THE RHIZOSPHERE MICROBIOME AND ITS BENEFICIAL EFFECTS ON PLANTS – CURRENT KNOWLEDGE AND PERSPECTIVES

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VOLUME 58 , ISSUE 1 (June 2019) > List of articles

THE RHIZOSPHERE MICROBIOME AND ITS BENEFICIAL EFFECTS ON PLANTS – CURRENT KNOWLEDGE AND PERSPECTIVES

Małgorzata Woźniak * / Anna Gałązka

Keywords : microbiome, promoting plant growth, rhizosphere

Citation Information : Postępy Mikrobiologii - Advancements of Microbiology. Volume 58, Issue 1, Pages 59-69, DOI: https://doi.org/10.21307/PM-2019.58.1.059

License : (CC-BY-NC-ND 4.0)

Published Online: 10-June-2019

ARTICLE

ABSTRACT

The root system of a plant works like a factory that produces a huge amount of chemicals to communicate effectively with the microorganisms around it. At the same time, micro-organisms can use these compounds as an energy source. The variety of microorganisms associated with plant roots is enormous, amounting to tens of thousands of species. This complex microbial community, also called the second plant genome, is essential for plant health and productivity. Over the last few years, there has been significant progress in research into the structure and dynamics of the microbial sphere of the rhizosphere. It has been proven that plants shape the composition of microorganisms by synthesizing root secretions. On the other hand, microorganisms play a key role in the functioning of plants through their positive impact on their growth and development. In general, rhizosphere microorganisms promote plant growth directly by providing plants with minerals such as nitrogen and phosphorus and by synthesizing growth regulators, as well as indirectly, by inhibiting the development of various plant pathogens.

1. Introduction. 2. Functions of rhizosphere microorganisms. 3. Microorganisms increasing the availability of minerals. 4. Microorganisms synthesizing plant growth regulators. 5. Biological plant protection. 6. Summary

Translated

Streszczenie: System korzeniowy roślin działa jak fabryka, która produkuje ogromną ilość związków chemicznych, aby skutecznie komunikować się z otaczającymi go/ją mikroorganizmami. Jednocześnie mikroorganizmy mogą wykorzystywać te związki jako źródło energii. Różnorodność drobnoustrojów związanych z korzeniami roślin jest ogromna, rzędu dziesiątek tysięcy gatunków. Tę złożoną społeczność drobnoustrojów, nazywany również drugim genomem rośliny, który ma zasadnicze znaczenie dla zdrowia i produktywności roślin. W ciągu ostatnich kilku lat nastąpił znaczny postęp w zakresie badań dotyczących struktury mikrobiomów ryzosfery i ich dynamiki. Udowodniono, że rośliny kształtują skład mikroorganizmów poprzez syntezę wydzielin korzeniowych. Natomiast drobnoustroje odgrywają kluczową rolę w funkcjonowaniu roślin poprzez pozytywne oddziaływanie na ich wzrost i rozwój. Ogólnie, mikroorganizmy ryzosferowe promują wzrost roślin bezpośrednio poprzez udostępnianie roślinom składników mineralnych m.in. azotu i fosforu oraz syntetyzowanie regulatorów wzrostu. Natomiast pośrednio poprzez hamowanie rozwoju różnych patogenów roślin.

1. Wstęp. 2. Funkcje mikroorganizmów ryzosferowych. 3. Mikroorganizmy zwiększające dostępność składników mineralnych. 4. Mikroorganizmy syntetyzujące regulatory wzrostu roślin. 5. Biologiczna ochrona roślin. 6. Podsumowanie

