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Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Beneficial interactions
  5. Harmful interactions
  6. Concluding remarks
  7. Acknowledgements
  8. References

Plant growth and development are significantly influenced by the presence and activity of microorganisms. To date, the best-studied plant-interacting microbes are Gram-negative bacteria, but many representatives of both the high and low G+C Gram-positives have excellent biocontrol, plant growth-promoting and bioremediation activities. Moreover, actinorhizal symbioses largely contribute to the global biological nitrogen fixation and many Gram-positive bacteria promote other types of symbioses in tripartite interactions. Finally, several prominent and devastating phytopathogens are Gram-positive. We summarize the present knowledge of the beneficial and detrimental interactions of Gram-positive bacteria with plants to underline the importance of this particular group of bacteria.


Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Beneficial interactions
  5. Harmful interactions
  6. Concluding remarks
  7. Acknowledgements
  8. References

The surfaces and surroundings of plants form a nutrient-rich habitat for complex microbial populations that can positively or negatively influence plant health and growth. Moreover, bacteria can attack, repel, antagonize, compete or collaborate with other organisms affecting the composition of the microbial communities and plant development (Welbaum et al., 2004).

The most extensively studied bacteria interacting with plants are Gram-negatives because they are readily isolated from plant tissues, easily handled, and amenable to genetic approaches. The impact of Gram-positive bacteria on plants is far less documented but should not be underestimated. Typically, the Gram-positives differ from the Gram-negatives in their cell wall structure that mainly consists of peptidoglycan, forming a thick barrier surrounding the plasma membrane. Many Gram-positive bacteria are pigmented, form spores, produce a plethora of bioactive secondary metabolites and/or have specialized lifestyles that can be advantageous for agricultural applications. Although the best-known Gram-positives are human and animal pathogens, such as Mycobacterium tuberculosis, Bacillus anthracis, Clostridium botulinum and Rhodococcus equi, a number of economically significant phytopathogens and biocontrol bacteria belong to this group. These plant-associated bacteria occur in the two Gram-positive phyla, the Firmicutes and the Actinobacteria. The Firmicutes have a low G+C content and encompass the classes of the Bacilli, the Clostridia, the Erysipelotrichi, the Thermolithobacteria and the Mollicutes. The Actinobacteria have a high G+C content and consist of a single class. By means of specific examples we give an overview of the current knowledge on the beneficial and harmful interactions of Gram-positive bacteria with plants (schematically represented in Fig. 1) and illustrate that this group of bacteria deserves its fair share of research attention in the field of plant–microbe interactions.

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Figure 1. Schematic representation of the diversity of plant interactions in which Gram-positive bacteria are implicated. Beneficial bacteria (light coloured), detrimental bacteria (dark coloured) and soil pollutants (blue particles). Leaf tissues: cuticle (black), epidermis (orange), palisade parenchyma (dark green), spongy parenchyma (light green), xylem (red) and phloem (blue); stem tissues: epidermis (orange), cortical parenchyma (dark grey), pith (light grey), xylem (red) and phloem (blue); and root tissues: epidermis (orange), cortical parenchyma (brown), endodermis (purple), xylem (red) and phloem (blue).

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Beneficial interactions

  1. Top of page
  2. Summary
  3. Introduction
  4. Beneficial interactions
  5. Harmful interactions
  6. Concluding remarks
  7. Acknowledgements
  8. References

Plant growth promotion and biofertilization

Plant growth can be promoted by a diversity of mechanisms that increase nutrient accessibility, facilitate mineral and nutrient uptake, decrease soil toxicity, release growth-stimulating phytohormones, modulate hormone production by the plant, supply nitrogen and phosphate via symbioses, or enhance the effects of symbioses (Welbaum et al., 2004; Podile and Kishore, 2006). Most plant growth-promoting (PGP) bacteria inhabit the plant rhizosphere and/or rhizoplane, but potentially beneficial phyllosphere and endophytic bacteria have been isolated as well (Kishore et al., 2005). Besides agricultural benefits, such as improving crop yield, PGP bacteria can be important partners of pioneer plants for revegetation and reforestation of barren or contaminated soils (Bashan and Holguin, 2002).

Mineral nutrient solubilization.  In many soils, essential mineral nutrients are largely unavailable to plants because they are fixed in insoluble forms. By secreting specific enzymes or chelators, microorganisms can improve the bioavailability of essential compounds. For example, in soil, organic phosphorus is stored mainly as insoluble myo-inositol hexaphosphate or phytate. Many rhizosphere bacteria can solubilize phosphorus from phytate by secreting active phytases. The most efficient Gram-positive strains that promote plant growth in this manner belong to the genus Bacillus, but high phytase activity has also been reported for Brevibacterium, Sarcina, Paenibacillus, Corynebacterium and Micrococcus strains (Jorquera et al., 2008). Other strains, including Bacillus spp. and Paenibacillus macerans, release phosphorus from rock sediments through the secretion of organic acids (Vazquez et al., 2000). Bacillus mucilaginosus promotes growth of tobacco by dissolving potassium from feldspar and phosphorus from calcium phosphate; introduction of the phyA gene of Aspergillus fumigatus resulted in a transgenic strain NKTS-3 with increased soil-improving properties and a superior PGP effect (Li et al., 2007).

