Environment friendly control of plant disease is an emerging need for agriculture in the twenty‐first century. Biological control using antimicrobial producing rhizobacteria to suppress plant diseases and promote plant health offers a powerful alternative to the use of synthetic chemicals. Many studies have been conducted to identify the specific traits by which plant growth‐promoting rhizobacteria (PGPR) promote plant growth. Most of these studies were limited to examining just one or two of these traits. The plant growth‐promoting rhizobacteria produce a wide variety of antimicrobial compounds against pathogens. The addition of antagonistic antimicrobial producing bacterial strains, either individual or as mixture in combination with fungicide, significantly decreased the plant disease stress. A single PGPR strain can produce different kinds of antimicrobial defense compounds to compete pathogens. A biocontrol agent possessing multimechanism systems of defense can antagonize pathogens in a better way. This research chapter highlights the current advancements about plant‐PGPR interactions focusing on the principles and defensive mechanisms of PGPR during disease stress conditions and their potential use for the biocontrol of plant diseases. The integrated use of genetic, molecular, and ecological approaches will form the basis for significant future advances in biocontrol research against plant diseases.
- plant health
- plant growth‐promoting bacteria
- microbial pathogens
- antimicrobial compounds
Pathogenic microorganisms affecting plant health are a major and chronic threat to food production and ecosystem stability worldwide. Agricultural yield and production increased in past few decades due to intensive use of agrochemicals providing more stable and reliable method for crop protection. The increasing use of these fertilizers and pesticides results in several negative effects on the environment, i.e., development of pathogen resistance and adverse impacts on nontarget organisms. In addition, the high cost of these fertilizers and pesticides and increasing demand of consumers for chemical‐free food have led to a search for alternative natural products. There are many plant diseases for which chemical pesticides and stable protection from pathogens are not available. In this scenario, an alternative way of reducing the use of agrochemicals in agriculture, which also provides an effective disease protection and continuous supply of natural food, is biological control .
The ability of microorganisms to respond to stress in their environment is the key to their survival. In general terms, any condition that prevents an organism from growing at its optimal rate may be considered a form of environmental stress. For an organism to survive, it must respond to the environmental conditions imposed upon it, whether it is the absence of a nutrient, extremes in temperature, pH or oxidative state, or the presence of toxic compounds. Bacterial responses to these factors are varied and can include the expression of new proteins, the loss of plasmids, changes in membrane fatty acid content, changes in DNA super coiling and, in some cases, cross‐tolerances to yet unencountered forms of environmental stress .
The lack of homogeneity and varied make up of soil dictates that organisms living in it must be able to adapt and survive. It was the purpose of this study to examine the interplay of nutrient limitation, specifically iron, and the presence of a wide array of antimicrobial compounds on the ability of the plant growth‐promoting rhizobacteria to adapt to its environment and suppress the pathogenic disease. To understand the role of antimicrobial compounds in biocontrol of soil‐borne pathogens, an overview of the plant rhizospheric ecology, PGPR, and biocontrol mechanisms is first required.
1.1. Plant rhizosphere
The “rhizosphere” can be defined as the part of soil around plant roots where bacterial growth is stimulated. It is the habitat where several biologically important processes and plant microbe interactions take place. A diverse range of microorganisms are populated in rhizosphere and the bacteria colonizing this habitat are usually named as rhizobacteria.
1.1.1. Plant growth‐promoting rhizobacteria (PGPR)
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. Plant growth‐promoting bacteria (PGPR) are associated with almost all plant species in a range of environments. Plant growth‐promoting rhizobacteria (PGPR) colonizing the root surfaces and the closely adhering soil interface are the extensively and widely studied group. These PGPR can also enter into the interior parts of roots and establish populations of endophytic bacteria. Majority of these rhizobacteria transcend the barrier of endodermis, penetrating from the cortex of root to the vascular system, and finally reach in the upper parts of plants like stem, leaves, and tubers . The ability of bacteria to selectively adapt these specific ecological niches depends on the extent of endophytic colonization of host plant organs and tissues. Consequently, without harming the plant, eco‐friendly associations between bacteria and host plants become established.
It is generally considered that many endophytic bacteria are the final product of a plant microbe process of colonization occurred in the root zone .
1.1.2. Direct plant growth promotion
PGPR can influence plant growth directly. These ways differ species to species and even from one bacterial strain to other strain. Rhizobia as symbiotic plant colonizers contribute to plant growth stimulation by enhancing nitrogen fixation. Free‐living rhizobacteria usually do not depend on single plant growth‐promoting mechanism. Several PGPR are also able to provide the plant with sufficient iron in iron‐limiting soils or other important minerals, e.g., phosphate and zinc .