Graphical ABSTRACT

1. Introduction

Plants are multicellular organisms which under the influence of metabolic changes continuously undergo the process of growth and development. Being autotrophic organisms, plants play an important role in sustaining all other life forms. In a developing plant, we can define at least three main parts: (1) the root, growing usually under the soil surface, which plays an important role in the uptake of water and nutrients, (2) the stem, whose basic function is the transport of water and nutrients, and also supporting leaves and other organs, and (3) the shoot, which produces leaves, flowers and fruit and enables effective nutrition of plants through photosynthesis and is also responsible for the reproduction process [48, 63]. Plants are colonised by an extremely high number of (micro)organisms, which can reach cell density much greater than the number of cells in the plant itself. In addition, the number of the genes of the microorganisms inhabiting the rhizosphere significantly exceeds the number of plant genes. Plants act as a link between communities of microorganisms, insects and other invertebrate and vertebrate animals occurring both above and below the soil surface [10, 54, 64]. In the natural environment, abiotic and biotic factors have an indirect or direct impact on plants. For example, an attack by various organisms, e.g. insects, leads to a reduction of the leaf surface and therefore to the reduction of the photosynthetic potential. Modification of root secretions affecting soil microorganisms may be a consequence of this process. In addition, the use of plant protection agents and pesticides can change the concentration and type of secondary metabolites synthesised in the shoots and roots of plants and negatively affect the interactions of plants with non-pathogenic soil microorganisms [64]. Extensive communication between plants and microorganisms occurs at different stages of plant development in which the signalling molecules of both partners play an important role. Signalling molecules produced by bacteria and fungi are involved in the initiation of plant colonization. In contrast, plants recognise compounds derived from microorganisms and adapt their response depending on the type of microorganism and metabolite encountered. This chemical dialogue defines the final result of the relation between the plant and microorganisms [4]. Virtually all plant tissues can be populated by microorganisms. Research focuses mainly on the rhizosphere, phyllosphere and endosphere. The rhizosphere is an area enriched with nutrients derived from plant mucilage and root secretions and is characterised by the presence of numerous and metabolically active microorganisms [38, 90]. On the other hand, the phyllosphere is relatively poor in nutrients and subject to extreme temperatures, radiation and humidity [90, 95]. The microorganisms present in the rhizosphere and phyllosphere are epiphytes (occurring in the vicinity or on plant tissues), while microorganisms located inside plant tissues, whether in the leaves, roots or stems, are called endophytes [71, 90].

Microorganisms play a key role in the correct conduct of most processes occurring on Earth. Plant microbiome affects the viability of plants and is therefore one of the main indicators of plant productivity [9, 90]. Comprehensive studies targeting plant microbiome may contribute to reducing the incidence of plant diseases, increasing agricultural production and reducing the amount of chemical preparations in use [6, 90, 98]. The vast majority of metabolically active microorganisms are unable to grow on agar substrates. The classic techniques based on culturing microorganisms allow for studying isolated microorganisms in detail, and molecular techniques such as metagenomics/metatranscryptomics enable the identification of microbial populations, also those referred to as non-cultivable [26, 49, 51, 98]. In studies on prokaryotic microorganisms, amplification of the 16S rRNA gene is commonly used. Sequencing variable regions of this gene enables taxonomic identification at the generic or even at the species level. To identify eukaryotic microbes, such as fungi, the 18S rRNA gene as well as the ITS region are used. Metagenomic sequencing technology has become a widely used molecular biology tool which allows for identifying from thousands to millions of sequences in one environmental sample, revealing the wealth of even rare species of microorganisms [49, 56, 60, 90, 98].

Soil is a highly complex system in terms of the number and diversity of interactions between its physical, chemical and biological components [8, 12]. Soil functions depend to a large extent on the microorganisms which constitute a component for basic metabolic processes occurring in the soil environment [57]. Numerous reports in literature indicate that many soil microorganisms interact with plant roots and soil components at the root-soil boundary [8]. Root exudates and decomposing plant residues are the main source of carbon for heterotrophic microorganisms and the determinant of the rhizosphere function [8, 60]. In turn, active rhizosphere microorganisms and their metabolites influence the structure of the root system by modifying the quality and quantity of root exudates (bioactive substances of plants) [8, 56, 90]. In the rhizosphere, we can distinguish three interacting components: rhizosphere, rhizoplane and root. The rhizosphere is the soil area which is found near the root surface and which is affected by root exudates of plants. The rhizoplane is the outer surface of the root, along with the tightly adhering soil particles. The root, in turn, is the part of the plant which supports it in the substrate and is responsible for the supply of water and mineral salts [8, 56, 60, 90].