The most prevailing form of iron in the soil, Fe3+, is relatively insoluble compared with the more reduced Fe2+ ions that are readily taken up by plants and microorganisms. Several bacteria can reduce metals, potentially increasing the bioavailability of iron. Such a PGP mechanism has been demonstrated for Bacillus megaterium and Arthrobacter maltophilia on common bean grown in alkaline soil (Valencia-Cantero et al., 2007). Although plants themselves secrete siderophores or chelators to facilitate iron uptake, some plant species recognize and use siderophores synthesized by rhizospheric bacteria. However, because bacterial siderophore production also mediates iron competition in bacterial communities, the direct contribution of these molecules in iron-related plant growth stimulation remains a matter of debate (Beattie, 2006).

Phytohormones.  Many rhizosphere microbes produce and secrete phytohormones or mimics thereof and, thus, directly modulate plant growth. A diverse group of Gram-positive bacteria, including Arthrobacter, Micrococcus, Bacillus, Rhodococcus, Mycobacterium, Microbacterium, Streptomyces and Corynebacterium species, are capable of producing auxin that might stimulate nutrient uptake and root proliferation (Tsavkelova et al., 2006; Spaepen et al., 2007). Bacterization of different terrestrial and epiphytic orchid seeds with indole-3-acetic acid (IAA)-producing Bacillus pumilus KM MGU 467 improved seed germination and stimulated orchid development (Kolomeitseva et al., 2006).

Plant-associated Rhodococcus spp. and B. pumilus often display 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase activity and use ACC as a nitrogen source by hydrolyzing it to ammonium and α-ketobutyrate. The ACC concentration in plants associated with these bacteria is lowered and, consequently, stress-induced ethylene accumulation is reduced. Hence, bacterial ACC deaminase activity has the potential to sustain and improve plant growth under unfavourable environmental conditions (Arshad et al., 2007). Indeed, an Arthrobacter and a Bacillus species, positive for IAA production and ACC deaminase activity, increased the ability of pepper plants to cope with abiotic stress (Sziderics et al., 2007).

Similarly, inoculation of lettuce plants with cytokinin-producing Bacillus subtilis has a beneficial effect on plant growth under moderate drought stress and leads to accumulation of this hormone in the plant tissues and to an increased biomass (Arkhipova et al., 2007). Likewise, the impact of Paenibacillus polymyxa on plant growth is strong through the production of cytokinin and auxin (Lal and Tabacchioni, 2009).

Finally, ABA and jasmonic acid produced by endophytic B. pumilis strains isolated from sunflower (Forchetti et al., 2007) and gibberellin secreted by several plant-associated Bacillus, Micrococcus, Arthrobacter and Clostridium species (Joo et al., 2005; Tsavkelova et al., 2006) promote plant growth as well.

Bioremediation.  Contamination of soils with heavy metals, such as mercury (Hg), lead (Pb), cadmium (Cd), chromium (Cr), copper, nickel (Ni) and zinc, or toxic organic compounds, such as polychlorinated biphenyls (PCBs), polycyclic aromatic hydrocarbons (PAHs) and other halogenated compounds, decreases crop yield by causing stress-induced ethylene accumulation and reduced nutrient consumption (Khan et al., 2009). Such a pollution represents an important loss of fertile land and a severe threat to human health. Bioremediation mediated by plants via the uptake and/or degradation of pollutants is called phytoremediation. By stimulating seed germination, plant growth and root biomass through the mechanisms discussed above, contamination-tolerant PGP rhizobacteria and endophytes can improve the remediation capacity of plants (Pilon-Smits, 2005; Khan et al., 2009). Inoculation with B. subtilis strain SJ-101 of Brassica juncea growing on Ni-stressed sites resulted in high Ni concentrations in the plant tissues and an increased plant biomass as a combined effect of bacterial IAA production, solubilization of inorganic phosphate and adsorption of Ni (Khan et al., 2009).

Alternatively, some PGP bacteria can actively degrade the pollutants or prevent their accumulation in plant tissues. The presence of Arthrobacter mysorens 7, resistant to Cd and Pb, in the rhizosphere of barley growing in heavy-metal-contaminated soil improved plant growth and prevented heavy metal accumulation in the plant tissues. Several Bacillus strains isolated from Cr-contaminated soil reduced the highly toxic, mutagenic and carcinogenic Cr6+ to the less toxic Cr3+ (Khan et al., 2009). Psychotrophic Rhodococcus erythropolis MtCC7905 collected from a metal-contaminated site in the Himalayan region exhibited various PGP features and a chromate-reducing ability at temperatures as low as 10°C (Trivedi et al., 2007). Identification of such organisms holds the potential to extend phytoremediation to soils under low temperature and metal toxicity stress.

