1.1 Introduction

An intensification of agricultural production has been crucial in sustaining population growth throughout civilization history (Ellis et al. 2013). During the last century, the agricultural intensification has been largely achieved through improvement in crop productivity and the use of farm equipment, irrigation, intensive tillage, fertilizers, pesticides, and other manufactured inputs (Foley et al. 2005; 2011). However, these agricultural practices often lead to detrimental effects on environment as well as human health. Therefore, new environmentally benign pathways have to be employed to maintain increase in agricultural production while greatly reducing unsustainable uses of water, nutrients, and agricultural chemicals. This requires new means to overcome threats that cause loss of crop yield, including plant stresses associated with unfavorable environmental conditions, such as drought, temperature extremes, or soil salinity, as well as biotic stress induced by plant pathogens and pests. Therefore, the attention is drawn to exploitation of mutualistic and antagonistic biotic interactions within agroecosystems that would increase crop productivity and improve sustainability of pest control technologies (Gaba et al. 2014).

Plants live in intimate association with microorganisms that fulfill important functions in agricultural ecosystems and represent an important resource for improvement of plant performance through enhancing crop nutrition or reducing damages caused by pathogens or environmental stress (Jha et al. 2013; Singh et al. 2011). Bacteria constitute the most numerous group of microorganisms in soil (Whitman et al. 1998). They exist as free-living organisms, attached to the surface of roots or phyllosphere, and establish interactions with plants. The extreme forms of plant–microbe interactions could be categorized into commensal (acquire nutrients from the plant without damaging), mutualistic (positively influence plant health), and pathogenic (damage plant) type, yet many microorganisms exploit different forms of relationship with plants during their life cycles (Newton et al. 2010). Endophytic bacteria are a group of endosymbiotic microorganisms that live in internal plant tissues of apparently healthy host plants and do not normally cause any substantial disease symptoms (Schulz and Boyle 2006).

Endophytic bacteria colonize intercellular spaces of the cell walls and xylem vessels of plant roots, stems, and leaves, and they are also found in tissues of flowers (Compant et al. 2011), fruits (de Melo Pereira et al. 2012), and seeds (Cankar et al. 2005; Johnston-Monje and Raizada 2011; Trognitz et al. 2014). Meanwhile it is generally believed that endophytic bacteria reside in apoplast of plant cells, several studies of intracellular colonization of cytosol have been published (Cocking et al. 2006; Koskimaki et al. 2015; Thomas and Sekhar 2014; White et al. 2014). Plant roots have been established as the main entry point of the potential endophytes from soil and provide a base camp for colonization of other plant organs. Higher density of endophyte populations is characteristic to plant roots and other belowground tissues as compared to phyllosphere, and an ascending migration of endophytic bacteria from roots to leaves of rice plants has been demonstrated (Chi et al. 2005). It has been also shown that plant roots are capable to take up bacteria from surrounding environment (Paungfoo-Lonhienne et al. 2010). Isolation of endophytic bacteria from seeds suggests an alternative transmission route (Cankar et al. 2005; Johnston-Monje and Raizada 2011; Trognitz et al. 2014). Structure of the endophytic community is defined by abiotic and biotic factors such as environmental conditions, microbe–microbe interactions, and plant–microbe interactions (Ryan et al. 2008).

Diverse effects of endophytic bacteria on plant health and growth have been well documented. The endophytes aid nutrient availability and uptake, enhance stress tolerance, and provide disease resistance (Hamilton et al. 2012; Ryan et al. 2008). The plant growth-promoting capability of endophytes is established through activity that increases accessibility of nutrients, such as nitrogen and phosphorus, or is mediated by compounds produced by the microorganisms and the host cells, such as plant growth hormones (Brader et al. 2014; Glick 2012; Reinhold-Hurek and Hurek 2011). Disease protection properties are associated with ability of endophytic bacteria to produce compounds, such as antibiotics and fungal cell-wall lytic enzymes, which can inhibit growth of plant pathogens (Brader et al. 2014; Christina et al. 2013; Raaijmakers and Mazzola 2012; Wang et al. 2014) or priming plant response to pathogens by induced systemic resistance (ISR) mechanism (Pieterse et al. 2014). Owing to their plant growth-promoting and disease control properties, endophytes can be used in the form of bioinoculants in agriculture to benefit development of sustainable agricultural production practices (Mei and Flinn 2010).