2. Functions of rhizosphere microorganisms

The microorganisms present in the rhizosphere play an important role in the shaping of the plant host. Some of them have a beneficial effect on the growth and development of plants, e.g. bacteria which bind atmospheric nitrogen, mycorrhizal fungi or PGPR – Plant Growth-Promoting Rhizobacteria. Microorganisms – these establish symbiosis with plants, based on mutual benefits (mutualism). The next group is microorganisms which are harmful to plants: pathogenic fungi, oomycotes, bacteria and nematodes. Negative interactions between the bacterial flora and plants are the cause of many diseases in economically important crops around the world. The most important root pathogens include Agrobacterium tumefaciens, Ralstonia solanacearum, Dickeya dadanthi, Dickeya solani, Pectobacterium carotovorum and Pectobacterium atrosepticum [36, 54, 71]. Recently, there has appeared a lot of information in the literature, describing the third group of microorganisms found in the rhizosphere, namely human pathogens [30, 54, 91].

The rhizosphere is inhabited by various microorganisms, and the bacteria colonising this habitat are called rhizobacteria [42, 43]. In the late 1970s Kloepper and Schroth introduced the term PGPR to describe bacteria which colonise plant roots and possess the ability to stimulate plant growth [44]. The rhizosphere PGPR bacteria should be characterised by (1) the ability to colonise the root zone of plants, (2) the ability to survive and reproduce in the presence of competitive microorganisms, at least for the time needed to reveal their beneficial activity contributing to the promotion and protection of plants, (3) activity promoting plant growth [8]. Generally, interactions with microorganisms which are beneficial for plants have been divided into three categories. The first category includes microorganisms which are responsible for plant nutrition, i.e. microorganisms that increase the availability of minerals. The second group of microorganisms are those responsible for direct influence on the promotion of plant growth through the production of, for example, phytohormones. In turn, the third group of microorganisms stimulates plant growth indirectly by inhibiting the activity of microorganisms exhibiting pathogenic activity. Such impact is referred to as biological plant protection [60, 97]. The majority of PGPR microorganisms stimulate plant growth based on the combination of two or more mechanisms promoting plant growth [14, 56]. In addition, some PGPRs may influence the growth and development of plants through the synergistic effect of co-inoculation. For example, Tilak et al. [88] tested co-inoculation with the bacteria Pseudomonas putida, Pseudomonas fluorescens, Bacillus cereus with bacterial strains of the genus Rhizobium on the pigeon pea (Cajanus cajan L). Double vaccination resulted in a significant increase of plant growth, nitrogenase activity and the number of nodules formed compared to control plants.

We are currently observing a growing interest in the bacteria capable of stimulating growth and nutrition of plants, which is reflected in the rapidly growing number of scientific publications on the subject. The research is covering an increasingly broad range of plant species, new techniques of microorganism identification and analysis of their mechanisms of action. Various strains of bacteria and fungi have been successfully used to inoculate plants. They include bacteria from the genus Azospirillum [13], Bacillus [58], Pseudomonas [67], Rhizobium [28], Serratia [20], Stenotrophomonas [81], and Streptomyces [18]. The fungi endowed with a natural ability to stimulate various plant characteristics linked to their growth (PGPF – Plant Growth-Promoting Fungi) include species of the following genera: Aspergillus, Fusarium, Trichoderma, Penicillium, Piriformospora, Phoma and Rhizoctonia [32, 33, 80].

3. Microorganisms increasing the availability of minerals

Most species of rhizobacteria are organotrophs which obtain energy from assimilation of organic compounds. Limited resources of organic compounds and carbon in most soils are the most common factor inhibiting the growth of soil bacteria. Rhizosphere microorganisms play a fundamental role in the release of nutritional cations from soil minerals, which they use not only for their own nutrition but also for plant nutrition [1, 54].