Plants can stimulate growth of specific pollutant-degrading bacteria in their rhizosphere via nutrient-rich root exudates and they can facilitate the microbial biodegradation capacity by secreting phospholipid surfactants that make organic pollutants more available or by releasing secondary metabolites that induce the expression of degradative genes, a process called rhizodegradation or phytostimulation (Pilon-Smits, 2005). Rhodococcus spp. were the most prevalent group of culturable PCB degraders in the rhizosphere of trees naturally colonizing a PCB-contaminated site in the Czech Republic (van der Geize and Dijkhuizen, 2004).

Barley growing in soils contaminated with PAH due to fossil fuel combustion, asphalt production, wood preservation or coal processing supported growth of a specialized Mycobacterium species that could mineralize PAH (Child et al., 2007). Oil-contaminated soils typically contain high concentrations of m-toluate. Although Pseudomonas spp. are the best m-toluate degraders in the rhizospheric populations of Galega orientalis grown on such soils, most isolates were Gram-positive strains of the genera Rhodococcus, Arthrobacter, Bacillus and Nocardia. Interestingly, also m-toluate-tolerant bacteria unable to degrade the pollutant were present and acted as co-metabolizers (Jussila et al., 2006).

Biocontrol

Biocontrol refers to the suppression of phytopathogens by resident or introduced organisms and often results in plant growth promotion. Direct interference can be accomplished through diverse antimicrobial compounds (antibiosis), competition for iron by siderophore production or for colonization sites and/or nutrients, inactivation of pathogen germination factors, degradation of pathogenicity factors or parasitism of the pathogen. An indirect biocontrol mechanism involves the induction of systemic resistance in plants by harmless or beneficial bacteria. However, disease suppression mostly results from the simultaneous implementation of multiple mechanisms exhibited by one or several biocontrol agents (Beattie, 2006).

Characterization of biocontrol bacteria associated with plants and crops depends on efficient isolation and screening methods. The commonly used culture-dependent isolation methods mainly detect Pseudomonas and other Gram-negative species (Fravel, 2005). However, when screening procedures are focused on antibiosis, Gram-positives, predominately representatives of the Actinomycetales and Bacillus spp., are isolated that have properties superior to those of their Gram-negative counterparts or show different or complementary action spectra (El-Tarabily and Sivasithamparam, 2006). Additional biocontrol Gram-positives are anticipated to be identified by culturability-independent approaches, such as metagenomics and methods based on fatty acid analysis.

Antibiosis.  A typical example of disease control through antibiosis is the natural suppressive soil for the Streptomyces scabies-induced potato scab. The non-pathogenic Streptomyces diastatochromogenes strains PonR and PonSSII exert biocontrol activities against S. scabies through antibiotic production and competitive exclusion from infection sites (Neeno-Eckwall et al., 2001). Bacillus sp. Sunhua produces the lipopeptide iturin A and the polyene macrolide macrolactin A that disrupt and inhibit formation of the pathogen's mycelia and prevent sporulation (Han et al., 2005). Bacillus cereus strain UW85 suppresses disease via the production of the antibiotics aminopolyol zwittermicin A and aminoglycoside kanosamine, which affect oomycetes (Emmert and Handelsman, 1999). Bacillus thuringiensis probably represents the best-described case of bacteria with insecticidal activity. During sporulation, crystals of the Cry protein are formed that are toxic to many insect species because it causes pore formation in the membranes of the insect gut. This microbial insecticide has been used widely to control insect pests and transgenic plants containing the endotoxin-encoding cry genes are cultivated successfully worldwide (Rosas-García, 2009).

Mycoparasitism.  A different biocontrol mechanism, well established within the order of the Actinomycetales, depends on the destruction of fungal cell walls by extracellular bacterial hydrolytic enzymes, such as β-1,3-glucanases and chitinases. Streptomyces violaceusniger YCED-9 combines antibiosis and mycoparasitism and exhibits a strong antagonism against fungi of different taxonomic groups (Trejo-Estrada et al., 1998). Good candidates for biocontrol are chitin-degrading soil isolates related to Streptomyces griseus, Bacillus chitinolyticus and Bacillus ehimensis (Hoster et al., 2005). Bacillus subtilis AF1 has antifungal properties through the secretion of β-1,4-N-acetyl glucosaminidase and a β-1,3-glucanase (Manjula and Podile, 2005). Actinomycetes of the Micromonosporaceae, such as Amorphosporangium auranticolor, Ampullariella regularis, Spirillospora albida, and Actinoplanes and Micromonospora spp., form hyphae that coil around oospores and cause cytoplasmic collapse (El-Tarabily and Sivasithamparam, 2006).

Induction of systemic resistance.  Plants possess a basal immunity and multiple layers of defence responses that can be triggered systemically, thus reducing the incidence or the severity of diseases. Systemic acquired resistance (SAR) is the long-lasting protection against a broad spectrum of microorganisms, resulting from defence activation through prior infections with a pathogen. Induced systemic resistance (ISR) has a similar outcome, but the defence mechanisms in the plant are elicited via colonization by PGP bacteria. The combination of ISR and PGP activities in single organisms offers opportunities for their use as booster inoculants in agriculture and horticulture (Valad and Goodman, 2004). The best-known Gram-positive ISR-activating species belong to the genera Bacillus (Kloepper et al., 2004) and Streptomyces (Lehr et al., 2008). Recent studies on the PGP strains B. subtilis GB03 and Bacillus amiloliquefaciens IN937a have revealed the elicitation of ISR through the bacterial production of volatile organic compounds (Kloepper et al., 2004).

