxysporum f. sp. pisi and Pythium ultimum.Phytopathology86:114-178.
    OpenUrl
  13. 13.↵
    Benhamou, N., J. W. Kloepper, A. Quadt-Hallmann, and S. Tuzun. 1996. Induction of defense-related ultrastructural modifications in pea root tissues inoculated with endophytic bacteria. Plant Physiol.112:919-929.
    OpenUrlAbstract
  14. 14.↵
    Benhamou, N., J. W. Kloepper, and S. Tuzun. 1998. Induction of resistance against Fusarium wilt of tomato by combination of chitosan with an endophytic bacterial strain: ultrastructure and cytochemistry of the host response. Planta204:153-168.
    OpenUrlCrossRefWeb of Science
  15. 15.↵
    Bloemberg, G. V., and B. J. J. Lugtenberg. 2001. Molecular basis of plant growth promotion and biocontrol by rhizobacteria. Curr. Opin. Plant Biol.4:343-350.
    OpenUrlCrossRefPubMedWeb of Science
  16. 16.↵
    Boddey, R. M., S. Urquiaga, B. J. R. Alves, and V. Reis. 2003. Endophytic nitrogen fixation in sugarcane: present knowledge and future applications. Plant Soil252:139-149.
    OpenUrlCrossRef
  17. 17.↵
    Brodhagen, M., M. D. Henkels, and J. E. Loper. 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.
    OpenUrlAbstract/FREE Full Text
  18. 18.↵
    Brooks, D. S., C. F. Gonzalez, D. N. Apple, and T. H. Filer. 1994. Evaluation of endophytic bacteria as potential biological control agents for oak wilt. Biol. Control4:373-381.
    OpenUrlCrossRef
  19. 19.↵
    Castignetti, D., and J. Smarelli. 1986. Siderophores, the iron nutrition of plants, and nitrate reductase. FEBS Lett.209:147-151.
    OpenUrlCrossRef
  20. 20.↵
    Castillo, U. F., G. A. Strobel, E. J. Ford, W. M. Hess, H. Porter, J. B. Jensen, H. Albert, R. Robison, M. A. M. Condron, D. B. Teplow, D. Steevens, and D. Yaver. 2002. Munumbicins, wide-spectrum antiobiotics produced by Streptomyces NRRL 30562, endophytic on Kennedia nigriscans.Microbiology148:2675-2685.
    OpenUrlCrossRefPubMedWeb of Science
  21. 21.↵
    Chancey, S. T., D. W. Wood, and L. S. Pierson. 1999. Two-component transcriptional regulation of N-acyl-homoserine lactone production in Pseudomonas aureofaciens.Appl. Environ. Microbiol.65:2294-2299.
    OpenUrlAbstract/FREE Full Text
  22. 22.↵
    Chanway, C. P., M. Shishido, J. Nairn, S. Jungwirth, J. Markham, G. Xiao, and F. B. Holl. 2000. Endophytic colonization and field responses of hybrid spruce seedlings after inoculation with plant growth-promoting rhizobacteria. For. Ecol. Man.133:81-88.
    OpenUrlCrossRef
  23. 23.↵
    Chatterton, S., J. C. Sutton, and G. J. Boland. 2004. Timing Pseudomonas chlororaphis applications to control Pythium aphanidermatum,Pythium dissotocum, and root rot in hydroponic peppers. Biol. Control30:360-373.
    OpenUrlCrossRef
  24. 24.↵
    Chen, C., E. M. Bauske, G. Musson, R. Rodriguez-Kabana, and J. W. Kloepper. 1995. Biological control of Fusarium wilt on cotton by use of endophytic bacteria. Biol. Control5:83-91.
    OpenUrlCrossRef
  25. 25.↵
    Chen, C., R. R. Bélanger, N. Benhamou, and T. C. Paulitz. 2000. Defense enzymes induced in cucumber roots by treatment with plant growth-promoting rhizobacteria (PGPR) and Pythium aphanidermatum.Physiol. Mol. Plant Pathol.56:13-23.
    OpenUrlCrossRef
  26. 26.↵
    Chernin, L., and I. Chet. 2002. Microbial enzymes in biocontrol of plant pathogens and pests, p. 171-225. In R. G. Burns and R. P. Dick (ed.), Enzymes in the environment: activity, ecology, and applications. Marcel Dekker, New York, N.Y.
  27. 27.↵
    Chin-A-Woeng, T. F. C., J. E. Thomas-Oates, B. J. J. Lugtenberg, and G. V. Bloemberg. 2001. Introduction of the phzH gene of Pseudomonas chlororaphis PCL1391 extends the range of biocontrol ability of phenazine-1-carboxylic acid-producing Pseudomonas spp. strains. Mol. Plant-Microbe Interact.14:1006-1015.
    OpenUrlCrossRefPubMedWeb of Science
  28. 28.↵
    Compant, S., B. Reiter, A. Sessitsch, J. Nowak, C. Clément, and E. Ait Barka. 2005. Endophytic colonization of Vitis vinifera L. by a plant growth-promoting bacterium, Burkholderia sp. strain PsJN. Appl. Environ. Microbiol.71:1685-1693.
    OpenUrlAbstract/FREE Full Text
  29. 29.↵
    Conn, K. L., J. Nowak, and G. Lazarovits. 1997. A gnotobiotic bioassay for studying interactions between potato and plant growth-promoting rhizobacteria. Can. J. Microbiol.43:801-808.
    OpenUrl
  30. 30.↵
    Corbell, N., and J. E. Loper. 1995. A global regulator of secondary metabolite production in Pseudomonas fluorescens Pf-5. J. Bacteriol.177:6230-6236.
    OpenUrlAbstract/FREE Full Text
  31. 31.↵
    Cornelis, P., and S. Matthijs. 2002. Diversity of siderophore-mediated iron uptake systems in fluorescent pseudomonads: not only pyoverdines. Environ. Microbiol.4:787-798.
    OpenUrlCrossRefPubMedWeb of Science
  32. 32.↵
    de Boer, M., I. van der Sluis, L. C. van Loon, and P. A. H. M. Bakker. 1999. Combining fluorescent Pseudomonas spp. strains to enhance suppression of fusarium wilt of radish. Eur. J. Plant Pathol.105:201-210.
    OpenUrlCrossRef
  33. 33.↵
    Défago, G. 1993. 2,4-Diacetylphloroglucinol, a promising compound in biocontrol. Plant Pathol.42:311-312.
    OpenUrlCrossRef
  34. 34.↵
    Degenhardt, J., J. Gershenzon, I. T. Baldwin, and A. Kessler. 2003. Attracting friends to feast on foes: engineering terpene emission to make crop plants more attractive to herbivore enemies. Curr. Opin. Biotechnol.14:169-176.
    OpenUrlCrossRefPubMedWeb of Science
  35. 35.↵
    Dekkers, L. C., A. J. van der Bij, I. H. M. Mulders, C. C. Phoelich, R. A. R. Wentwoord, D. C. M. Glandorf, C. A. Wijffelman, and B. J. J. Lugtenberg. 1998. Role of the O-antigen of lipopolysaccheride, and possible roles of growth rate and of NADH:ubiquinone oxidoreductase (nuo) in competitive tomato root-tip colonization by Pseudomonas fluorescens WCS365. Mol. Plant-Microbe Interact.11:763-771.