The aim of this review is to outline the understanding about diversity of endophytic bacterial communities of agricultural crops and their implication in plant adaptation to stress and disease resistance. We provide a summary of the extensive information on taxonomic composition of bacterial endophytes identified in major agricultural crop plants that has been remarkably expanded due to application of advanced metagenomic analysis methods. Effect of different agricultural practices on the diversity of endophytic bacterial communities is assessed. Further, an implication of endophytes in plant adaptation to stress and disease resistance through modulation of phytohormone balance or induction of stress-related metabolites or systemic resistance signaling pathway is presented.

1.2 Assessment of Diversity of Bacterial Endophytes Using Cultivation Techniques and Metagenomic Analysis

Plants are naturally associated with continuum of other organisms, the majority of which are bacterial endophytes. Population densities of endophytic bacteria are extremely variable in different plants and tissues and have been shown to vary from hundreds to reaching as high as 9 × 109 of bacteria per gram of plant tissue (Chi et al. 2005; Jacobs et al. 1985; Misaghi and Donndelinger 1990). Initial studies of diversity of endophyte community were mostly based on the classic microbial culture techniques; therefore, bacterial endophytes isolated using surface sterilization methods have been reported for most species of agricultural plants (Rakotoniriana et al. 2013). One of the early reviews by Hallman et al. (1997) presented the list of isolated bacterial endophytes from various plant parts of different agricultural crops. The list was supplemented by latter studies on endophyte diversity (Bacon and Hinton 2007; Lodewyckx et al. 2002; Rosenblueth and Martinez-Romero 2006; Ryan et al. 2008; Sturz et al. 2003).

Innovative culture-independent sequencing technologies allow much deeper assessment of microbial communities and improve our understanding about diverse microbiomes occupying plants. In recent years, extensive information about diversity of endophytic microbiota has been gathered using metagenomic sequencing platforms. Application of hypervariable regions from small subunit ribosomal RNA gene (16S rRNA) for the metagenomic sequencing allows precise taxonomic identification (Turner et al. 2013). Direct amplification of microbial DNA from plant tissue samples and application of modern bioinformatics tools allow analysis of growing numbers of plant material samples, and such studies have revealed rarely reported endophyte species of δ- and ε-Proteobacteria (Sun et al. 2008). In addition, culture-independent high-throughput sequencing technologies reflect variations of total microbial diversity and their physiological potential and ecological functions (Akinsanya et al. 2015; Turner et al. 2013; van Overbeek and van Elsas 2008). For example, Tian and associates (Tian et al. 2015) used second-generation sequencing technology to assess diversity of bacterial endophytes before and after nematode attack, and the study revealed that nematode infection was associated with variation and differentiation of the endophyte bacterial populations.

Studies of microbial diversity using culture-independent molecular techniques could be limited by relatively low abundance of endophytic bacteria that results in underrepresentation in metagenomic library. This problem is associated with difficulties in separation and high sequence homology of endophytic bacteria, plant nuclei, plastids, mitochondria, and plant-associated microbial DNA (Govindasamy et al. 2014). In recent years, gene enrichment strategies have been broadly used. Bacterial DNA extraction from host plant tissues and enrichment is the key step in preparation of the metagenomic library harboring representative sample of microbial diversity. In order to recover target genes of metagenome, a suitable enrichment method should be used before DNA amplification (Mutondo et al. 2010). Jiao et al. (2006) enriched target genes from a metagenome by optimized hydrolysis of the plant cell walls, followed by differential centrifugation. Wang et al. (2008) efficiently enriched bacterial DNA from medicinal plant by specific enzymatic treatment. The same method increased representation of less abundant grapevine-associated bacteria (Bulgari et al. 2009). Series of differential centrifugation steps followed by a density gradient centrifugation efficiently enriched proportion of microbial DNA in stems of soybean (Ikeda et al. 2009). Maropola and colleagues (2015) analyzed the impact of metagenomic DNA extraction procedures on the endophytic bacterial diversity in sorghum and found that different DNA extraction methods introduce significant biases in community diversities. The authors stated that despite the differences in results of extraction of DNA, the agriculturally important genera such as Microbacterium, Agrobacterium, Sphingobacterium, Herbaspirillum, Erwinia, Pseudomonas, and Stenotrophomonas were predominant. An enrichment method useful for extraction of plant-associated bacteria of potato tubers was developed by Nikolic et al. (2011) and involved overnight shaking of small pieces of potato tubers in sodium chloride solution.