Endophytic colonization.  Endophytes have attracted attention as potential biocontrol agents because, inside the plant, these organisms are expected to be better protected against environmental fluctuations, stress and microbial competition (Sturz et al., 2000; Franco et al., 2007). Evidence suggests that plants select specific endophytes present in the soil or rhizosphere that confer protection against phytopathogens (Rosenblueth and Martínez-Romero, 2006). The biocontrol mechanisms exhibited by endophytic bacteria are similar to those of rhizospheric or epiphytic populations. For example, the endophyte Paenibacillus sp. HKA-15 produces antifungal peptide antibiotics that protect soybean against Rhizoctonia bataticola that causes charcoal rot disease (Lal and Tabacchioni, 2009). The B. pumilus strain SE34 stimulates plant defences and renders the host plant (pea) less sensitive to infection by Fusarium oxysporum f. sp. pisi (Jacobsen et al., 2004). Endophytic actinobacteria, such as Streptomyces sp. strain EN27 and Micromonospora sp. strain EN43, activate key genes in the SAR and jasmonate/ethylene pathways (Conn et al., 2008), whereas Curtobacterium spp. act via both antibiosis and SAR triggering (Raupach and Kloepper, 1998; Sturz et al., 2000). Curtobacterium flaccumfaciens has been isolated frequently from asymptomatic sweet orange trees in orchards infested with Xylella fastidiosa, the causal agent of citrus-variegated chlorosis (CVC). It effectively controls CVC through colonization of the same ecological niche and the production of three bacteriocins active against X. fastidiosa (Lacava et al., 2007).

Integrating strategies and technical advantages

Engineering for biocontrol and plant growth promotion is a challenging task. The soil dynamics, the resident soil microflora with its complex population dynamics, the plant–microbe ecosystem and the abiotic influences have to be taken into account. A reliable outcome of disease suppression in the field can be achieved by combining compatible microorganisms that exhibit different biocontrol mechanisms, are active against various pathogens and are adapted to varying environmental conditions. Mixtures of the Actinomycetales Micromonospora carbonacea and Streptomyces violascens, integrating cellulase production and antibiosis, respectively, have a synergistic effect on plant growth promotion and on suppression of the oomycete Phytophthora cinnamomi that provokes root rot of Banksia grandis (El-Tarabily and Sivasithamparam, 2006). The combination of B. pumilis INR7, B. subtilis GB03 and C. flaccumfaciens ME1 to treat seeds against a range of cucumber pathogens leads to better growth promotion and stronger disease reduction than traditional fumigation methods (Raupach and Kloepper, 1998). The simultaneous application of several Bacillus amyloliquefaciens and B. pumilis strains induces systemic protection against a broad spectrum of diseases in different hosts and increases plant growth and yield (Jetiyanon et al., 2003). A preparation of B. subtilis GB03 and B. amyloliquefaciens IN937a applied to Arabidopsis thaliana elicited plant growth promotion and protection against Pseudomonas syringae pv. tomato and cucumber mosaic virus (Ryu et al., 2007).

However, despite some promising results, pest management is still more efficient when biocontrol agents are supplemented with non-specific resistance elicitors or classical pesticides, or when they can be applied to partially resistant plant cultivars. By application of the pesticide, the biocontrol agent has time to establish itself and to protect the plant after degradation of the pesticide (Jacobsen et al., 2004; Fravel, 2005).

For pest management to be valuable, efficient distribution of bacteria is required, which depends on formulation, storage and delivery technologies. Growth characteristics of Gram-positive biocontrol bacteria, such as hyphal growth and sporulation, are extremely advantageous in this context. Dry formulations of spores combined with inert carriers have an extended shelf life, and can be safely transported, stored and suspended in liquid for easy application (Emmert and Handelsman, 1999; Fravel, 2005). Efficient disease suppression of Fusarium and Rhizoctonia spp. on various crops, such as cotton, is achieved by seed treatment with Kodiak® (Gustafson, Plano, TX, USA): a formulated concentrate of B. subtilis GB03 spores combined with traditional fungicides (Fravel, 2005). Treatment with Kodiak® protects the plant and promotes growth by stimulation of the root system.

Vegetative propagules from actively growing Gram-positive bacterial filaments are also functionally used in dry formulations. Control of Rhizoctonia-induced damping-off disease by a seed-coating powder of lyophilized and pulverized vegetative mycelium of Streptomyces sp. Di-944 was superior to the Streptomyces griseoviridis-based commercial product Mycostop® (Kemira Agro Oy, Helsinki, Finland) (Fravel, 2005). Common potato scab can be controlled by a combination of lyophilized spores of the antibiosis strain Streptomyces melanosporofaciens EF-76 with plant defence-eliciting chitosan (Jobin et al., 2005).