    OpenUrlCrossRefPubMedWeb of Science
  36. 36.↵
    Dekkers, L. C., C. C. Phoelich, L. van der Fits, and B. J. J. Lugtenberg. 1998. A site-specific recombinase is required for competitive root colonization by Pseudomonas fluorescens WCS365. Proc. Natl. Acad. Sci. USA95:7051-7056.
    OpenUrlAbstract/FREE Full Text
  37. 37.↵
    Dekkers, L. C., I. H. Mulders, C. C. Phoelich, T. F. C. Chin-A-Woeng, A. H. Wijfjes, and B. J. J. Lugtenberg. 2000. The sss colonization gene of the tomato-Fusarium oxysporum f. sp. radicis-lycopersici biocontrol strain Pseudomonas fluorescens WCS365 can improve root colonization of other wild-type Pseudomonas spp. bacteria. Mol. Plant-Microbe Interact.13:1177-1183.
    OpenUrlCrossRefPubMedWeb of Science
  38. 38.↵
    De Meyer, G., and M. Höfte. 1997. Salicylic acid produced by the rhizobacterium Pseudomonas aeruginosa 7NSK2 induces resistance to leaf infection by Botrytis cinerea on bean. Phytopathology87:588-593.
    OpenUrlCrossRefPubMedWeb of Science
  39. 39.↵
    De Meyer, G., K. Audenaert, and M. Höfte. 1999. Pseudomonas aeruginosa 7NSK2-induced systemic resistance in tobacco depends on in planta salicylic acid accumulation but is not associated with PR1a expression. Eur. J. Plant Pathol.105:513-517.
    OpenUrlCrossRef
  40. 40.↵
    de Souza, J. T., M. de Boer, P. de Waard, T. A. van Beek, and J. M. Raaijmakers. 2003. Biochemical, genetic, and zoosporicidal properties of cyclic lipopeptide surfactants produced by Pseudomonas fluorescens.Appl. Environ. Microbiol.69:7161-7172.
    OpenUrlAbstract/FREE Full Text
  41. 41.↵
    De Weert, S., H. Vermeiren, I. H. M. Mulders, I. Kuiper, N. Hendrickx, G. V. Bloemberg, J. Vanderleyden, R. de Mot, and B. J. J. Lugtenberg. 2002. Flagella-driven chemotaxis toward exudate components is an important trait for tomato root colonization by Pseudomonas fluorescens.Mol. Plant-Microbe Interact.15:1173-1180.
    OpenUrlCrossRefPubMedWeb of Science
  42. 42.↵
    De Weger, L. A., C. I. M. van der Vlugt, A. H. M. Wijfjes, P. A. H. M. Bakker, B. Schippers, and B. Lugtenberg. 1987. Flagella of a plant-growth-stimulating Pseudomonas fluorescens strain are required for colonization of potato roots. J. Bacteriol.169:2769-2773.
    OpenUrlAbstract/FREE Full Text
  43. 43.↵
    De Weger, L. A., P. A. H. M. Bakker, B. Schippers, M. C. M. van Loosdrecht, and B. Lugtenberg. 1989. Pseudomonas spp. with mutational changes in the O-antigenic side chain of their lipopolysaccharides are affected in their ability to colonize potato roots, p. 197-202. In B. J. J. Lugtenberg (ed.), Signal molecules in plant-microbe interactions. Springer-Verlag, Berlin, Germany.
  44. 44.↵
    De Weger, L. A., A. J. van der Bij, L. C. Dekkers, M. Simons, C. A. Wijffelman, and B. J. J. Lugtenberg. 1995. Colonization of the rhizosphere of crop plants by plant-beneficial pseudomonads. FEMS Microbiol. Ecol.17:221-228.
    OpenUrlCrossRefWeb of Science
  45. 45.↵
    Di Santo, R., R. Costi, M. Artico, S. Massa, G. Lampis, D. Deidda, and R. Pompei. 1998. Pyrrolnitrin and related pyrroles endowed with antibacterial activities against Mycobacterium tuberculosis.Bioorg. Medicinal Chem. Lett.8:2931-2936.
    OpenUrlCrossRefPubMed
  46. 46.↵
    Dobbelaere, S., J. Vanderleyden, and Y. Okon. 2003. Plant growth-promoting effects of diazotrophs in the rhizosphere. Crit. Rev. Plant Sci.22:107-149.
    OpenUrlCrossRefWeb of Science
  47. 47.↵
    Dong, Y. H., J. L. Xu, X. Z. Li, and L. H. Zhang. 2000. AiiA, an enzyme that inactivates the acylhomoserine lactone quorum-sensing signal and attenuates the virulence of Erwinia carotovora.Proc. Natl. Acad. Sci. USA97:3526-3531.
    OpenUrlAbstract/FREE Full Text
  48. 48.↵
    Dong, Y. H., X. F. Zhang, J. L. Xu, and L. H. Zhang. 2004. Insecticidal Bacillus thuringiensis silences Erwinia carotovora virulence by a new form of microbial antagonism, signal interference. Appl. Environ. Microbiol.70:954-960.
    OpenUrlAbstract/FREE Full Text
  49. 49.↵
    Dörr, J., T. Hurek, and B. Reinhold-Hurek. 1998. Type IV pili are involved in plant-microbe and fungus-microbe interactions. Mol. Microbiol.30:7-17.
    OpenUrlCrossRefPubMed
  50. 50.↵
    Duffy, B. K. 2001. Competition, p. 243-244. In O. C. Maloy and T. D. Murray (ed.), Encyclopedia of plant pathology. John Wiley & Sons, Inc., New York, N.Y.
  51. 51.↵
    Duffy, B. K., and G. Défago. 1997. Zinc improves biocontrol of Fusarium crown and root rot of tomato by Pseudomonas fluorescens and represses the production of pathogen metabolites inhibitory to bacterial antibiotic biosynthesis. Phytopathology87:1250-1257.
    OpenUrlCrossRefPubMedWeb of Science
  52. 52.↵
    Duffy, B. K., and G. Défago. 1999. Environmental factors modulating antibiotic and siderophore biosynthesis by Pseudomonas fluorescens biocontrol strains. Appl. Environ. Microbiol.65:2429-2438.
    OpenUrlAbstract/FREE Full Text
  53. 53.↵
    Duffy, B. K., and G. Défago. 2000. Controlling instability in gacS-gacA regulatory genes during inoculum production of Pseudomonas fluorescens bicontrol strains. Appl. Environ. Microbiol.66:3142-3150.
    OpenUrlAbstract/FREE Full Text
  54. 54.↵
    Duffy, B., C. Keel, and G. Défago. 2004. Potential role of pathogen signaling in multitrophic plant-microbe interactions involved in disease protection. Appl. Environ. Microbiol.70:1836-1842.
    OpenUrlAbstract/FREE Full Text
  55. 55.↵
    Duffy, B., A. Schouten, and J. M. Raaijmakers. 2003. Pathogen self defense: mechanisms to counteract microbial antagonism. Annu. Rev. Phytopathol.41:501-538.
    OpenUrlCrossRefPubMedWeb of Science
  56. 56.↵
    Duffy, B. K., A. Simon, and D. M. Weller. 1996. Combination of Trichoderma koningii with fluorescent pseudomonads for control of take-all on wheat. Phytopathology86:188-194.
    OpenUrlCrossRefWeb of Science
  57. 57.↵
    Duijff, B. J., V. Gianinazzi-Pearson, and P. Lemanceau. 1997. Involvement of the outer membrane lipopolysaccharides in the endophytic colonization of tomato roots by biocontrol Pseudomonas fluorescens strain WCS417r. New Phytol.135:325-334.