Although 16S rRNA gene clone library technique provides efficient means to study different agricultural plant microbiota in detail (genetics and physiology), however, not all endophytes are easily amenable using this method as well (Sessitsch et al. 2012). The methods for microbe enrichment in plant tissues may lead to overrepresentation of high-abundance bacterial species and reduced representation of low-abundance species. Therefore, a combination of microbial cultivation and culture-independent metagenomic analysis methods provides broader perspective of the diversity of endophytes.

A summary of the most widespread bacterial isolates identified in common agricultural crop plants is presented in Table 1.1. Due to a vast diversity of bacterial species and host plants described to this day, the list is not complete and presents a sample of important agricultural crops and overview of associated endophytic bacterial species identified using both, cultivation and metagenomic, analysis methods.

Table 1.1 Endophytic bacteria isolated from common agricultural crop species plants
Full size table

A study of direct comparison of culture-dependent and culture-independent approaches for assessing bacterial communities in the phyllosphere of apple has been published by Yashiro et al. (2011). Among the cultivated isolates only order of Actinomycetales has been found, while metagenomic approach has revealed the presence of Bacteroidales, Enterobacteriales, Myxococcales, and Sphingobacteriales. Differences between plant-associated microbial phyla are revealed when comparing the niches of rhizosphere, endosphere, and phyllosphere. The largest diversity is found in the roots, as it is the primary site of interaction between plants and soil microorganisms (Hardoim et al. 2011). Maropolla and colleagues (2015) found that diversity of sorghum-associated endophytic bacteria is lower in stems than that of rhizospheric communities. Rhizospheric endophytic species mostly belong to α-, β-, and γ-Proteobacteria subgroups and are closely related to epiphytic species (Kuklinsky-Sobral et al. 2004). The group of γ-Proteobacteria is found to be the most diverse. Culture-dependent methods revealed bacteria species that belong to the Proteobacteria, meanwhile Firmicutes, Actinobacteria, and also Bacteroides are less common (Reinhold-Hurek and Hurek 2011).

Culture-independent approach suggests a 100–1000-fold higher diversity of the bacterial communities in economically important crops (Suman et al. 2016; Turner et al. 2013). Sessitsch with associates (Chi et al. 2005) investigated genomic characteristics of the most abundant bacterial endophytes colonizing rice roots under field conditions without cultivation bias. In this study, the members of γ-Proteobacteria, comprising mostly Enterobacter-related endophytes, were predominant. Metagenomic analyses demonstrated that rhizobia (and other α-Proteobacteria) were the most abundant plant-associated endophytes, including β-Proteobacteria, γ-Proteobacteria, and Firmicutes (Turner et al. 2013). However, it was found that only culture-independent techniques were able to identify endophytic archaea (Euryarchaeota) (Suman et al. 2016). In general, the species of Pseudomonas, Bacillus, Enterobacter, Klebsiella, Rhizobium, Sphingomonas, Pantoea, Microbacterium, Acinetobacter, Erwinia, and Arthrobacter were defined as the most dominant using both methods.