Gram-positive bacteria in tripartite relationships and symbiosis

Plant growth can be improved by microorganisms that engage in nitrogen- and phosphate-delivering symbioses or that stimulate symbiosis in tripartite relationships.

Mycorrhiza helper bacteria.  The majority of the terrestrial plants establish a root symbiosis with mycorrhizal fungi that support plant development under low phosphate availability and protect plants against soil-borne pathogens (Selosse et al., 2006). Mycorrhiza helper bacteria can further improve plant growth by strengthening the mycorrhizal symbiosis (Barea et al., 2005; Frey-Klett et al., 2007). Gram-positive bacteria are more common in such tripartite alliances than Gram-negatives (Frey-Klett et al., 2007). Bacillus subtilis, for instance, promotes root colonization by the fungus Glomus intraradices and, together, these organisms enhance the phosphate availability and increase the absorptive surface area of the roots (Barea et al., 2005). Similarly, the interaction between Bacillus circulans and Glomus sp. 88, and between P. polymyxa and Glomus aggregatum, improved nutrient uptake in wheat and crop yield of the aromatic grass Cymbopogon martini (Singh and Kapoor, 1999; Ratti et al., 2001). Streptomyces spp. that associate with mycorrhizal fungi stimulate mycorrhization of the plant host and exert a biocontrol activity over phytopathogenic fungi. Such a tripartite interaction is found between Streptomyces strain AcH 505, Amanita muscaria, and spruce with inhibition of Armillariella obscura and Heterobasidion annosum. Paenibacillus sp. strain B2 combines biocontrol against fungal plant pathogens via secretion of cellulolytic, proteolytic, chitinolytic and pectinolytic enzymes, with improved mycorrhization of sorghum (Frey-Klett et al., 2007).

Tripartite relationships in legume-rhizobia symbiosis.  Atmospheric dinitrogen is inaccessible to plants and, consequently, nitrogen can be a limiting factor for growth. The ability to fix atmospheric dinitrogen into ammonium is restricted to diazotrophic bacteria that possess the nitrogenase enzyme complex. The best-described nitrogen-fixing symbioses are those between Gram-negative rhizobia and legume crops (Samac and Graham, 2007), but tripartite relationships with Gram-positive bacteria may stimulate nodulation. Retama sphaerocarpa, a drought-adapted legume, is used for the prevention of erosion and desertification in semi-arid and arid areas. Plant survival is promoted through the combined activities of rhizobial symbiosis that provides nitrogen, and B. thuringiensis and the arbuscular mycorrhizal fungus G. intraradices that contribute to a more efficient water use (Marulanda et al., 2006). Similarly, by improving the development of the root system, Bacillus spp. or Curtobacterium luteum stimulate the interaction between rhizobia and legumes (Petersen et al., 1996; Vessey et al., 2004).

Actinorhizal symbiosis and associative nitrogen fixation.  The Gram-positive counterpart of the rhizobia-legume symbiosis is the interaction between actinobacterial Frankia spp. and non-legumes of taxonomically diverse groups of angiosperms, mainly woody shrubs and trees that grow as pioneer plants in poor soils. The annual contribution of these actinorhizal plants to the total amount of fixed nitrogen is estimated to be no less than 25% in terrestrial ecosystems. In contrast to most Gram-negative rhizobia, Frankia spp. are able to fix nitrogen in the free-living state, which accounts in part for their ubiquitous occurrence in poor soils, even in the absence of suitable hosts. They persist by feeding on root exudates of non-host plants and remain infective throughout the saprophytic phase (Mirza et al., 2007; Sellstedt et al., 2007).

Saprophytic Streptomyces, Actinoplanes and Micromonospora spp. can increase actinorhizal nodulation and plant growth in tripartite relationships, as reported for the Discaria trinervis–Frankia symbiosis. Moreover, Frankia and the mycorrhizal fungus Paxillus involutus act synergistically on the performance of Alnus incana ssp. rugosa by providing the plant with a constant source of nitrogen and phosphorus (Roy et al., 2007).

The occurrence of more loose associations in the rhizosphere and the rhizoplane with epiphytic nitrogen-fixing bacteria or with endophytic diazotrophs is widespread. Among the Firmicutes, diazotrophs are largely represented by Bacillus and Paenibacillus spp. (Liu et al., 2006; Ma and Chen, 2008). Also the obligate anaerobes Clostridium and Heliobacterium are nitrogen fixers that occur in association with plants (Minamisawa et al., 2004; Enkh-Amgalan et al., 2006). Among the Actinobacteria, diazotrophic Arthrobacter, Nocardia and Rhodococcus strains are found most frequently in humus of Norway spruce (Elo et al., 2000) and nitrogen-fixing isolates clustering with the Thermomonosporaceae and the Micromonosporaceae have been recovered from surface-sterilized roots of Casuarina equisetifolia (Valdés et al., 2005). Since many of these bacteria also produce PGP compounds, it is difficult to assess the contribution of associative biological nitrogen fixation to plant growth stimulation.