    OpenUrlCrossRef
  58. 58.↵
    Frankowski, J., M. Lorito, F. Scala, R. Schmidt, G. Berg, and H. Bahl. 2001. Purification and properties of two chitinolytic enzymes of Serratia plymuthica HRO-C48. Arch. Microbiol.176:421-426.
    OpenUrlCrossRefPubMedWeb of Science
  59. 59.↵
    Fridlender, M., J. Inbar, and I. Chet. 1993. Biological control of soilborne plant pathogens by a β-1,3-glucanase-producing Pseudomonas cepacia.Soil Biol. Biochem.25:1211-1221.
    OpenUrlCrossRef
  60. 60.↵
    Gaffney, T. D., S. T. Lam, J. Ligon, K. Gates, A. Frazelle, J. Di Maio, S. Hill, S. Goodwin, N. Torkewitz, and A. M. Allshouse. 1994. Global regulation of expression of antifungal factors by a Pseudomonas fluorescens biological control strain. Mol. Plant-Microbe Interact.7:455-463.
    OpenUrlCrossRefPubMedWeb of Science
  61. 61.↵
    Georgakopoulos, D. G., M. Hendson, N. J. Panopoulos, and M. N. Schroth. 1994. Cloning of a phenazine biosynthetic locus of Pseudomonas aureofaciens PGS12 and analysis of its expression in vitro with the ice nucleation reporter gene. Appl. Environ. Microbiol.60:2931-2938.
    OpenUrlAbstract/FREE Full Text
  62. 62.↵
    Gerhardson, B. 2002. Biological substitutes for pesticides. Trends Biotechnol.20:338-343.
    OpenUrlCrossRefPubMedWeb of Science
  63. 63.↵
    Glick, B. 1995. The enhancement of plant growth by free-living bacteria. Can. J. Microbiol.41:109-117.
    OpenUrl
  64. 64.↵
    Glick, B. R., Penrose, D. M., and J. Li. 1998. A model for the lowering of plant ethylene concentrations by plant growth-promoting bacteria. J. Theor. Biol.190:63-68.
    OpenUrlCrossRefPubMedWeb of Science
  65. 65.↵
    Gray, E. J., and D. L. Smith. 2005. Intracellular and extracellular PGPR: commonalities and distinctions in the plant-bacterium signaling processes. Soil Biol. Biochem.37:395-412.
    OpenUrlCrossRef
  66. 66.↵
    Haas, D., C. Blumer, and C. Keel. 2000. Biocontrol ability of fluorescent pseudomonads genetically dissected: importance of positive feedback regulation. Curr. Opin. Biotechnol.11:290-297.
    OpenUrlCrossRefPubMedWeb of Science
  67. 67.↵
    Haas, D., C. Keel, and C. Reimmann. 2002. Signal transduction in plant-beneficial rhizobacteria with biocontrol properties. Antonie Leeuwenhoek81:385-395.
    OpenUrlCrossRefPubMedWeb of Science
  68. 68.↵
    Haas, D., and C. Keel. 2003. Regulation of antibiotic production in root-colonizing Pseudomonas spp. and relevance for biological control of plant disease. Annu. Rev. Phytopathol.41:117-153.
    OpenUrlCrossRefPubMedWeb of Science
  69. 69.↵
    Hahn, H. P. 1997. The type-4 pilus is the major virulence-associated adhesin of Pseudomonas aeruginosa-a review. Gene192:99-108.
    OpenUrlCrossRefPubMedWeb of Science
  70. 70.↵
    Hallman, J., A. Quadt-Hallman, W. F. Mahafee, and J. W. Kloepper. 1997. Bacterial endophytes in agricultural crops. Can. J. Microbiol.43:895-914.
    OpenUrl
  71. 71.↵
    Hase, S., J. A. van Pelt, L. C. van Loon, and C. M. J. Pieterse. 2003. Colonization of Arabidopsis roots by Pseudomonas fluorescens primes the plant to produce higher levels of ethylene upon pathogen infection. Physiol. Mol. Plant Pathol.62:219-226.
    OpenUrlCrossRef
  72. 72.↵
    Hashidoko, Y., T. Nakayama, Y. Homma, and S. Tahara. 1999. Structure elucidation of xanthobaccin A, a new antibiotic produced from Stenotrophomonas sp. strain SB-K88. Tetrahedron Lett.40:2957-2960.
    OpenUrlCrossRef
  73. 73.↵
    Hoffland, E., C. Pieterse, L. Bik, and J. A. van Pelt. 1995. Induced systemic resistance in radish is not associated with accumulation of pathogenesis-related proteins. Physiol. Mol. Plant Pathol.46:309-320.
    OpenUrlCrossRefWeb of Science
  74. 74.↵
    Huang, Z., R. F. Bonsall, D. V. Mavrodi, D. M. Weller, and L. S. Thomashow. 2004. Transformation of Pseudomonas fluorescens with genes for biosynthesis of phenazine-1-carboxylic acid improves biocontrol of rhizoctonia root rot and in situ antibiotic production. FEMS Microbiol. Ecol.49:243-251.
    OpenUrlCrossRef
  75. 75.↵
    Isnansetyo, A., L. Z. Cui, K. Hiramatsu, and Y. Kamei. 2003. Antibacterial activity of 2,4-diacetylphloroglucinol produced by Pseudomonas sp. AMSN isolated from a marine alga, against vancomycin-resistant Staphylococcus aureus.Int. J. Antimicrob. Agents22:545-547.
    OpenUrlCrossRefPubMed
  76. 76.↵
    Jeun, Y. C., K. S. Park, C. H. Kim, W. D. Fowler, and J. W. Kloepper. 2004. Cytological observations of cucumber plants during induced resistance elicited by rhizobacteria. Biol. Control29:34-42.
    OpenUrlCrossRef
  77. 77.↵
    Kamensky, M., M. Ovadis, I. Chet, and L. Chernin. 2003. Soil-borne strain IC14 of Serratia plymuthica with multiple mechanisms of antifungal activity provides biocontrol of Botrytis cinerea and Sclerotinia sclerotiorum diseases. Soil Biol. Biochem.35:323-331.
    OpenUrlCrossRef
  78. 78.↵
    Keel, C., C. Voisard, C. H. Berling, G. Kahr, and G. Défago. 1989. Iron sufficiency, a prerequisite for the suppression of tobacco black root rot by Pseudomonas fluorescens strain CHA0 under gnotobiotic conditions. Phytopathology79:584-589.
    OpenUrlCrossRefWeb of Science
  79. 79.↵
    Kerry, B. R. 2000. Rhizosphere interactions and the exploitation of microbial agents for the biological control of plant-parasitic nematodes. Annu. Rev. Phytopathol.38:423-441.
    OpenUrlCrossRefPubMedWeb of Science
  80. 80.↵
    Kilic-Ekici, O., and G. Y. Yuen. 2004. Comparison of strains of Lysobacter enzymogenes and PGPR for induction of resistance against Bipolaris sorokiniana in tall fescue. Biol. Control30:446-455.
    OpenUrlCrossRef
  81. 81.↵
    Kim, B. S., S. S. Moon, and B. K. Hwang. 1999. Isolation, identification and antifungal activity of a macrolide antibiotic, oligomycin A, produced by Streptomyces libani.Can. J. Bot.77:850-858.