1.1.3. Indirect plant growth promotion
Indirect growth promotion occurs when PGPR promote plant growth by improving growth‐restricting conditions. This can happen directly by producing antagonistic substances or indirectly by inducing resistance in host plants to a broad spectrum of pathogens. A bacterium can affect plant growth by one or more of these mechanisms and also use different abilities for growth promotion at various times during the life cycle of the plants. The widely recognized mechanisms of biocontrol mediated by PGPR are competent for an ecological niche or a substrate, production of inhibitory allelochemicals, induction of systemic resistance (ISR), and/or abiotic stresses .
1.1.4. Competitive root colonization
Successful application of PGPR has been hampered by inconsistent performance under field conditions. This is usually due to their poor and unstable rhizosphere competence. Effective root colonization with the ability to survive and proliferate along growing plant roots for a definitive time period in the presence of the other indigenous microflora results in effective rhizosphere competence development. Rhizosphere competence is considered as a prerequisite of effective biological control. Understanding root‐microbe interactions as affected by genetic and environmental factors in spatial temporal contexts could significantly contribute to improve the efficacy of these biocontrol agents under wide range of field conditions . Successful and stable application of PGPR is most directly affected by competition for root niches and bacterial determinants.
Root exudates determine which microorganism colonizes roots in the rhizosphere. It is now known that plant roots also generate electrical signals and zoospores of oomycetic pathogens take advantage of these signals to guide their movements toward the root surface. Both physical and chemical benefits to plants are provided by exudates, e.g., reduce the friction between root tips and the soil by root mucilages and reduction of root desiccation establish the effective contact between the root tips and the soil and contribute to soil structural stability. Root exudates also attract microorganism. Conversely, rhizobacteria can also elicit root exudation in a specific manner, e.g., metabolites produced by
Important bacterial traits identified for effective and stable root colonization are linked to phase variation, a regulatory process for DNA rearrangements controlled by site‐specific recombinase enzyme. In some PGPR, efficient root colonization is subject to their ability to secrete an effective site‐specific recombinase. This importance has been found when a site‐specific recombinase gene from a rhizosphere‐competent
2. Biocontrol of soil pathogens by antimicrobial producing rhizobacteria
A great diversity of rhizospheric microorganisms has been studied, characterized, and analyzed as biocontrol agents against many soil‐borne pathogens over the past decades. Such microorganisms can produce substances that may reduce the damage caused by phytopathogens, e.g., by producing antibiotics, siderophores, and variety of enzymes. These microorganisms can also serve as competitors of pathogens for root colonization sites and nutrients. Biocontrol has not yet become widely popular and applied as alternative source of agrochemicals due to several factors. For example, the efficiency and activity of a biocontrol strain under field condition is usually affected by changing environmental conditions: water contents, pH, temperature, and interactions with other microorganisms. As a result, these biocontrol agents that showed promising plant growth stimulation and disease protection traits in initial laboratory experiments failed to be efficient rhizosphere colonizers under more complex biological field conditions. This highlights the need to address these limitations by extensive study of genetic, biochemical, and physiological factors that contribute to the effective and successful activity of biocontrol agents under wide range of environmental conditions.
Antibiotics play a very important role in pant disease suppression by biocontrol agaents. Molecular and genetic tools could be effective in this regard because mutant defective in antibiotic production are easily obtained and studied by
Antibiosis as a biocontrol mechanism of PGPR has become increasingly popular, better studied and used over the past decades. A large variety of antibiotics have been identified and formulated such as amphisin, 2,4‐diacetylphloroglucinol (DAPG), oomycin A, phenazine, pyrrolnitrin, pyoluteorin, tensin, tropolone, hydrogen cyanide, and cyclic lipopeptides produced by
Regulatory cascades of these efficient antibiotics include
2.2. Hydrolytic enzymes production
A variety of microorganisms also shows hyperparasitic mechanism, attacking plant pathogens by excreting cell wall enzymes called hydrolases.
2.3. Detoxification and degradation of virulence factors
Biological control exhibits antagonism by detoxification of pathogen virulence factors also. For example, few biocontrol microorganisms are capable of detoxifying albicidin toxin synthesized by
It has been discovered recently that few PGPB show pathogen quorum sensing ability by degrading autoinducer signals, thereby blocking expression of various virulence genes. Bacterial plant pathogens use autoinducer‐mediated quorum sensing to switch on gene cascades for their key virulence factors (e.g., cell‐degrading enzymes and phytotoxin production). This approach holds tremendous antagonistic potential for suppression of diseases, even after the onset of infection effectively.