Harmful interactions

  1. Top of page
  2. Summary
  3. Introduction
  4. Beneficial interactions
  5. Harmful interactions
  6. Concluding remarks
  7. Acknowledgements
  8. References

Deleterious rhizobacteria

Deleterious rhizobacteria (DRB) compromise plant growth without actively invading and parasitizing the tissues. They affect plant health indirectly by increasing the susceptibility to other pathogens, but they also have a more direct effect. In the latter case, DRB are considered mild or minor pathogens because they induce subtle and easily overlooked symptoms, such as browning and discoloration of roots, inhibition of root hair development, distortion of leaves and roots, and necrotic lesions. The questionable position of DRB as true pathogens is illustrated by the deleterious effect of some PGP bacteria under certain environmental conditions (Kremer, 2006). For instance, P. polymyxa has been reported to antagonize pathogens and to induce drought tolerance in Arabidopsis, but also to cause root stunting and reduced plant growth (Lal and Tabacchioni, 2009). Leifsonia xyli ssp. cynodontis, isolated from Bermuda grass, provoked symptoms that resemble ratoon stunting disease caused by L. xyli ssp. xyli. The bacteria can colonize the lumen and the pits of xylem vessels and reach titres so high that the sap flow is disturbed, causing leaf chlorosis and plant stunting (Davis and Augustin, 1984).

Gram-positive phytopathogens

A number of economically important phytopathogenic Gram-positives are found in the order of the Actinomycetales, in the families of the Microbacteriaceae, Nocardiaceae and Streptomycetaceae, and in the class of the Mollicutes. The need for eradication procedures created a vivid interest in pathogenic strategies and is reflected in the relatively high number of sequenced genomes of (phyto)pathogens. To date, eight Gram-positive phytopathogens have been sequenced and several others are in progress (http://www.sanger.ac.uk/Projects/Microbes). The increasing number of complete genomic sequences will allow comprehensive comparative genomics to identify mechanisms and genes involved in Gram-positive bacterial plant pathogenicity (Setubal et al., 2005; Hogenhout and Loria, 2008).

Leifsonia xyli ssp. xyli. The first Gram-positive genome to be fully sequenced was that of the obligate endophyte L. xyli ssp. xyli strain CTCB07, the causative agent of ratoon stunting disease of sugarcane and responsible for major losses in the sugar industry (Monteiro-Vitorello et al., 2004). Analysis of the single circular chromosome revealed a high level of genome reduction, presumably indicative of a profound adaptation to a restricted niche, the nutrient-poor xylem. Interestingly, the genetic variation among L. xyli ssp. xyli isolates worldwide is restricted, hinting at spreading of a single pathogenic clone and a rather recent contact with plants as a host (Young et al., 2006). The genome contains four islands, LxxGI1 to LxxGI4, with deviant G+C contents, codon biases, and dinucleotide signatures, and multiple insertion sequences and transposases, suggestive of horizontal gene transfer events. The genomic islands encode several putative virulence factors. For instance, LxxGI2 contains a gene with homology to endopolygalacturonases involved in plant cell wall degradation and LxxGI4 has a pat-1 homologue encoding a serine protease also found in the closely related Clavibacter michiganensis ssp. michiganensis. LxxGI3 carries a homologue of another C. michiganensis ssp. michiganensis virulence gene, celA, encoding a β-1,4-endoglucanase, and a δ-fatty acid desaturase that might produce ABA (Monteiro-Vitorello et al., 2004).

Clavibacter michiganensis.  The genus Clavibacter consists of only one species, C. michiganensis, that causes bacterial wilt and canker in a variety of crops. Epidemic outbursts lead to major economic losses. Clavibacter michiganensis is subdivided according to host plant specificity: ssp. sepedonicus causes ring rot on potato; ssp. nebraskensis is responsible for wilt and blight of maize; ssp. tesselarius induces leaf freckles and leaf spots in wheat; ssp. insidiosus provokes wilting and stunting in alfalfa; and ssp. michiganensis bacterial wilt and canker of tomato. The bacteria infect seeds, can cause latent infections in which no or only mild symptoms develop, and are not destroyed by composting and pasteurization strategies. These characteristics have led to strict international quarantine regulations (Gartemann et al., 2008). The recent observation that C. michiganensis ssp. michiganensis produces several antimicrobial substances that inhibit the ssp. sepedonicus offers an opportunity for the development of a biocontrol strategy (Holtsmark et al., 2007). The genomes of C. michiganensis ssp. sepedonicus (Bentley et al., 2008) and C. michiganensis ssp. michiganensis (Gartemann et al., 2008) have been sequenced and, in both, the virulence genes celA and pat-1 are located on a plasmid. In the two genomes, several homologues of pat-1 are distributed over the chromosome and the plasmids, but the role of these multiple copies is currently unknown (Gartemann et al., 2008). Another virulence-related gene, tomA, is located on the chromosome and encodes a tomatinase, which degrades the antimicrobial saponin (Kaup et al., 2005). Plasmids seem to be essential for symptom development, but genes required for host recognition, efficient colonization, infection and evasion or suppression of plant defence are located on the chromosome (Gartemann et al., 2008).