1.3 Effect of Agricultural Practices on Diversity of Endophytic Bacterial Communities

Bacteria constitute the most numerous group of microorganisms in soil (Whitman et al. 1998), and many endophytic bacteria originate from the population of plant-associated microorganisms in rhizosphere (Hardoim et al. 2008). Microbial diversity of the plant rhizosphere itself is defined by overall composition of microbial pool of soil and further refined by specific plant–microbe interactions that are largely mediated by root exudates (Sorensen and Sessitsch 2006). It has been demonstrated that endophytic community represents a plant genotype-specific subset of the wider microbial population of soil (Bulgarelli et al. 2012; Lundberg et al. 2012). Agricultural land management, such as tillage or irrigation, greatly alters soil characteristics that may lead to reduction in soil microbial diversity due to mechanical destruction, soil compaction, reduced pore volume, desiccation, and disruption of access to food resources (Garcia-Orenes et al. 2013; Jangid et al. 2008). Several studies have established the effect of tillage systems on soil microbial communities in different soils and cropping systems (Balota et al. 2003; Dorr de Quadros et al. 2012; Mathew et al. 2012). The effect of excessive use of pesticides can induce significant changes in the function and structure of soil microbial populations due to direct inhibition of microbial growth or overall changes in the structure of agricultural ecosystems (Pampulha and Oliveira 2006). Balanced mineral or organic fertilizers have been shown to have positive effect on diversity and metabolic activity of the soil microbial community (Zhong et al. 2010).

The effect of the agronomic practices on the overall soil microbial community could be expected to reflect differences in endophyte populations of agricultural crop plants. However, the research aimed to elicit effect of agricultural practices on composition of the endophytic bacteria populations is limited to several studies. An early study by Fuentes-Ramirez et al. (1999) demonstrated that colonization ability of nitrogen-fixing endophytic bacterium Acetobacter diazotrophicus was largely decreased in the sugarcane plants fertilized with high levels of nitrogen. A recent study using automated ribosomal intergenic spacer analysis showed that structure of rice root endophytic community was affected by the nitrogen fertilization level (Sasaki et al. 2013). Another study assessed root bacterial endophyte diversity in maize grown using different fertilizer application conditions. Application of PCR-based group-specific markers revealed that type I methanotroph patterns were different for plants cultivated using mineral and organic fertilizer (Seghers et al. 2004).

Recently, culture-based and metagenomic analyses were employed to assess bacterial endophyte diversity of plants grown using conventional and organic practices. An extensive study by Xia et al. (2015) evaluated diversity of culturable bacterial endophytes in different tissues of corn, tomato, melon, and pepper grown using organic or conventional practices. The endophyte diversity was significantly higher among all the crops grown organically versus those grown using conventional practices. There were 32 species isolated from organically grown plants and 28 species from plants grown using conventional practices.

No significant effect of herbicide treatment on composition of the maize root endophyte population was detected using the PCR-based group-specific markers (Seghers et al. 2004). However, recent study using automated ribosomal intergenic spacer fingerprinting and metagenomic analysis using 16S rDNA pyrosequencing identified differences in the composition of endophytic communities in grapevines cultivated using organic and integrated pest management conditions (Campisano et al. 2014a). While a different outcome of the two studies might be a consequence of improvement in the capability of the analysis methods, it could as well be related to differences specific to the plant species or pesticide treatment conditions.

The studies described in this section showed that agricultural conditions could alter diversity of endophytic bacteria populations; however, further insight would be required to elucidate the mechanisms that mediate such changes. The variation in bacterial diversity could be a consequence of changes in overall soil microbial population upon the fertilizer treatment or application of other agronomic practices. On the other hand, the agronomical conditions potentially had a direct effect on the root endophytic bacterial community as was suggested by Xia et al. (2015). In addition, an important role might be attributed to differences in plant physiological state and changes in composition of the plant root exudates that influence growth of endophytic bacteria (Paungfoo-Lonhienne et al. 2010). This notion that factors related to plant biochemistry regulate endophyte diversity was supported by the study demonstrating that application of chitin resulted in changes in bacterial communities in soil, rhizosphere, and cotton roots, and the organic amendment supported the endophytic species in cotton roots that otherwise did not occur (Hallman et al. 1999). Intriguingly, it was shown that composition of the endophytic community was largely different from that of the rhizosphere; therefore, the amendment of chitin, which enhanced chitinase and peroxidase concentrations, might have changed preference of the plants for certain bacterial endophytes.

