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AGRICULTURAL BIOLOGY, ISSN 2412-0324 (ВДЛ ed. Online)
2015, V. 50, № 5, pp. 648-654
(SEL’SKOKHOZYAISTVENNAYA BIOLOGIYA) ISSN 0131-6397 (Russian ed.
v_____________________________________' ISSN 2313-4836 (Russian ed. Online)
UDC 631.8:632.9:579.64 doi: 10.15389/agrobiology.2015.5.648rus
doi: 10.15389/agrobiology.2015.5.648eng
BIODIVERSITY OF ENDOPHYTIC BACTERIA AS A PROMISING BIOTECHNOLOGICAL RESOURCE
V.K. CHEBOTAR’, A.V. SHCHERBAKOV, E.N. SHCHERBAKOVA,
S.N. MASLENNIKOVA, A.N. ZAPLATKIN, N.V. MAL’FANOVA
All-Russian Research Institute for Agricultural Microbiology, Federal Agency of Scientific Organizations, 3, sh.
Podbel’skogo, St. Petersburg, 196608 Russia, e-mail vladchebotar@rambler.ru
Acknowledgements:
Supported by Russian Science Foundation (project No. 14-16-00146)
Received April 24, 2015
Abstract
Endophytic called bacteria are those colonizing the internal tissues of plants without causing disease and not rendering negative influence on its development. There are great prospects for search, selection and study of new species of endophytic bacteria, improving the development of plants, with the aim of creating new microbial preparations for adaptive crop production. Since bacterial endophytes colonize the same ecological niches in the plant as phytopathogenic microorganisms, they are a promising agent for biocontrol of phytopathogens. Classical studies of biodiversity of endophytic bacteria based on a characterization of isolates obtained from internal plant tissues after surface sterilization. Endophytic bacteria are able to improve phosphorus nutrition of plants, to produce IAA and siderophores. It is shown that endophytic bacteria are capable of producing vitamins, have a number of additional properties necessary for the improvement of plant development, such as: regulation of osmotic pressure, regulation of stomata, modification of root development of plants, regulation of nitrogen nutrition of plants. Endophytic bacteria are able to reduce or prevent the negative effects of pathogenic microorganisms on plants. Inoculation of plants by endophytic bacteria is able to significantly reduce the harm caused to plants by pathogenic fungi, bacteria, viruses, insects and nematodes. Unique strains of endophytic bacteria can be used directly for inoculation of seeds or seedlings, reducing, thus, the influence of biotic and abiotic factors on the plant, due to the active colonization of internal tissues of plants and subsequent positive biochemical and physiological effect on the plant. While in endosphere, endophytes have a significant advantage over organisms that live in the rhizosphere and phyllosphere due to the stable pH, humidity, flow of nutrients and lack of competition from a large number of microorganisms. For the inoculation of plants with endophytic bacteria do not require large amounts of inoculum, taking into account high specificity of such plant-microbe symbiosis and competitiveness of endophytic bacteria. This technique can be very attractive for biotechnological productions, seeking the replacement of traditional chemical pesticides.
Keywords: endophytic bacteria, biodiversity, plant-microbial interaction, plant growth promotion biocontrol, secondary metabolites, the genome of bacteria, microbial preparations.
Associations of plants with beneficial microorganisms attract the attention of scientists not only as an object for the study of the fundamental bases of interaction of different organisms, but also in terms of their possible use in the practice of environmentally oriented crop production. Besides rhizosphere microorganisms [1-3], the so called endophytic bacteria are known that colonize the plant tissues without causing diseases and do not render the negative effect on the plant [4, 5]. Any of the 300,000 species of plants that exist in the world is the host for one or more species of endophytic bacteria [6]. However, currently, only a few of plant species have been sufficiently studied with respect to the presence of endophytes.
So, the search of new species of endophytic bacteria that have beneficial effect on the development of plants opens the prospects for the development of effective microbial preparations for adaptive crop production [7]. Bacterial endophytes colonize the same ecological niches in the plant as phytopathogenic microorganisms, so they are a promising agent for the biocontrol of phytopathogens [3].
Several studies have shown that endophytic bacteria are capable of inhibiting the development of pathogenic microorganisms [8, 9] and nematodes [1012] by the synthesis of biologically active compounds. The study of the biodiversity of these bacteria will make it possible to isolate and identify the substances for the new drugs against human, plant and animal diseases [6]. Also, some strains of endophytic bacteria can be used for phytoremediation, i.e. for the cleaning of technologically contaminated areas by creating special plant-bacterial systems [7, 13-18].