Scab-causing Streptomyces spp. Streptomyces scabies is the major scab-causing pathogen on several important root and tuber crops, such as potato, carrot, raddish, beet and peanut, and is responsible for considerable annual losses in the USA. Scab symptoms are also provoked by Streptomyces acidiscabies, S. turgidiscabies, S. europaeiscabiei, S. stelliscabiei, S. aureofaciens, S. reticuliscabiei, S. luridiscabiei, S. bottropensis, S. puniciscabiei and S. niveiscabiei, whereas S. ipomoea is the causative agent of soil rot or pox, a widespread and destructive disease of sweet potato (Loria et al., 2006). The genomic sequence of S. scabies strain 87–22 has been determined (Seipke and Loria, 2008). Based on DNA–DNA homology and rRNA sequences, the phytopathogenic streptomycetes show great diversity, but the virulence-associated genes are conserved. Divergent non-pathogenic saprophytic species have probably acquired the ability to infect and colonize plant tissues through horizontal gene transfer of a mobile pathogenicity island (Loria et al., 2006). The pathogenicity island of S. scabies, S. acidiscabies and S. turgidiscabies contains a tomA homologue (Seipke and Loria, 2008) and other pathogenicity genes, such as nec1, a non-ribosomal peptide synthetase, a P450 monooxygenase and a nitric acid synthase involved in thaxtomin production (Loria et al., 2008). Thaxtomins, modified dipeptide phytotoxins that inhibit cellulose synthesis in expanding plant cells, are the main pathogenicity determinants. Full virulence also requires the conserved nec1 gene, which codes for an unknown protein. Bioassays revealed that secreted Nec1 causes necrosis on potato tuber tissue, suggesting a function in colonization of the root meristem or a role in host defence suppression (Joshi and Loria, 2007).

The pathogenicity island of S. turgidiscabies carries an operon that is related to the fasciation (fas) operon of the Gram-positive phytopathogen Rhodococcus fascians and is involved in cytokinin biosynthesis. When inoculated on tobacco or Arabidopsis, S. turgidiscabies induces leafy galls indistinguishable from those induced by R. fascians. Currently, the role of cytokinins in scab disease remains to be determined (Joshi and Loria, 2007).

Rhodococcus fascians.  This ubiquitous soil bacterium has an epiphytic and an endophytic life phase and infections mainly affect the ornamentals industry, because the leafy gall syndrome consists of shoot and flower deformations. The bacteria have a very broad host range that encompasses dicotyledonous and monocotyledonous plants (Putnam and Miller, 2007; Depuydt et al., 2008). Cytokinins play a central role in the virulence and the genes implicated in leafy gall formation are located on a conjugative linear plasmid that is not essential for bacterial growth (Pertry et al., 2009).

The linear plasmid of strain D188, pFiD188, is very similar to catabolic linear plasmids of other Rhodococcus spp., suggesting a common origin (Francis et al., 2007). Non-conserved regions in pFiD188 code for functions involved in the interaction with the plant host and in virulence. The fas operon encodes the cytokinin biosynthesis machinery in which an isopentenyl transferase (ipt) gene plays a central role (Pertry et al., 2009). Cytokinin production via an ipt gene is a virulence determinant that is shared among Gram-positive and Gram-negative gall-inducing bacteria (Sakakibara et al., 2005; Joshi and Loria, 2007; Pertry et al., 2009); nevertheless, the fas operon seems to be restricted to the Gram-positives, suggesting a different biosynthetic strategy or another cytokinin spectrum. The att operon encodes the production of an autoregulatory compound involved in virulence gene expression and the hyp locus is presumably involved in balancing virulence. For the stk and the nrp loci, a more ecological role is postulated (Francis et al., 2007). The chromosome also plays an important role in establishment and adaptation to the plant niche: the vic locus is imperative for endophytic survival because it is involved in the utilization of nutrients available inside the plant and auxin biosynthesis most probably suppresses the host defence (Francis et al., 2007; Depuydt et al., 2009).

Curtobacterium and Rathayibacter.  These genera harbour some important, but less characterized, phytopathogens. Curtobacterium flaccumfaciens has been reported as a biocontrol agent against X. fastidiosa that provokes CVC (Lacava et al., 2007), but the species also includes several pathovars, pv. flaccumfaciens, pv. betae, pv. oortii, pv. poinsettiae, pv. basellae, pv. ilicis and pv. beticola, that cause bacterial leaf spot on bean, red beet, tulip, poinsettia, malabar spinach, American holly and sugar beet, respectively (Chen et al., 2007).