One of the best-known examples of plant growth promotion is BNF – Biological Nitrogen Fixation. Of all the elements known in the world, plants react most strongly to nitrogen deficit in the soil. It determines the proper development of underground and aboveground parts of plants. The nitrogen pool in the atmosphere is not available to plants. In addition, the intensive use of fertilisers in agricultural crops has led to an increasing accumulation of harmful nitrates in soil and water resources, as well as nitrogen oxides in the atmosphere. Due to the increased efficiency of the application of nitrogen fertilisers, priority should be given to the process of biological nitrogen binding. Symbiotic binding of N2 is a well-known process in which bacteria possessing an enzymatic complex – nitrogenase, reduce atmospheric N2 to ammonia in root nodules of bean plants [1, 8, 50, 52, 56, 90]. The bacteria responsible for this process belong, among others, to the genera: Rhizobium, Sinorhizobium, Bradyrhizobium, Mesorhizobium and Azorhizobium, collectively referred to as rhizobia. These bacteria interact with the roots of the Fabaceae plants leading to the establishment of effective symbiosis. Another group of microorganisms are bacteria which bind nitrogen in the asymbiotic (free) state, e.g. Azospirillum sp., Azotobacter sp., Azomonas sp. or Bacillus sp. The Actinobacteria of the genus Frankia also have the ability to bind atmospheric nitrogen by forming a specific symbiosis called actinorhizal symbiosis on tree roots, e.g. alder (Alnus Mill.) [8, 50]. Another group of microorganisms which exert a positive effect on soil fertility by establishing symbiosis and binding atmospheric nitrogen are cyanobacteria – a group of photosynthetic prokaryotes (Cyanobacteria, Blue-Green Algae – BGA). In addition to making nitrogen available to plants, they also affect the aggregation of soil particles, and thus moisture retention and prevention of erosion [77].

Another type of symbiosis occurring in the rhizosphere is mycorrhiza – mutual symbiosis of fungi with the roots of most plants. The most common type of this symbiosis is arbuscular mycorrhiza (AM). AM fungi were initially included in the division Glomales and Zygomycota [70], but currently they are assigned to the division Glomeromycota [76]. The presence of arbuscular mycorrhiza positively affects the condition of plants, among others by increasing the absorbent surface of roots, which allows plants to have better access to water and minerals, especially those whose ionic forms show poor mobility or those present in low concentrations in the soil. The results of numerous studies indicate that plants colonised by the fungi of arbuscular mycorrhiza show greater resistance to environmental stress factors and biotic stress [8].

Phosphorus (P) is the second important factor limiting plant growth [40, 52]. It plays an important role in practically all metabolic processes of plants, including photosynthesis, energy transfer, signal transduction, biosynthesis of macromolecules and respiration [3, 41, 78]. On average, the phosphorus content in the soil is about 0.05% (weight percentage), however only 0.1% of this phosphorus is available to plants [3, 99]. Soil phosphorus deficiency is often supplemented by the use of phosphate fertilisers. However, most of the phosphorus applied in the form of fertilisers is not available to plants, and their application in excessive amounts can lead to environmental problems, such as groundwater contamination, eutrophication of water reservoirs and loss of soil fertility [37]. The effectiveness of the phosphate fertilisers applied in a chemical form rarely exceeds 30% due to their fixation, either in the form of iron/aluminium phosphate in acidic soils [61] or in the form of calcium phosphate in neutral to alkaline soils [47]. In the natural environment, numerous microorganisms present in the soil and rhizosphere effectively release phosphorus from its insoluble forms thanks to solubilisation and mineralization [3, 11, 52, 78]. This group of microorganisms is referred to as phosphate solubilising microorganisms (PSM) (Figure 1). The metabolic products of these microorganisms are, among others, organic acids such as gluconic, citric, lactic, propionic and succinic ones. They are seen as the main factor responsible for availability of phosphorus. A large number of microorganisms, including bacteria, fungi, actinomycetes and cyanobacteria, exhibit the ability to dissolve and mineralise phosphorus compounds.

Fig. 1.

Biodiversity of PSM [according to 3, 78].