    OpenUrlCrossRef
  82. 82.↵
    Kloepper, J. W., and M. N. Schroth. 1978. Plant growth-promoting rhizobacteria on radishes, p. 879-882. In Station de pathologie vegetale et phyto-bacteriologie (ed.), Proceedings of the 4th International Conference on Plant Pathogenic Bacteria,vol. II. Gilbert-Clarey, Tours, France.
    OpenUrl
  83. 83.↵
    Kloepper, J. W., B. Schippers, and P. A. H. M. Bakker. 1992. Proposed elimination of the term endorhizosphere. Phytopathology82:726-727.
    OpenUrlWeb of Science
  84. 84.↵
    Kloepper, J. W., R. Rodriguez-Ubana, G. W. Zehnder, J. F. Murphy, E. Sikora, and C. Fernandez. 1999. Plant root-bacterial interactions in biological control of soilborne diseases and potential extension to systemic and foliar diseases. Austral. Plant Pathol.28:21-26.
    OpenUrlCrossRef
  85. 85.↵
    Knee, E. M., F. C. Gong, M. Gao, M. Teplitski, A. R. Jones, A. Foxworthy, A. J. Mort, and W. D. Bauer. 2001. Root mucilage from pea and its utilization by rhizosphere bacteria as a sole carbon source. Mol. Plant-Microbe Interact.14:775-784.
    OpenUrlCrossRefPubMedWeb of Science
  86. 86.↵
    Kojic, M., G. Degrassi, and V. Venturi. 1999. Cloning and characterization of the rpoS gene from the plant growth-promoting Pseudomonas putida WCS358: RpoS is not involved in siderophore and homoserine lactone production. Biochim. Biophys. Acta1489:413-420.
    OpenUrlPubMedWeb of Science
  87. 87.↵
    Kuiper, I., G. V. Bloemberg, S. Noreen, J. E. Thomas-Oates, and B. J. J. Lugtenberg. 2001. Increased uptake of putrescine in the rhizosphere inhibits competitive root colonization by Pseudomonas fluorescens strain WCS365. Mol. Plant-Microbe Interact.14:1096-1104.
    OpenUrlCrossRefPubMedWeb of Science
  88. 88.↵
    Leeman, M., J. A. van Pelt, F. M. Denouden, M. Heinsbroek, P. Bakker, and B. Schippers. 1995. Induction of systemic resistance against Fusarium wilt of radish by lipopolysaccharides of Pseudomonas fluorescens.Phytopathology85:1021-1027.
    OpenUrlCrossRefWeb of Science
  89. 89.↵
    Leeman, M., F. M. Denouden, J. A. VanPelt, C. Cornelissen, A. MatamalaGarros, P. A. H. M. Bakker, and B. Schippers. 1996. Suppression of fusarium wilt of radish by co-inoculation of fluorescent Pseudomonas spp. and root-colonizing fungi. Eur. J. Plant Pathol.102:21-31.
    OpenUrl
  90. 90.↵
    Leeman, M., E. M. Denouden, J. A. van Pelt, F. Dirkx, H. Steijl, P. Bakker, and B. Schippers. 1996. Iron availability affects induction of systemic resistance to fusarium wilt of radish by Pseudomonas fluorescens.Phytopathology86:149-155.
    OpenUrlCrossRefWeb of Science
  91. 91.↵
    Lim, H. S., Y. S. Kim, and S. D. Kim. 1991. Pseudomonas stutzeri YPL-1 genetic transformation and antifungal mechanism against Fusarium solani, an agent of plant root rot. Appl. Environ. Microbiol.57:510-516.
    OpenUrlAbstract/FREE Full Text
  92. 92.↵
    Lodewyckx, C., J. Vangronsveld, F. Porteous, E. R. B. Moore, S. Taghavi, M. Mezgeay, and D. van der Lelie. 2002. Endophytic bacteria and their potential applications. Crit. Rev. Plant Sci.21:583-606.
    OpenUrlCrossRefWeb of Science
  93. 93.↵
    Loper, J. E., and M. D. Henkels. 1997. Availability of iron to Pseudomonas fluorescens in rhizosphere and bulk soil evaluated with an ice nucleation reporter gene. Appl. Environ. Microbiol.63:99-105.
    OpenUrlAbstract/FREE Full Text
  94. 94.↵
    Loper, J. E., and M. D. Henkels. 1999. Utilization of heterologous siderophores enhances levels of iron available to Pseudomonas putida in the rhizosphere. Appl. Environ. Microbiol.65:5357-5363.
    OpenUrlAbstract/FREE Full Text
  95. 95.↵
    Lugtenberg, B. J. J., and L. C. Dekkers. 1999. What make Pseudomonas bacteria rhizosphere competent? Environ. Microbiol.1:9-13.
    OpenUrlCrossRefPubMedWeb of Science
  96. 96.↵
    Lugtenberg, B. J., L. V. Kravchenko, and M. Simons. 1999. Tomato seed and root exudate sugars: composition, utilization by Pseudomonas biocontrol strains, and role in rhizosphere colonization. Environ. Microbiol.1:439-446.
    OpenUrlCrossRefPubMedWeb of Science
  97. 97.↵
    Lugtenberg, B. J. J., L. Dekkers, and G. V. Bloemberg. 2001. Molecular determinants of rhizosphere colonization by Pseudomonas.Annu. Rev. Phytopathol.39:461-490.
    OpenUrlCrossRefPubMedWeb of Science
  98. 98.↵
    Lutz, M. P., S. Wenger, M. Maurhofer, G. Défago, and B. Duffy. 2004. Signaling between bacterial and fungal biocontrol agents in a strain mixture. FEMS Microbiol. Ecol.48:447-455.
    OpenUrlCrossRef
  99. 99.↵
    Mathesius, U., S. Mulders, M. S. Gao, M. Teplitski, G. Caetano-Anolles, B. G. Rolfe, and W. D. Bauer. 2003. Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals. Proc. Natl. Acad. Sci. USA100:1444-1449.
    OpenUrlAbstract/FREE Full Text
  100. 100.↵
    Maurhofer, M., C. Hase, P. Meuwly, J. P. Metraux, and G. Défago. 1994. Induction of systemic resistance of tobacco to tobacco necrosis virus by the root-colonizing Pseudomonas fluorescens strain CHA0: influence of the gacA gene and of pyoverdine production. Phytopathology84:139-146.
    OpenUrlCrossRefWeb of Science
  101. 101.↵
    Mayak, S., T. Tirosh, and B. R. Glick. 2004. Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol. Biochem.42:565-572.
    OpenUrlCrossRefPubMedWeb of Science
  102. 102.↵
    McInroy, J. A., and J. W. Klopper. 1995. Population dynamics of endophytic bacteria in field-grown sweet corn and cotton. Can. J. Microbiol.41:895-901.
    OpenUrlWeb of Science
  103. 103.↵
    Milner, J. L., S. J. Raffel, B. J. Lethbridge, and J. Handelsman. 1995. Culture conditions that influence accumulation of zwittermicin A by Bacillus cereus UW85. Appl. Microbiol. Biotechnol.43:685-691.
    OpenUrlCrossRefPubMedWeb of Science
  104. 104.↵
    Milner, J. L., L. Silo-Suh, J. C. Lee, H. He, J. Clardy, and J. Handelsman. 1996. Production of kanosamine by Bacillus cereus UW85. Appl. Environ. Microbiol.62:3061-3065.
    OpenUrlAbstract/FREE Full Text
  105. 105.↵
    Molina, L., F. Constantinescu, C. Reimmann, B. Duffy, and G. Défago. 2003. Degradation of pathogen quorum-sensing molecules by soil bacteria: a preventive and curative biological control mechanism. FEMS Microbiol. Ecol.45:71-81.