The genus Rathayibacter comprises the phytopathogenic species R. rathayi, R. iranicus, R. tritici and R.  toxicus (Zgurskaya et al., 1993). Juveniles of the plant-pathogenic nematode Anguina transmit the bacteria to a plant host, where they cause gumming disease by secreting large amounts of yellow slime on seed heads, stems and leaves. Infection of grasses with R. toxicus provokes dwarfing, distortion and annual ryegrass toxicity as a consequence of corynetoxin production (glycolipid tunicaminyluracil antibiotics). When lifestock ingest R. toxicus-infected grasses and cereals, corynetoxin poisoning leads to a neurological disorder caused by protein glycosylation inhibition (Finnie, 2006). Corynetoxin production is correlated with the presence of a bacteriophage, but the exact mechanism is unknown (Agarkova et al., 2006).

Phytoplasmas and spiroplasmas. Mollicutes are cell wall-less Gram-positive bacteria derived from a Bacillus/Clostridium-like ancestor. They are insect-transmitted, obligate endophytes with broad plant and insect host ranges, and are often associated with worldwide quarantine infectious plant diseases. Phytoplasmas and spiroplasmas cause an array of symptoms, including witches' broom, phyllody, virescence, bolting, flower alterations, yellowing, phloem necrosis, and general decline and stunting of plants (Hogenhout et al., 2008).

Phytoplasmas form a monophyletic clade, recently assigned to a novel genus ‘Candidatus Phytoplasma’. Examples of diseases are the very aggressive elm yellows, also known as phloem necrosis, which affected historical and new elm plantations in Europe and North America and vineyards of southern France and northern Italy and are responsible for significant losses in apple, pear, plum, apricot, cherry and citrus nurseries (Bertaccini, 2007). With a two-host life cycle, these bacteria adapt to very different environments (Hogenhout et al., 2008). Recently, the genomes of two ‘Candidatus Phytoplasma asteris’ strains [onion yellows mutant (OY-M) and aster yellows witches' broom (AY-WB)], and two ‘Candidatus Phytoplasma australiense’ strains (from Australia and from New Zealand) (Hogenhout et al., 2008; Tran-Nguyen et al., 2008) have been sequenced. Analysis showed a strong genome reduction, the absence of metabolic and regulatory genes previously thought to be essential for autonomously replicating bacteria, and a relatively high frequency of membrane transport systems, likely enabling the uptake of metabolites available in the phloem. Interestingly, no conserved pathogenicity factors were identified, suggesting novel virulence strategies that completely differ from those of the Gram-negative phytopathogens. One approach to deal with changing environments might be encrypted in the highly repetitive nature of the phytoplasma genomes. Multiple copies of genes seem to be organized into large clusters, referred to as putative mobile units, and might allow adaptation to different conditions through horizontal gene transfer, DNA rearrangements and recombination events between the chromosome and the plasmids (Hogenhout et al., 2008).

Spiroplasma diseases are most often found in insects, ticks and even higher vertebrates. Nevertheless, the best-studied spiroplasmas are the insect-transmitted phytopathogens Spiroplasma citri, responsible for citrus stubborn disease, Spiroplasma kunkelii, causing corn stunt disease, and Spiroplasma phoeniceum affecting aster or periwinkle. These spiroplasmas display a lifestyle similar to that of the phytoplasmas, but appear to have undergone less extensive gene loss (Regassa and Gasparich, 2006).

Concluding remarks

  1. Top of page
  2. Summary
  3. Introduction
  4. Beneficial interactions
  5. Harmful interactions
  6. Concluding remarks
  7. Acknowledgements
  8. References

In summary, much can be learned from Gram-positive plant-associated bacteria, both in plant sickness and in health. The economic importance of most plant diseases caused by Gram-positives has emphasized the dark side of this group of bacteria, but their potential for agricultural applications is equally meaningful. The significance of Gram-positive bacteria in diverse beneficial interactions has long been underestimated, mostly because they could not easily be isolated with standard procedures. With improved isolation and detection protocols, many Gram-positives have now been identified with interesting characteristics that distinguish them from their Gram-negative counterparts. The great versatility of the secondary metabolism of many Gram-positive bacteria makes them very suitable as biocontrol organisms against insects, nematodes, fungi and other bacteria, and their broad catabolic capacities provide a basis for their use as bioremediation agents. The best-described genera are undoubtedly Bacillus and Streptomyces for the Firmicutes and the Actinobacteria, respectively. However, several other genera are being recognized for their highly attractive competences and await further characterization. Finally, with the continued depletion of stratospheric ozone, the amount of UV-B reaching the earth's surface may cause a population shift to favour Gram-positive populations within the plant phyllosphere, because pigmentation and endospore production render them more resistant against UV radiation and elevated temperatures. Hence, the importance of continued research in this field.

Acknowledgements

  1. Top of page
  2. Summary
  3. Introduction
  4. Beneficial interactions
  5. Harmful interactions
  6. Concluding remarks
  7. Acknowledgements
  8. References

The authors apologize to the colleagues whose scientific contributions could not be cited due to space limitations and thank Roelinde Francis for artwork and Martine De Cock for help in preparing the manuscript. I.F. was indebted to the ‘Instituut voor de aanmoediging van innovatie door Wetenschap en Technologie in Vlaanderen’ for a predoctoral fellowship.

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  6. Concluding remarks
  7. Acknowledgements
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