10.21307_PM-2019.58.1.059-f001.jpg

The rhizosphere microorganisms may also facilitate the uptake of trace elements, such as iron (Fe) [2, 25, 52]. Iron is an essential nutrient for almost all life forms. Iron is abundantly present in the soil, but in a form, which is inaccessible to microorganisms and plants, namely Fe3+. Many microorganisms have developed specific systems and carriers of iron ions – siderophores. Siderophores are organic compounds of low molecular weight which enable obtaining iron from sparingly soluble substrates and from environments with low iron concentrations. In the case of both Gram-negative and Gram-positive bacteria, iron (Fe3+) is captured by siderophores and in such complex, in the bacterial membrane, there occurs a reduction to Fe2+ ions, which are then released into the cell through active transport mechanism [1, 2]. In recent years, siderophores have been given more and more attention due to their potential role and application in various areas of environmental research. Microbiological siderophores play an important role in bioremediation, biological control, weathering of soil minerals and promotion of plant growth. The research of Qi and Zhao [100] confirms that the siderophores produced by Trichoderma asperellum stimulate the growth and resistance of cucumber (Cucumis sativus) under salt stress conditions. Siderophores are extremely effective in solubilising and increasing the mobility of a wide range of metals which may pose a threat to the environment, e.g. Al, Cd, Cu, Ga, In, Pb and Zn, as well as radioactive elements, including U (uranium) and Np (neptune) [68, 74]. This process depends mainly on the functionality of the ligand, which means that the siderophores can have a strong affinity to a particular metal other than iron [59]. In recent years, interest in researching the potential of siderophores in bioremediation has also increased. Hong et al. [31] report on siderophores produced by Fusarium solani, which contributed to in vitro solubilisation of Cu and Zn. In addition, it has been demonstrated that the siderophores produced by Agrobacterium radiobacter contribute to reducing the content of As in soil by approximately 54% [96]. Microbial siderophores can play an important role in the remediation of petroleum hydrocarbons from marine environments [17]. Petrobactin is the first structurally characterised siderophore produced by a marine bacterium Marinobacter hydrocarbonoclasticus, which degrades petroleum [7]. Hickford and colleagues [29] studied another siderophore named petrobactin sulfonate (isolated from the same marine bacteria), which also breaks down petroleum. The presence of siderophores close to the roots of plants can protect them from many pathogens by binding all available iron forms to chelates and blocking its availability to pathogenic organisms. Some of the siderophores (pyoverdines) produced by fluorescent Pseudomonas bacteria can be an extremely effective tool for inhibiting the growth of phytopathogens, because they exhibit a high affinity to iron ions (III). For example, pyoverdine is involved in the biological control of potato wilt disease caused by Fusarium oxysporum, as well as in limiting the growth of phytopathogens in peanuts and maize [2]. In addition, pyroveridine is used as a probiotic in fish farming because it inhibits the growth of several fish pathogens: Vibrio anguillarum, Vibrio ordalii, Aeromonas salmonicida, Lactococcus garvieae, Streptococcus iniae, Flavobacterium psychrophilum [21]. It should be noted that siderophores have also found application in the ecology and taxonomy of microorganisms. Siderotyping is defined as a method of characterization and identification of microorganisms according to the types of siderophores which they produce [2]. Pyoverdine is a group of siderophores typical of bacterial strains belonging to the genus Pseudomonas. At present, at least 50 pyoverdine molecules with different peptide chain sequences are known. Variability within the peptide is used to determine the relationship between the bacteria of the genus Pseudomonas [55]. In addition, the siderophores can be used as chemotaxonomic markers to identify other types of bacteria, such as Burkholderia sp. and Mycobacterium sp. [2]. In summary, siderotyping can become a powerful tool in environmental research, facilitating efficient and rapid identification of microorganisms [55].