    OpenUrlCrossRef
  106. 106.↵
    Morello, J. E., E. A. Pierson, and L. S. Pierson. 2004. Negative cross-communication among wheat rhizosphere bacteria: effect on antibiotic production by the biological control bacterium Pseudomonas aureofaciens 30-84. Appl. Environ. Microbiol.70:3103-3109.
    OpenUrlAbstract/FREE Full Text
  107. 107.↵
    Morrissey, J. P., J. M. Dow, G. L. Mark, and F. O'Gara. 2004. Are microbes at the root of a solution to world food production? EMBO Rep.5:922-926.
    OpenUrlCrossRefPubMedWeb of Science
  108. 108.↵
    Morrissey, J. P., U. F. Walsh, A. O'Donnell, Y. Moënne-Loccoz, and F. O'Gara. 2002. Exploitation of genetically modified inoculants for inductrial ecology applications. Antonie Leeuwenhoek81:599-606.
    OpenUrlCrossRefPubMedWeb of Science
  109. 109.↵
    M'Piga, P., R. R. Belanger, T. C. Paulitz, and N. Benhamou. 1997. Increased resistance to Fusarium oxysporum f. sp. radicis-lycopersici in tomato plants treated with the endophytic bacterium Pseudomonas fluorescens strain 63-28. Physiol. Mol. Plant Pathol.50:301-320.
    OpenUrlCrossRef
  110. 110.↵
    Nakayama, T., Y. Homma, Y. Hashidoko, J. Mizutani, and S. Tahara. 1999. Possible role of xanthobaccins produced by Stenotrophomonas sp. strain SB-K88 in suppression of sugar beet damping-off disease. Appl. Environ. Microbiol.65:4334-4339.
    OpenUrlAbstract/FREE Full Text
  111. 111.↵
    Natsch, A., C. Keel, H. A. Pfirter, D. Hass, and G. Défago. 1994. Contribution of the global regulator gene gacA to persistence and dissemination of Pseudomonas fluorescens biocontrol strain CHA0 introduced into soil microcosms. Appl. Environ. Microbiol.60:2553-2560.
    OpenUrlAbstract/FREE Full Text
  112. 112.↵
    Nelson, E. B. 2004. Microbial dynamics and interactions in the spermosphere. Annu. Rev. Phytopathol.42:271-309.
    OpenUrlCrossRefPubMedWeb of Science
  113. 113.↵
    Newton, J. A., and R. G. Fray. 2004. Integration of environmental and host-derived signals with quorum sensing during plant-microbe interactions. Cell. Microbiol.6:213-224.
    OpenUrlCrossRefPubMedWeb of Science
  114. 114.↵
    Nielsen, T. H., D. Sørensen, C. Tobiasen, J. B. Andersen, C. Christeophersen, M. Givskov, and J. Sørensen. 2002. Antibiotic and biosurfactant properties of cyclic lipopeptides produced by fluorescent Pseudomonas spp. from the sugar beet rhizosphere. Appl. Environ. Microbiol.68:3416-3423.
    OpenUrlAbstract/FREE Full Text
  115. 115.↵
    Nielsen, T. H., and J. Sørensen. 2003. Production of cyclic lipopeptides by Pseudomonas fluorescens strains in bulk soil and in the sugar beet rhizosphere. Appl. Environ. Microbiol.69:861-868.
    OpenUrlAbstract/FREE Full Text
  116. 116.↵
    Notz, R., M. Maurhofer, U. Schnider-Keel, B. Duffy, D. Haas, and G. Défago. 2001. Biotic factors affecting expression of the 2,4-diacetylphloroglucinol biosynthesis gene phlA in Pseudomonas fluorescens biocontrol strain CHA0 in the rhizosphere. Phytopathology91:873-881.
    OpenUrlCrossRefPubMedWeb of Science
  117. 117.↵
    Nowak, J., and V. Shulaev. 2003. Priming for transplant stress resistance in in vitro propagation. In Vitro Cell. Dev. Biol.-Plant.39:107-124.
    OpenUrl
  118. 118.↵
    Okubara, P. A., J. P. Kornoely, and B. B. Landa. 2004. Rhizosphere colonization of hexaploid wheat by Pseudomonas fluorescens strains Q8rl-96 and Q2-87 is cultivar-variable and associated with changes in gross root morphology. Biol. Control.30:392-403.
    OpenUrlCrossRef
  119. 119.↵
    Olivain, C., C. Alabouvette, and C. Steinberg. 2004. Production of a mixed inoculum of Fusarium oxysporum Fo47 and Pseudomonas fluorescens C7 to control Fusarium diseases. Biol. Sci. Technol.14:227-238.
    OpenUrl
  120. 120.↵
    Ongena, M., F. Daayf, P. Jacques, P. Thonart, N. Benhamou, T. C. Paulitz, and R. R. Bélanger. 2000. Systemic induction of phytoalexins in cucumber in response to treatments with fluorescent pseudomonads. Plant Pathol.49:523-530.
    OpenUrlCrossRef
  121. 121.↵
    Ordentlich, A., Y. Elad, and I. Chet. 1988. The role of chitinase of Serratia marcescens in biocontrol of Sclerotium rolfsii.Phytopathology78:84-88.
    OpenUrlWeb of Science
  122. 122.↵
    O'Sullivan, D. J., and F. O'Gara. 1992. Traits of fluorescent Pseudomonas spp. involved in suppression of plant root pathogens. Microbiol. Rev.56:662-676.
    OpenUrlAbstract/FREE Full Text
  123. 123.↵
    Ovadis, M., X. Liu, S. Gavriel, Z. Ismailov, I. Chet, and L. Chernin. 2004. The global regulator genes from biocontrol strain Serratia plymuthica IC1270: cloning, sequencing, and functional studies. J. Bacteriol.186:4986-4993.
    OpenUrlAbstract/FREE Full Text
  124. 124.↵
    Ownley, B. H., D. M. Weller, and L. S. Thomashow. 1992. Influence of in situ and in vitro pH on suppression of Gaeumannomyces graminis var. tritici by Pseudomonas fluorescens 2-79. Phytopathology82:178-184.
    OpenUrlCrossRefWeb of Science
  125. 125.↵
    Ownley, B. H., B. K. Duffy, and D. M. Weller. 2003. Identification and manipulation of soil properties to improve the biological control performance of phenazine-producing Pseudomonas fluorescens.Appl. Environ. Microbiol.69:3333-3343.
    OpenUrlAbstract/FREE Full Text
  126. 126.↵
    Park, K. S., and J. W. Kloepper. 2000. Activation of PR-1a promoter by rhizobacteria which induce systemic resistance in tobacco against Pseudomonas syringae pv. tabaci.Biol. Control18:2-9.
    OpenUrlCrossRef
  127. 127.↵
    Parke, J. L. 1991. Root colonization by indigenous and introduced microorganisms, p. 33-42. In D. L. Keister and P. B. Gregan (ed.), The rhizosphere and plant growth. Kluwer Academic Publishers, Dordrecht, The Netherlands.
  128. 128.↵
    Pettersson, M., and E. Bååth. 2004. Effects of the properties of the bacterial community on pH adaptation during recolonization of a humus soil. Soil Biol. Biochem.36:1383-1388.