Biocontrol activity of microorgansims by production of allelochemicals has been studied widely with free‐living rhizobacteria. Similar antagonistic mechanisms are used by endophytic bacteria as they can also synthesize antagonistic metabolites against plant pathogens. For example, it has been established that antibiotics munumbicins produced by the endophytic bacteria
Certain endophytic bacteria isolated from field‐grown potato plants can suppress the
2.4. Induction of systemic resistance
An advanced level of resistance at sites within that plant distant to those parts where infection had occurred is called systemic resistance. PGPR‐triggered ISR provides strength and integrity to plant cell walls and boost host physiological and metabolic responses, leading to an increased production of plant defense chemicals against plant pathogens or abiotic stress factors. This recognition mediates the extracellular to intracellular signals. Then, the metabolite by itself or a signal generated by the plant cell turns on a signal transduction cascade. Consequently, distant plant cells, triggering the activation of defense arsenal of the diseased host plant, recognize the translocated signals. The pathways of signal transduction are activated upon microbial challenge, which results in activation of different sets of effector molecules.
Salicylic acid (SA), jasmonate (JA), and ethylene (ET) are the signaling molecules when accumulating trigger the defense responses and, if used exogenously, are even sufficient to induce resistance and suppress disease . These SA signaling molecules activate genes encoding pathogenesis‐related proteins (PRs). These self‐defense proteins have antimicrobial potential. ET is involved in the regulation and expression of the defensive genes encoding
Two defense pathways, induced systemic resistance and systemic acquired resistance (SAR), are found induced in
2.5. Hydrogen cyanide production
Hydrogen cyanide (HCN) is released as a product of secondary metabolism by several microorganisms and affects sensitive organisms by inhibiting the synthesis of ATP mediated by cytochrome oxidase. The percentage of cyanogens found is very low among rhizobacteria . Therefore, depending on the target organisms, HCN‐producing microorganisms are regarded as harmful when they impair plant health and beneficial when they suppress unwanted components of a microbial community. It has been reported that an isolate capable of cyanide production could be a better biocontrol agent because cyanide acts as an inducer of plant resistance .
2.6. Competition for iron: Siderophores production
Siderophores, from the Greek: “iron carriers,” play the role to scavenge iron from environment and to make the mineral, which is always essential, available to microbial cell. Consequently, iron becomes unavailable to microorganisms that are unable to use these siderophores and competition for iron between microorganisms seems probable. Studies of siderophore‐producing microorganisms have received much attention because of the clinical application and potential utilization of these chelators in agriculture.
Fungal strains produced both extracellular and intracellular siderophores, as discovered in spores and mycelia of
Siderophores detection is mostly achieved in iron‐limited media, which means that either a synthetic (minimal) recipe or introduction of a complexing agent will render the iron selectively unavailable. The chrome azurol sulfonate (CAS) assay has become widely used since it is comprehensive, responsive, and more convenient than other microbiological assays, which although sensitive is rigidly specific . Quantitative detection of siderophores can be done by spectrophotometry and by HPLC. The presence of hydroxamate siderophores is usually detected by Csaky's test , and catechol siderophores are usually detected by Arnow's test .
Siderophores differ substantially in structure, so no uniform procedure is available for its isolation. The siderophore can be isolated as individual compound or as its iron chelate. The iron chelates has the benefit of visual color identification but the iron must be removed before any natural product can be characterized by antimicrobial assays. Complete hydrolysis in the presence of iron could damage oxidizable moieties and direct NMR analysis is ruled out by paramagnetism of the ferric ion. By a combination of NMR and mass spectroscopy, structural characterization is done in the best possible way. These methods are sensitive and capable of providing absolute answers to all arising questions. Less than half of the siderophores could be crystallized. However, by X‐ray diffraction technique, the successful configuration of those molecules containing a chiral center‐like siderophores could be easily possible.
Among the siderophore‐producing microbes, bacteria produce both hydroxamate and catecholate siderophores but fungi produce only hydroxamate‐type compounds .