4. Microorganisms synthesizing plant growth regulators

The rhizosphere is a relatively nutrient-rich environment containing amino acids, sugars, fatty acids and other organic compounds which attract microorganisms [95]. In turn, microbes synthesise biologically active compounds, including phytohormones: auxins, cytokinins, gibberellins, ABA (abscisic acid), vitamins and volatile compounds. These microbiological metabolites play an important role in the growth, nutrition and development of plants [23, 52, 63]. The term “plant hormones” or “phytohormones” was finally introduced by Thimann in 1948. With further research, more and more plant hormones have been identified that were described as trace organic substances synthesised in some parts of the plant. Vegetable hormones play a significant role in agriculture because they participate in the process of fruit ripening, leaf abscission and seed germination [23, 79, 87]. Plant hormones are found not only in higher plants, but they are also synthesised by bacteria and fungi. Initially, plant hormones for agricultural purposes were obtained mainly by extraction from plant tissues. Due to the increased demand, chemical synthesis was gradually introduced. Nevertheless, due to the relatively complex structure of plant hormones, chemical synthesis poses a number of problems, such as high costs, complex production process, low purity, etc. In comparison with the previous two methods, microbiological production is an ecological and balanced process of plant hormone synthesis. In addition, final products are characterised by higher biological activity and purity. Thanks to numerous innovative research tools, microbiological production of plant hormones is more efficient and economical [79]. In general, auxins affect the division and differentiation of cells, stimulate the germination of seeds and tubers, increase the rate of xylem formation, control the processes of vegetative growth, initiate root formation, participate in photosynthesis reactions, synthesis of pigments and biosynthesis of various metabolites [1]. It is reported that 80% of microorganisms isolated from the rhizosphere of different crops have the ability to synthesise and release auxins as secondary metabolites [1, 39, 56]. For example, Sorty et al. [84] isolated from the halotolerant weeds (Psoralea corylifolia L.) various groups of bacteria which produce IAA (indolyl-3-acetic acid; indole-3-acetic acid; auxin) belonging to the genus Acinetobacter, Bacillus, Enterobacter, Pantoea, Pseudomonas, Rhizobium and Sinorhizobium. Bacteria of the genus Mycobacterium producing IAA have been found in the rhizosphere of the tropical orchid (Dendrobium moschatum Buch.-Ham.) [89], and Azotobacter, Azospirillum, Cellulomonas, Mycoplan and Rahnell have been identified in the rhizosphere of wheat (Triticum L.) [23]. In addition to direct impact on the growth and development of plants, the auxins synthesised by microorganisms indirectly affect plants by increasing the activity of atmospheric nitrogen binding and solubilisation of phosphorus, an example of which is the bacterium Sinorhizobium meliloti 1021, strain RD64 [34]. Although not as intensively studied as auxins, cytokinins and gibberellins also stimulate plant growth [23, 56]. Ethylene is another important plant hormone. Ethylene influences the growth and development of plants by regulating the size and division of cells, and in terms of development by controlling the process of maturation and aging of plants [75]. In addition, ethylene was defined as a stress hormone [1]. Under stressful conditions, such as high salinity, drought, heavy metals, etc., the endogenous level of ethylene is significantly increased, which negatively affects the entire plant and may lead to a reduction in crop yield [1, 11]. Some plant growth promoting rhizobacteria possess the enzyme 1-aminocyclopropane-1-carboxylase (ACC-1-aminocyclopropane-1-carboxylate deaminase deaminase), which lowers the level of ethylene and thus facilitates the growth and development of plants under stress [1, 27]. Currently, the bacteria which synthesise ACC deaminase include: Acinetobacter sp., Achromobacter sp., Agrobacterium sp., Alcaligenes sp., Azospirillum sp., Bacillus sp., Burkholderia sp., Enterobacter sp., Pseudomonas sp., Ralstonia sp., Serratia sp., Rhizobium sp. etc. [1].

Some bacteria and rhizosphere fungi are able to produce vitamins, especially B vitamins, which have a positive effect on plant growth. The water-soluble vitamins act synergistically with other biologically active substances, stimulating the development of not only plants but also microorganisms [35, 53]. The rhizosphere bacterium P. fluorescens 267 synthesises, among others, biotin, thiamine, cobalamin, pantothenic acid and niacin [19]. Marek-Kozaczuk and Skorupska [53] have demonstrated that the strains of P. fluorescens 267.1 with a mutation in the gene of thiamine and niacin synthesis have lost their ability to promote the growth of clover roots (Trifolium pratense L. cv. Ulka). The vitamins of Group B produced by the P. fluorescens strain 267 stimulate the activity of nitrogen binding in the bacterium Rhizobium leguminosarum bv. trifolii, , being symbiotic with clover, which increases the amount of fresh and dry plant mass and the number and weight of root nodules [19].

According to recent studies, volatile organic compounds (VOCs) produced by plant growth promoting rhizobacteria have the potential to control plant pathogens, stimulate plant growth and induce systemic disease resistance [69, 85]. PGPR or products synthesised by PGPR usually require physical contact with parts of plants to stimulate plant growth [86]. However, many types of bacteria can regulate plant growth from a distance without direct contact. Thus, these bacteria secrete invisible volatile compounds which promote or inhibit plant growth. According to Lemfack et al. [46] there are approximately 350 species of bacteria and fungi producing more than 846 different VOCs. Microbiological VOCs are signal molecules characterised by:

  • low molecular weight (< 300 g/mol),

  • low boiling point,

  • low polarity,

  • lipophilic nature,

  • high vapor pressure (0.01 kPa at 20°C),

Volatile organic compounds synthesised by some microorganisms belong to, among others, alkanes, alkenes, alcohols, esters, ketones, terpenoids and sulphur compounds [24, 45].