    OpenUrlCrossRef
  129. 129.↵
    Picard, C., F. Di Cello, M. Ventura, R. Fani, and A. Guckert. 2000. Frequency and biodiversity of 2,4-diacetylphloroglucinol-producing bacteria isolated from the maize rhizosphere at different stages of plant growth. 66:948-955.
  130. 130.↵
    Pierson, E. A., D. W. Wood, J. A. Cannon, F. M. Blachere, and L. S. Pierson. 1998. Interpopulation signaling via N-acyl-homoserine lactones among bacteria in the wheat rhizosphere. Mol. Plant-Microbe Interact.11:1078-1084.
    OpenUrlCrossRefWeb of Science
  131. 131.↵
    Pierson, L. S., D. W. Wood, and E. A. Pierson. 1998. Homoserine lactone-mediated gene regulation in plant-associated bacteria. Annu. Rev. Phytopathol.36:207-225.
    OpenUrlCrossRefPubMedWeb of Science
  132. 132.↵
    Pieterse, C. M. J., S. C. M. van Wees, E. Hoffland, J. A. van Pelt, and L. C. van Loon. 1996. Systemic resistance in Arabidopsis induced by biocontrol bacteria is independent of salicylic acid accumulation and pathogenesis-related gene expression. Plant Cell8:1225-1237.
    OpenUrlAbstract/FREE Full Text
  133. 133.↵
    Pieterse, C. M. J., S. C. M. van Wees, J. A. van Pelt, M. Knoester, R. Laan, H. Gerrits, P. J. Weisbeek, and L. C. van Loon. 1998. A novel signaling pathway controlling induced systemic resistance in Arabidopsis.Plant Cell10:1571-1580.
    OpenUrlAbstract/FREE Full Text
  134. 134.↵
    Pieterse, C. M. J., and L. C. van Loon. 1999. Salicylic acid-independent plant defense pathways. Trends Plant Sci.4:52-58.
    OpenUrlCrossRefPubMedWeb of Science
  135. 135.↵
    Ping, L., and W. Boland. 2004. Signals from the underground: bacterial volatiles promote growth in Arabidopsis.Trends Plant Sci.9:263-269.
    OpenUrlCrossRefPubMed
  136. 136.↵
    Postma, J., M. Montanari, and P. H. J. F. van den Boogert. 2003. Microbial enrichment to enhance the disease suppressive activity of compost. Eur. J. Soil Biol.39:157-163.
    OpenUrlCrossRefWeb of Science
  137. 137.↵
    Raaijmakers, J. M., I. Vandersluis, M. Koster, P. A. H. M. Bakker, P. J. Weisbeek, and B. Schippers. 1995. Utilization of heterologous siderophores and rhizosphere competence of fluorescent Pseudomonas spp. Can. J. Microbiol.41:126-135.
    OpenUrl
  138. 138.↵
    Raaijmakers, J. M., M. Vlami, and J. T. de Souza. 2002. Antibiotic production by bacterial biocontrol agents. Antonie Leeuwenhoek81:537-547.
    OpenUrlCrossRefPubMedWeb of Science
  139. 139.↵
    Ramamoorthy, V., R. Viswanathan, T. Raguchander, V. Prakasam, and R. Smaiyappan. 2001. Induction of systemic resistance by plant growth-promoting rhizobacteria in crop plants against pests and diseases. Crop Prot.20:1-11.
    OpenUrlCrossRef
  140. 140.↵
    Raupach, G. S., and J. W. Kloepper. 1998. Mixtures of plant growth-promoting rhizobacteria enhance biological control of multiple cucumber pathogens. Phytopathology88:1158-1164.
    OpenUrlCrossRefPubMedWeb of Science
  141. 141.↵
    Ravel, J., and P. Cornelis. 2003. Genomics of pyoverdine-mediated iron uptake in pseudomonads. Trends Microbiol.11:195-200.
    OpenUrlCrossRefPubMedWeb of Science
  142. 142.↵
    Reinhold, B., T. Hurek, and I. Fendrik. 1985. Strain-specific chemotaxis of Azospirillum spp. J. Bacteriol.162:190-195.
    OpenUrlAbstract/FREE Full Text
  143. 143.↵
    Rovira, A. D. 1965. Interactions between plant roots and soil microorganisms. Annu. Rev. Microbiol.19:241-266.
    OpenUrlCrossRefPubMedWeb of Science
  144. 144.↵
    Ryan, P. R., E. Delhaize, and D. L. Jones. 2001. Function and mechanism of organic anion exudation from plant roots. Annu. Rev. Plant Physiol. Plant Mol. Biol.52:527-560.
    OpenUrlCrossRefPubMedWeb of Science
  145. 145.↵
    Ryu, C.-M., M. A. Farag, C. H. Hu, M. S. Reddy, J. W. Kloepper, and P. W. Paré. 2004. Bacterial volatiles induce systemic resistance in Arabidopsis.Plant Physiol.134:1017-1026.
    OpenUrlAbstract/FREE Full Text
  146. 146.↵
    Ryu, C. M., J. F. Murphy, K. S. Mysore, and J. W. Kloepper. 2004. Plant growth-promoting rhizobacterial systemically protect Arabidopsis thaliana against Cucumber mosaic virus by a salicylic acid and NPR1-independent and jasmonic acid-dependent signaling pathway. The Plant J.39:381-392.
    OpenUrlCrossRefPubMedWeb of Science
  147. 147.↵
    Sacherer, P., G. Défago, and D. Hass. 1994. Extracellular protease and phospholipase C are controlled by the global regulatory gene gacA in the biocontrol strain Pseudomonas fluorescens CHA0. FEMS Microbiol. Lett.116:155-160.
    OpenUrlCrossRefPubMedWeb of Science
  148. 148.↵
    Saleh, S. S., and B. R. Glick. 2001. Involvement of gacS and rpoS in enhancement of the plant growth promoting capabilities of Enterobacter cloacae CAL2 and UW4. Can. J. Microbiol.47:698-705.
    OpenUrlCrossRefPubMedWeb of Science
  149. 149.↵
    Sánchez-Contreras, M., M. Martín, M. Villacieros, F. O'Gara, I. Bonilla, and R. Rivilla. 2002. Phenotypic selection and phase variation occur during alfalfa root colonization by Pseudomonas fluorescens F113. Appl. Environ. Microbiol.184:1587-1596.
    OpenUrl
  150. 150.↵
    Schisler, D. A., P. J. Slininger, and R. J. Bothast. 1997. Effects of antagonist cell concentration and two-strain mixtures on biological control of Fusarium dry rot of potatoes. Phytopathology87:177-183.
    OpenUrlCrossRefPubMedWeb of Science
  151. 151.↵
    Schnider-Keel, U., A. Seematter, M. Maurhofer, C. Blumer, B. Duffy, C. Gigot-Bonnefoy, C. Reimmann, R. Notz, G. Défago, D. Haas, and C. Keel. 2000. Autoinduction of 2,4-diacetylphloroglucinol biosynthesis in the biocontrol agent Pseudomonas fluorescens CHA0 and repression by the bacterial metabolites salicylate and pyoluteorin. J. Bacteriol.182:1215-1225.
    OpenUrlAbstract/FREE Full Text
  152. 152.↵
    Schouten, A., G. van der Berg, V. Edel-Hermann, C. Steinberg, N. Gautheron, C. Alabouvette, C. H. de Vos, P. Lemanceau, and J. M. Raaijmakers. 2004. Defense responses of Fusarium oxysporum to 2,4-diacetylphloroglucinol, a broad-spectrum antibiotic produced by Pseudomonas fluorescens.Mol. Plant-Microbe Interact.17:1201-1211.