The endophyte niche in a plant can be taken only by those bacteria that penetrate plant tissues. Usually they colonize intercellular spaces and can be isolated from all plant parts, including seeds. Endophytic bacteria have been found in monocotyledonous and dicotyledonous plants, both woody (oak Quercus L., pear Pyrus L.) and herbaceous (sugar beet Beta vulgaris L., corn Zea mays L.) [19]. Classical studies were based on the characterization of isolates obtained from internal plant tissues after surface sterilization [20, 21]. Detailed lists of bacterial endophytes, including Gram-positive and Gram-negative species are given in several reviews [22, 23].
The study of endophyte microbial communities that inhabit stems, roots and tubers of crops by sequence analysis of the 16S RNA gene, fatty acids profile and utilization of various carbon sources, revealed that they are represented by the genera Celiulomonas, Clavibacter, Curtobacterium, Pseudomonas and Microbacterium [24]. The study of the aerial part of Crocus albiflo-rus revealed the diversity of bacterial endophyte communities, both previously known and unknown to science [25]. The high density of endophytic bacteria was observed in seedlings of poplar (Populus L.), spruce (Picea A. Dietr.) and larch (Lai Mill.) grown from tissue culture [26]. Based on the sequence analysis of the 16S RNA gene, the most of these isolates were classified as belonging to the Paenibacillus genus. Other endophytic bacteria of the genera Methylo-bacterium, Stenotrophomonas or Bacillus were found only in some poplar, spruce and larch tissue cultures. The Paenibacillus species that are close to P. humicus are accumulated in tissues in vitro without the apparent adverse effect on plants. Poplar microsprings inoculated with an endophytic strain of Paenibacillus sp. 22 had significantly more roots per spring, and such roots were longer compared to control roots after 3 weeks of culture [26].
In China (Hebei Province), the diversity of endophytic bacteria of rice was studied using the sequence analysis of the 16S RNA gene (Oryza sativa L.) [27]. The presence of phylae of bacteria belonging to the alpha, beta, gamma, delta and epsilon subclasses of Proteobacteria, Cytophaga, Flexibacter, Deinococcus-Thermus, Acidobacteria and archean has been shown. Betaproteobacteria were the dominant group (27.08 % of all isolates), in which the Stenotrophomonas genus was predominant. Over 14 % of the isolates belonged to the uncultivated bacterial species [27]. In India, the variety of endophytic bacteria was investigated in the stalks of maize (Zea mays L.) grown in the tropics [28]. Endophytes were found throughout the growing season. Their abundance was 1.36*105-6.12*105 CFU/g of raw biomass. Identification of bacterial isolates performed by chromatographic analysis of fatty acid profiles demonstrated the dominance of Bacillus pumlus, B. subtilis, Pseudomonas aeruginosa and P. fluorescens.
A total of 853 strains of endophytes were isolated in the study of four crop species, corn Zea mays L., sorghum Sorghum Moench, soybean Glycine max (L.) Merr. and wheat Triticum L., as well as a wide range of wild cereals and legumes. About half of them belonged to the Gram-positive, and the rest were the Gram-negative bacteria. The analysis of the profile of fatty acids showed that the isolates of endophytes belonged to 15 genera, Agrobacterium, Bacillus, Bradyr-
hizobium, Cellulomonas, Clavibacter, Corynebacterium, Enterobacter, Erwinia, Escherichia, Klebsiella, Microbacterium, Micrococcus, Pseudomonas, Rothia, Xanthomonas. Bacillus, Corynebacterium and Microbacterium were predominant. Moreover, endophytic bacteria of the Cellulomonas, Clavibacter, Curtobac-terium and Microbacterium genera isolated from both the cultural and wild plants were of the highest colonization activity in maize and sorghum [29].
Modern method of imaging of the microorganisms based on auto fluorescent proteins [30] help to detect and count the microorganisms in situ on the surface and within a plant [30-32]. One of these marker systems is represented by a green fluorescent protein (GFP), which proved to be very useful in the monitoring the colonization of internal plant tissues by pseudomonas [31, 32]. Bacterial cells with the gfp gene under a constitutive promoter integrated into the chromosome can be readily identified using epifluorescent microscopy or a confocal laser scanning microscope [15, 33]. The colonization of internal plant tissues by endophytic bacteria can also be visualized using a p -glucuronidase (GUS) reporter system. Thus, a GUS-labeled Herbaspirillum seropedicae Z67 strain was used to inoculate rice seedlings. At this, the most intense staining was observed in coleoptiles, roots and at the junction of lateral roots to the main root [34]. Subsequently, Herbaspirillum seropedicae colonizes intercellular space, aeren-chyma and cortical cells, and some bacterial cells can permeate the stele and further into the vascular tissue.