Ryu et al. [73] when studying the strains of Bacillus subtilis GB03 and B. amyloliquefaciens IN937a, observed that these bacteria produce volatile organic compounds which support the growth of plants: 2,3-butanediol and acetoin. In addition, literature reported that 2-pentylfuran synthesised by Bacillus megaterium XTBG34 stimulates the growth of Arabidopsis thaliana (101), and P. fluorescens SS1 produces 13-tetradecadiene-1-ol and 2-butanone and 2-methyl-n-1-tridecene, which promote the growth of tobacco (Nicotiana tabacum) [65]. The research carried out by Orozco-Mosqueda et al. showed that alfalfa seedlings (Medicago truncatula) under the influence of volatile substances produced by Arthrobacter agilis UMCV2 for 5 days increased the fresh mass of aboveground and root parts and chlorophyll concentration by 40%, 35% and 35%, respectively [62].

In addition to plant growth-promoting activity, volatile organic compounds modulate the plant’s response to stress inducing factors. It has been demonstrated that 2,3-butanediol significantly induces the resistance of the Arabidopsis to the pathogen Erwinia carotovora subsp. carotovora [72], while 3-pentanol and 2-butanone are used as anti-breeding factors for Pseudomonas syringae pv. lachrymans, a pathogen of cucumber seedlings [83].

Recent research confirms that VOCs secreted by microorganisms can be used as molecules which significantly stimulate plant growth. However, there is still a need for additional experiments to accurately characterise the VOC structure and mechanism of action on a larger number of plant species under field conditions.

5. Biological plant protection

Baker and Cook in 1974 formulated the basis for biological plant protection, defining this term as the use of live microorganisms to reduce the occurrence of pathogenic organisms [5]. The rhizosphere provides a defence line for plants against the attack by pathogens found in soil. Various elements of the rhizosphere microbiome may antagonise pathogens present in soil both before and during the primary infection, as well as during secondary dissemination in the root tissue. The main mechanisms by means of which rhizosphere microorganisms protect plants from pathogens are divided into direct and indirect ones [8, 54, 60].

Direct biological control mechanisms include, among others:

  • competing for an ecological niche, and thus limiting the population of pathogenic organisms,

  • limitation of the nutrients required for the growth of pathogens, such as iron,

  • production of signal components which interfere with the reproduction of pathogens and reduce their growth, e.g. toxins, antibiotics, lytic enzymes, biosurfactants.

Indirect biocontrol mechanisms include:

  • triggering induced systemic resistance (ISR) and systemic acquired resistance (SAR),

  • stimulation of additional organisms capable of inhibiting pests or pathogens [8, 11, 15, 54, 56, 60, 66].

Colonization of roots results not only in the high number of PGPR populations in the root system, but also acts as a delivery system for antagonistic metabolites involved in the direct inhibition of plant pathogens [60]. Among the compounds synthesised by PGPR there are, among others: ammonia, butyrolactone, 2,4-diacetylochloroglucine (DAPG), HCN (hydrogen cyanide), phenazine-1-carboxylic acid, viscominamide, kanosamine, oligomycin A, oomycin A, xanthobaccin and pyoverdine and many others [11, 15, 16, 82].

The strains of the bacterium B. subtilis synthesise many varieties of potent antifungal metabolites, e.g. Zwittermycin-A, kanosamine and lipopeptides (surfactins, iturins) [60]. Bacteria such as Burkholderia cepacia and Ralstonia solanacearum hydrolyse fusarium acid, synthesised by fungi of the genus Fusarium being a common plant pathogen [15]. Another protection strategy for PGPR is the production of lytic enzymes. In 2000 Dunne et at. demonstrated the overproduction of extracellular protease in the mutant strains of Stenotrophomonas maltophilia W81, which caused improvement in the biocontrol of Pythium ultimum (root pathogen of many crops) [22]. In the present study, transposon mutagenesis Tn 5-764cd in the presence of casein caused isolation of two mutants (W81M3 and W81M4), producing about three times more extracellular protease than the wild type W81 strain. In addition, the mutant W81M4 also exhibited increased chitinolytic activity compared to W81, which is also useful for the biological control of chitin-sensitive pathogens and plant parasites.