    OpenUrlCrossRefPubMedWeb of Science
  153. 153.↵
    Schroth, M. N., and J. G. Hancock. 1981. Selected topics in biological control. Annu. Rev. Microbiol.35:453-476.
    OpenUrlCrossRefPubMed
  154. 154.↵
    Sessitsch, A., B. Reiter, and G. Berg. 2004. Endophytic bacterial communities of field-grown potato plants and their plant growth-promoting and antagonistic abilities. Can. J. Microbiol.50:239-249.
    OpenUrlCrossRefPubMedWeb of Science
  155. 155.↵
    Sessitsch, A., T. Coenye, A. V. Sturz, P. Vandamme, E. Ait Barka, J. F. Salles, J. D. van Elsas, D. Faure, B. Reiter, B. R. Glick, G. Wang-Pruski, and J. Nowak. 2005. Burkholderia phytofirmans sp. nov., a novel plant-associated bacterium with plant beneficial properties. Int. J. Syst. Evol. Microbiol.55:1187-1192.
    OpenUrlCrossRefPubMedWeb of Science
  156. 156.↵
    Sharma, V. K., and J. Nowak. 1998. Enhancement of verticillium wilt resistance in tomato transplants by in vitro coculture of seedlings with a plant growth-promoting rhizobacterium (Pseudomonas sp. strain PsJN). Can. J. Microbiol.44:528-536.
    OpenUrlCrossRef
  157. 157.↵
    Simons, M., A. J. van der Bij, L. A. de Weger, C. A. Wijffelman, and B. J. Lugtenberg. 1996. Gnotobiotic system for studying rhizosphere colonization by plant growth-promoting Pseudomonas bacteria. Mol. Plant-Microbe Interact.9:600-607.
    OpenUrlCrossRefPubMedWeb of Science
  158. 158.↵
    Simons, M., H. P. Permentier, L. A. de Weger, C. A. Wijffelman, and B. J. J. Lugtenberg. 1997. Amino acid synthesis is necessary for tomato root colonization by Pseudomonas fluorescens strain WCS365. Mol. Plant-Microbe Interact.10:102-106.
    OpenUrlCrossRefWeb of Science
  159. 159.↵
    Singh, P. P., Y. C. Shin, C. S. Park, and Y. R. Chung. 1999. Biological control of Fusarium wilt of cucumber by chitinolytic bacteria. Phytopathology89:92-99.
    OpenUrlCrossRefPubMedWeb of Science
  160. 160.↵
    Smith, K. P., and R. M. Goodman. 1999. Host variation for interactions with beneficial plant-associated microbes. Annu. Rev. Phytopathol.37:473-491.
    OpenUrlCrossRefPubMedWeb of Science
  161. 161.↵
    Smith, K. P., J. Handelsman, and R. M. Goodman. 1999. Genetic basis in plants for interactions with disease-suppressive bacteria. Proc. Natl. Acad. Sci. USA96:4786-4790.
    OpenUrlAbstract/FREE Full Text
  162. 162.↵
    Steenhoudt, O., and J. Vanderleyden. 2000. Azospirillum, a free-living nitrogen-fixing bacterium closely associated with grasses: genetic, biochemical and ecological aspects. FEMS Microbiol. Rev.24:487-506.
    OpenUrlCrossRefPubMedWeb of Science
  163. 163.↵
    Strom, M. S., and S. Lory. 1993. Structure-function and biogenesis of the type IV pili. Annu. Rev. Microbiol.30:565-596.
    OpenUrlCrossRef
  164. 164.↵
    Sturz, A. V., B. R. Christie, B. G. Matheson, W. J. Arsenault, and N. A. Buchanan. 1999. Endophytic bacterial communities in the epiderm of potato tubers and their potential to improve resistance to soil-borne plant pathogens. Plant Pathol.48:360-369.
    OpenUrlCrossRef
  165. 165.↵
    Sturz, A. V., B. R. Christie, and J. Nowak. 2000. Bacterial endophytes: potential role in developing sustainable systems of crop production. Crit. Rev. Plant Sci.19:1-30.
    OpenUrlCrossRefWeb of Science
  166. 166.↵
    Sturz, A. V., and B. R. Christie. 2003. Beneficial microbial allelopathies in the root zone: the management of soil quality and plant disease with rhizobacteria. Soil Tillage Res.72:107-123.
    OpenUrlCrossRef
  167. 167.↵
    Thomashow, L. S. 1996. Biological control of plant root pathogens. Curr. Opin. Biotechnol.7:343-347.
    OpenUrlCrossRefPubMedWeb of Science
  168. 168.↵
    Timms-Wilson, T. M., R. J. Ellis, A. Renwick, D. J. Rhodes, D. V. Mavrodi, D. M. Weller, L. S. Thomashow, and M. J. Bailey. 2000. Chromosomal insertion of phenazine-1-carboxylic acid biosynthetic pathway enhances efficacy of damping-off disease control by Pseudomonas fluorescens.Mol. Plant-Microbe Interact.13:1293-1300.
    OpenUrlCrossRefPubMedWeb of Science
  169. 169.↵
    Toyoda, H., H. Hashimoto, R. Utsumi, H. Kobayashi, and S. Ouchi. 1988. Detoxification of fusaric acid by a fusaric acid-resistant mutant of Pseudomonas solanacearum and its application to biological control of fusarium wilt of tomato. Phytopathology78:1307-1311.
    OpenUrlCrossRef
  170. 170.↵
    Toyoda, H., and R. Utsumi. January 1991. Method for the prevention of Fusarium diseases and microorganisms used for the same. U.S. patent 4,988,586.
  171. 171.↵
    Turnbull, G. A., J. A. W. Morgan, J. M. Whipps, and J. R. Saunders. 2001. The role of motility in the in vitro attachment of Pseudomonas putida PaW8 to wheat roots. FEMS Microbiol. Ecol.35:57-65.
    OpenUrlCrossRefPubMedWeb of Science
  172. 172.↵
    Turnbull, G. A., J. A. W. Morgan, J. M. Whipps, and J. R. Saunders. 2001. The role of bacterial motility in the survival and spread of Pseudomonas fluorescens in soil and in the attachment and colonization of wheat roots. FEMS Microbiol. Ecol.36:21-31.
    OpenUrlCrossRefPubMedWeb of Science
  173. 173.↵
    Uroz, S., C. D'Angelo-Picard, A. Carlier, M. Elasri, C. Sicot, A. Petit, P. Oger, D. Faure, and Y. Dessaux. 2003. Novel bacteria degrading N-acylhomoserine lactones and their use as quenchers of quorum-sensing-regulated functions of plant-pathogenic bacteria. Microbiology149:1981-1989.
    OpenUrlCrossRefPubMedWeb of Science
  174. 174.↵
    Van der Broek, D., T. F. C. Chin-A-Woeng, K. Eijkemans, I. H. M. Mulders, G. V. Bloemberg, and B. J. J. Lugtenberg. 2003. Biocontrol traits of Pseudomonas spp. are regulated by phase variation. Mol. Plant-Microbe Interact.16:1003-1012.
    OpenUrlCrossRefPubMedWeb of Science
  175. 175.↵
    Van Loon, L. C., P. A. H. M. Bakker, and C. M. J. Pieterse. 1998. Systemic resistance induced by rhizosphere bacteria. Annu. Rev. Phytopathol.36:453-483.