Visible anatomical differentiation of the partners is not characteristic of the plant associations with endophytic bacteria. However, the molecular mechanisms described for the legume-Rhizobium and arbuscular-mycorrhizal symbio-ses may be involved in their development [35].
There is evidence indicating the existence of certain specific interactions in the system of «endophytic bacteria—host plant». The Azoarcus sp. obligate nitrogen-fixing endophyte (strain BH 72) has been shown to induce the defense mechanisms of the host plant, making the colonization of rice with other endophytic bacteria difficult [36]. As a result of maize seedlings inoculation by dominant strains of stem endophytes Bacillus pumilus, B. subtilis, Pseudomonas aeruginosa, and P. fluorescens, greatest density of endophytic bacteria in seedlings was observed in the variant with B. subtilis [37].
Investigations of the growth-stimulating activity of endophytic bacteria have been conducted [37]. Unlike the biological control strains of rhizosphere bacteria, they do not inhibit the growth of pathogenic microorganisms but stimulate plant growth by improving their mineral nutrition. Endophytic bacteria are able to improve phosphorus nutrition of plants [38, 39], to produce indolyl acetic acid [40], siderophores [41], and vitamins [42]. In addition, they have been shown to take part in the regulation of osmotic pressure, regulation of stomata, modification of root development, and regulation of nitrogen nutrition. In recent years, growth-stimulating endophytes have been actively used for reforestation and phytoremediation of technologically contaminated soils [7].
Endophytic bacteria are able to reduce or prevent the negative effects of pathogenic microorganisms on plants [18, 44, 45]. Inoculation of plants by endophytic bacteria is able to significantly reduce the harm caused to plants by pathogenic fungi, bacteria, viruses, insects and nematodes [22, 45-47]. Certain species of endophytic bacteria are assumed to trigger the defense mechanism of plants known as induced systemic resistance (ISR) which is similar to systemic acquired resistance (SAR) [7, 48]. Consequently, bacterial endophytes are promising for the development of environmentally friendly methods of microbiological control of plant diseases.
Many endophytes are the representatives of well-known soil bacteria of the genera Pseudomonas, Bacillus and Burkholderia [22] serving as producers of bacterial secondary metabolites (antibiotics, anti-cancer substances, volatile organic compounds, fungicidal, insecticidal and immunosuppressive agents). However, endophytic bacteria are still insufficiently used as sources of biologically active substances [7].
Unique strains of endophytic bacteria can be used directly for inoculation of seeds or seedlings, reducing the effect of biotic and abiotic factors on the plant, due to the active colonization of internal tissues of plants and subsequent positive biochemical and physiological effect on the plant. While in endosphere, endophytes have a significant advantage over organisms that live in the rhizosphere and phyllosphere due to the stable pH, humidity, flow of nutrients and lack of competition from a large number of microorganisms [42]. It is very important that endophytes are not accidental bacteria occupying the endosphere niche. Most likely, they are chosen by the very plant as most compatible and capable of providing it with the substances required for the protection against stress factors. The energy spent by the plant to produce the biomass of endophytic bacteria, is compensated by the improved development ofthe physiological state of the host.
The study of endophytes in the internal tissues of poplar showed that they are promising for the creation of microbial preparations used for phytoremediation of fields contaminated with toluene, volatile hydrocarbons and heavy metals [7, 15, 17].
Inoculation of plants with endophytic bacteria does not require large amounts of inoculum, taking into account high specificity of such plant-microbe symbiosis and the competitiveness of endophytic bacteria. This technique can be very attractive for biotechnological production, seeking for the replacement of traditional chemical pesticides. The future use of combinations of endophytes with commercial pesticides for the treatment of seeds or seedlings may result in a synergistic effect against one or more pathogens. Chemical pesticides can produce a transient inhibitory effect on phytopathogenic microorganisms, while the biological agents affect phytopathogens adversely throughout the growing season.
Thus, in nature, plants develop in close interaction with endophytic bacteria that are able to increase crop yields, promote soil phytoremediation, inhibit the development of pathogens, fix atmospheric nitrogen and produce biologically active substances. Using endofit-plant interactions can enhance the development of crops and reduce costs on the production of food and technical agricultural production. Understanding the mechanisms that ensure endophytic bacteria the ability to interact with plants and to positively affect their development will enable the better use of the biotechnological potential of these microorganisms.
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