In the rhizosphere, microorganisms compete with each other for nutrients, sources of carbon and energy [54, 60]. The strategies used by rhizobacteria include, among others, the ability to grow rapidly after encountering substrates and the capability of extracellular conversion of glucose to gluconic acid and 2-ketogluconic acid. Some bacteria, including several species of Pseudomonas, effectively capture glucose from the environment and then convert it to gluconic acid and 2-ketogluconic acid. Therefore, they ensure an advantage over microorganisms which do not have the ability to use these compounds [60].

Microorganisms that inhabit the rhizosphere can also exert an influence on herbivorous insects. An example is furnished by the research carried out by van de Mortel et al. using P. fluorescens SS101, whose presence inhibited the development of Spodoptera exigua, which is an insect feeding on tomato (Solanum lycopersicum) [92].

The rhizosphere microorganisms activate systemic acquired immunity (SAR) in their relationships with plants and participate in triggering induced systemic immunity (ISR). Both ISR and SAR induce a state of increased resistance of the plant, which is accompanied by the synthesis of signal compounds such as jasmonic acid, ethylene and salicylic acid [60, 66, 93]. The term “induced systemic immunity” defines resistance induced by biotic pathogens, while the term “acquired systemic resistance” refers to the interaction of plants with pathogens [66]. Early recognition of a threat by the plant immediately initiates a cascade of molecular signals and transcription of many genes, which ultimately leads to the production of defence molecules by the host plant [66, 93]. These defensive molecules include phytoalexins, pathogenesis-related proteins (PR), such as chitinases, β-1,3-glucanases, inhibitors of proteinase and lignin, etc. [60, 93]. Verhagen and others have demonstrated that tomatoes (Solanum lycopersicum) inoculated with P. fluorescens strain WCS417r (meaning that they are ISR-positive), exhibits a faster and stronger defence induction against the Pseudomonas syringae, a leaf pathogen [94].

6. Summary

Numerous literature data confirm that microorganisms colonising the root zone of plants perform a variety of functions, primarily affecting the promotion of plant growth and development. The roots of plants release compounds being a source of energy for microorganisms. The high concentration of root exudates in the rhizosphere attracts metabolically active microorganisms, the number of which is much higher than in other parts of the soil. The species of the plant, stage of development, soil type and climatic conditions are the main factors determining the composition of microbiological communities of the rhizosphere. Concerns over the excessive use of agricultural chemistry cause the increasing popularity of organic farming promoting biopreparations based on rhizosphere microorganisms which stimulate plant growth and development. Large-scale application of PGPR can reduce the global use of agrochemicals and pesticides. What is more, it is a technology easily available to farmers in both developed and developing countries. The rhizosphere microorganisms, apart from the activity in promoting plant growth, also present a bioremediation potential in relation to heavy metals and pesticides, as well as participate in the control of a number of different phytopathogens. Despite numerous studies on the interaction of plants and rhizosphere microorganisms, there still exists a need for a more detailed understanding of the basic principles of the rhizosphere ecology, including the function and diversity of microorganisms. Familiarization with the dynamics and composition of the communities of microorganisms inhabiting the rhizosphere, as well as the communication with the plant will contribute to the effective use of microbial preparations based on PGPR. Further research on the mechanism of phytostimulation by PGPR would allow for developing bacterial, fungal and bacterial-fungal consortia commercially used in agroecological conditions.

Table I presents examples of rhizosphere organisms which can potentially be used in microbiological preparations which promote plant growth.

Table I

Selected types of bacteria and their properties to promote the growth and development of plants

10.21307_PM-2019.58.1.059-tbl1.jpg

Acknowledgements

The research was financed from Research Grant 1.21 implemented as part of the statutory activities of IUNG-PIB.

The article was translated by EURO-ALPHABET from Polish into English under agreement 659 / P-DUN / 2018 and funded by the Ministry of Science and Higher Education.

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FIGURES & TABLES

Fig. 1.

Biodiversity of PSM [according to 3, 78].

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