    OpenUrlCrossRefPubMedWeb of Science
  176. 176.↵
    Van Overbeek, L. S., and J. D. Van Elsas. 1995. Root exudates-induced promoter activity in Pseudomonas fluorescens mutants in the wheat rhizosphere. Appl. Environ. Microbiol.61:890-898.
    OpenUrlAbstract/FREE Full Text
  177. 177.↵
    Van Peer, R., H. L. M. Punte, L. A. de Weger, and B. Schippers. 1990. Characterization of root surface and endorhizosphere pseudomonads in relation to their colonization of roots. Appl. Environ. Microbiol.56:2462-2470.
    OpenUrlAbstract/FREE Full Text
  178. 178.↵
    Van Peer, R., G. J. Niemann, and B. Schippers. 1991. Induced resistance and phytoalexin accumulation in biological control of Fusarium wilt of carnation by Pseudomonas sp. strain WCS417r. Phytopathology81:728-734.
    OpenUrlCrossRefWeb of Science
  179. 179.↵
    van Wees, S., C. Pieterse, A. Trijssenaar, Y. Van't Westende, F. Hartog, and L. C. van Loon. 1997. Differential induction of systemic resistance in Arabidopsis by biocontrol bacteria. Mol. Plant-Microbe Interact.10:716-724.
    OpenUrlCrossRefPubMedWeb of Science
  180. 180.↵
    van Wees, S. C. M., M. Luijendijk, I. Smoorenburg, L. C. van Loon, and C. M. J. Pieterse. 1999. Rhizobacteria-mediated induced systemic resistance (ISR) in Arabidopsis is not associated with a direct effect on expression of known defense-related genes but stimulates the expression of the jasmonate-inducible gene Atvsp upon challenge. Plant Mol. Biol.41:537-549.
    OpenUrlCrossRefPubMedWeb of Science
  181. 181.↵
    von Bodman, S. B., W. D. Bauer, and D. L. Coplin. 2003. Quorum sensing in plant-pathogenic bacteria. Annu. Rev. Phytopathol.41:455-482.
    OpenUrlCrossRefPubMedWeb of Science
  182. 182.↵
    Viswanathan, R., and R. Samiyappan. 1999. Induction of systemic resistance by plant growth-promoting rhizobacteria against red rot disease caused by Colletotrichum falcatum went in sugarcane, p. 24-39. InProceedings of the Sugar Technology Association of India,vol. 61. Sugar Technology Association, New Delhi, India.
    OpenUrl
  183. 183.↵
    Walker, M. J., R. G. Birch, and J. M. Pemberton. 1988. Cloning and characterization of an albicidin resistance gene from Klebsiella oxytoca.Mol. Microbiol.2:443-454.
    OpenUrlCrossRefPubMed
  184. 184.↵
    Walsh, U. F., Morrissey, J. P., and F. O'Gara. 2001. Pseudomonas for biocontrol of phytopathogens: from functional genomics to commercial exploitation. Curr. Opin. Biotechnol.12:289-295.
    OpenUrlCrossRefPubMedWeb of Science
  185. 185.↵
    Wang, C., E. Knill, B. R. Glick, and G. Défago. 2000. Effect of transferring 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase genes into Pseudomonas fluorescens strain CHA0 and its gacA derivative CHA96 on their growth-promoting and disease-suppressive capacities. Can. J. Microbiol.46:898-907.
    OpenUrlCrossRefPubMedWeb of Science
  186. 186.↵
    Wang, Y., H. N. Brown, D. E. Crowley, and P. J. Szaniszlo. 1993. Evidence for direct utilization of a siderophore, ferrioxamine B in axenically grown cucumber. Plant Cell Environ.16:579-585.
    OpenUrlCrossRef
  187. 187.↵
    Wei, L., J. W. Kloepper, and S. Tuzun. 1991. Induction of systemic resistance of cucumber to Colletotrichum orbiculare by select strains of plant growth-promoting rhizobacteria. Phytopathology81:1508-1512.
    OpenUrlCrossRefWeb of Science
  188. 188.↵
    Welbaum, G., A. V. Sturz, Z. Dong, and J. Nowak. 2004. Fertilizing soil microorganisms to improve productivity of agroecosystems. Crit. Rev. Plant Sci.23:175-193.
    OpenUrlCrossRefWeb of Science
  189. 189.↵
    Weller, D. M. 1988. Biological control of soilborne plant pathogens in the rhizosphere with bacteria. Annu. Rev. Phytopathol.26:379-407.
    OpenUrlCrossRefWeb of Science
  190. 190.↵
    Whipps, J. M. 1997. Developments in the biological control of soil-borne plant pathogens. Adv. Bot. Res.26:1-133.
    OpenUrl
  191. 191.↵
    Whipps, J. M. 2001. Microbial interactions and biocontrol in the rhizosphere. J. Exp. Bot.52:487-511.
    OpenUrlCrossRefPubMedWeb of Science
  192. 192.↵
    Yamaki, M., M. Miwa, K. Ishiguro, and S. Takagi. 1994. Antimicrobial activity of naturally occurring and synthetic phloroglucinols against Staphylococcus aureus.Phytother. Res.8:112-114.
    OpenUrlCrossRef
  193. 193.↵
    Zala, M., C. Gyawali, B. Duffy, K. Keel, and G. Défago. 1999. Application of phloroglucinol (PHL) production as a phenotypic marker for selecting better biocontrol bacteria. Phytopathology89:88-89.
    OpenUrl
  194. 194.↵
    Zhang, L., and R. G. Birch. 1996. Biocontrol of sugar cane leaf scald disease by an isolate of Pantoea dispersa which detoxifies albicidin phytotoxins. Lett. Appl. Microbiol.22:132-136.
    OpenUrlCrossRef
  195. 195.↵
    Zhang, L., and R. G. Birch. 1997. The gene for albicidin detoxification from Pantoea dispersa encodes an esterase and attenuates pathogenicity of Xanthomonas albilineans to sugarcane. Proc. Natl. Acad. Sci. USA94:9984-9989.
    OpenUrlAbstract/FREE Full Text
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Use of Plant Growth-Promoting Bacteria for Biocontrol of Plant Diseases: Principles, Mechanisms of Action, and Future Prospects
Stéphane Compant, Brion Duffy, Jerzy Nowak, Christophe Clément, Essaïd Ait Barka
Applied and Environmental Microbiology Sep 2005, 71 (9) 4951-4959; DOI: 10.1128/AEM.71.9.4951-4959.2005

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Use of Plant Growth-Promoting Bacteria for Biocontrol of Plant Diseases: Principles, Mechanisms of Action, and Future Prospects
Stéphane Compant, Brion Duffy, Jerzy Nowak, Christophe Clément, Essaïd Ait Barka
Applied and Environmental Microbiology Sep 2005, 71 (9) 4951-4959; DOI: 10.1128/AEM.71.9.4951-4959.2005
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  • Top
  • Article
    • COMPETITIVE ROOT COLONIZATION
    • BIOCONTROL ACTIVITY MEDIATED BY THE SYNTHESIS OF ALLELOCHEMICALS
    • INDIRECT PLANT GROWTH PROMOTION THROUGH INDUCED SYSTEMIC RESISTANCE
    • CONCLUSIONS AND FUTURE PROSPECTS TO MAKE BETTER USE OF PGPB
    • ACKNOWLEDGMENTS
    • REFERENCES
  • Info & Metrics
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KEYWORDS

bacteria
Pest Control, Biological
Plant Development
Plant Diseases

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