In Gram‐negative genera such as the
The production of siderophores has been linked to the disease suppression ability of PGPR either through a direct effect on plant by control of noxious organisms in soil or via some other routes. The involvement of siderophores in plant growth promotion and disease suppression by
Furthermore, the inhibitory effects of both the purified siderophore and the producing strain were eliminated under high‐iron conditions. Subsequent genetic evidence indicated that the inhibitory properties of certain fluorescent pseudomonads were abolished in siderophore‐negative mutants. Specific siderophore‐producing rhizobacteria (
In response to iron‐deficiency stress, graminaceous plant species differ widely. Understanding the mechanism of stress responses is significant for increasing crop yields on calcareous soils. It also helps in improving the iron content of grains for human consumption. The response of graminaceous plants to iron deficiency occurs by the exudation of phytosiderophores to increase the availability of iron and by improving the uptake capacity of iron (III)‐phytosiderophores. Phytosiderophores are usually hexadentate ligands that coordinate iron (III) with their amino and carboxyl groups. Phytosiderophores chelate sparingly soluble soil iron by forming iron (III)‐phytosiderophore complexes that can be subsequently transported across the root plasma membrane via facilitated transport when released to the rhizosphere. In general, plant species releasing high quantities of phytosiderophores, such as barley, rye, and wheat are more resistant to iron deficiency chlorosis than species releasing smaller quantities, such as maize, sorghum, and rice. However, the quantity of phytosiderophores released is not always constant, for example, chlorosis resistance in different maize cultivars has been reported but this is not related to the total amounts of phytosiderophores released, indicating the contribution of other factors regulating iron efficiency process .
3. Identification of antagonistic antimicrobial producing rhizobacteria
Identification of bacteria is traditionally performed by isolation of the organisms and study of their phenotypic characteristics, including Gram staining, morphology, culture requirements, and biochemical reactions. The discovery of PCR and DNA sequencing, comparison techniques of the gene sequences of bacterial species, proved that the 16S rRNA gene is highly conserved within a species and among species of the same genus, and thus can be used for bacterial identification at species level. For bacterial systematic studies at the family, genus, species, and subspecies levels, the 16S rDNA, which codes for the small subunit of ribosomal RNA, is now the most widely and successfully used informational macromolecule. For natural relationships between distantly related species and variable regions that can be used to separate closely related genera, the 16S rDNA conserved sequences can be used by constructing and comparing phylogenetic trees.
Such a 16S rDNA sequence‐based identification technique will substantially facilitate the ecological study and the control of microorganisms difficult to culture .
Interests in biological control have recently increased due to imminent bans on chemical control, widespread development of fungicide resistance in pathogens, and a general need of sustainable disease control strategies. A wide variety of antagonistic biocontrol agents, such as
Biocontrol of plant pathogens is being so popular because it can decrease the disease incidence, reduce the use of chemical fungicides, has no undesirable effects on nontarget organisms and environment, and is safer for the user and community.
4. Conclusions and scope
The plant growth promoting (IAA production, nitrogen fixation, and P‐solubilization) and biocontrol traits (production of HCN, siderophores, hydrolytic enzymes, and antibiotics) suggest that these traits are more worthy of screening for plant growth promotion and bioantagonistic potential against plant pathogens. The plant growth‐promoting rhizobacteria produce a wide variety of antimicrobial compounds against pathogens. A biocontrol agent possessing multimechanism systems of defense can antagonize root pathogens in a better way. This chapter highlights the need of screening the PGPR capable of producing a wide variety of antimicrobial compounds. Further evaluating/characterizing the biocontrol mechanisms and then testing the efficacy of selected antimicrobial‐producing bacteria by lab, green house, and field trials could make them potent and successful biocontrol agents against many plant pathogens. This research chapter will help to minimize the chances of failure of biocontrol activity under field conditions, which is an emerging current problem of agriculture sector, and these tools will allow the isolation of improved antimicrobial bacterial strains and more efficient bioformulation to control pathogens. Molecular methods developed for the study of microorganisms in their environments are key tools for the study of the influence of the microbial community on biocontrol through variety of antimicrobial compounds produced by rhizobacteria. Further experiments should be initiated to study the optimum formulation and the interaction of these bacteria with the constituent of established PGPR preparations, with a view to incorporating them for field use. Research along these lines will increase the impact of PGPR on the biocontrol of plant diseases in the commercial world.
The author acknowledges Dr. Fauzia Yusuf Hafeez, COMSATS University Islamabad, Pakistan, for helping in the collection of the literature (books and journals) about antimicrobial rhizobacteria and antagonistic biocompounds and her expertise advise during the preparation of this chapter.
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