Another aspect related to the effect of agricultural practices on soil and plant microbiome is reflected by disease-suppressive soil phenomenon that is associated with the capability of soils to suppress or reduce plant disease of susceptible host plants in the presence of virulent pathogen (Weller et al. 2002). It was shown several decades ago that disease-suppressive properties of soil were largely induced by long-term cultivation of wheat and potato monoculture leading to buildup of host-specific microbial community (Lorang et al. 1989; Scher and Baker 1980; Whipps 1997). Further studies elucidated possible mechanisms of disease suppression that include competition for space and nutrients, antagonism due to production of secondary metabolites, and elicitation of ISR by soil microbiota (Philippot et al. 2013; Pieterse et al. 2014). Specific role of the endophytic bacteria in the development of the disease-suppressive traits was rarely addressed in the studies on disease-suppressive soil communities; however, bacteria of genus Streptomyces, Bacillus, Actinomyces, and Pseudomonas that are known to lead endophytic lifestyle were shown to contribute to the disease-suppressive traits of soils (Haas and Defago 2005; Kinkel et al. 2012; Mendes et al. 2011; Siddiqui and Ehteshamul-Haque 2001; Weller et al. 2002).

The importance of agricultural practices that maintain natural diversity of plant endophytic bacteria is emphasized by the observations that agricultural plants may become a niche for human pathogens and a source for outbreaks of food-borne illness (Brandl 2006). Use of manures contaminated with virulent bacteria was identified as a main source of human pathogens (Brandl 2006; Holden et al. 2009; van Overbeek et al. 2014). Other routes included irrigation water (Erickson et al. 2010) or flies (Talley et al. 2009). Meanwhile a decline of species antagonistic to the pathogenic bacteria in soil and endosphere was associated with plant colonization by human pathogen species (Latz et al. 2012); it was also demonstrated that the presence of certain plant pathogens and other species living in soil plays an important role in colonization of plants by human pathogens (Barak and Liang 2008; Brandl 2008; Brandl et al. 2013). On the other hand, typical plant-associated bacteria species belonging to the genera of Enterobacter, Serratia, and Klebsiella could become virulent to humans by acquisition of mobile genetic elements from human pathogens through horizontal gene transfer (van Overbeek et al. 2014). Pathogenic bacteria of the family Enterobacteriaceae, including pathogenic Salmonella genus strains, E. coli, Klebsiella pneumoniae, and Vibrio cholerae strains, and the human opportunistic pathogens Pseudomonas aeruginosa and Propionibacterium acnes were described as endophytic colonizers of plants (Campisano et al. 2014b; Deering et al. 2012; El-Awady et al. 2015; Kumar et al. 2013; Kutter et al. 2006; Schikora et al. 2008).

1.4 Role of Endophytic Bacteria in Adaptation of Agriculture Crops to Biotic and Abiotic Environmental Stress

1.4.1 Induction of Accumulation of Stress-Related Metabolites and Enzymes

Plants are capable to acclimate to environmental stresses by altering physiology to attain state adopted to overcome stress factors such as dehydration, mechanical injury, nutrient deficiency, high solar radiation, or stress-induced increase in concentration of reactive oxygen species. This acclimation is associated with enhanced production of compounds that mediate osmotic adjustment, stabilize cell components, and act as free radical scavengers. It has been observed that plant inoculation with endophytic bacteria leads to accumulation of such compounds, including proline, phenolic compounds, carbohydrates, and antioxidants.

It was shown that bacterial endophyte Burkholderia phytofirmans PsJN enhances cold tolerance of grapevine plants by altering photosynthetic activity and metabolism of carbohydrates involved in cold stress tolerance (Ait Barka et al. 2006; Fernandez et al. 2012). The presence of the bacterium in the plant promoted acclimation to chilling temperatures resulting in lower cell damage, higher photosynthetic activity, and accumulation of cold-stress-related metabolites such as starch, proline, and phenolic compounds (Ait Barka et al. 2006). Fernandez et al. (2012) demonstrated that bacterization of grapevine plants resulted in a twofold increase in soluble sugar content, and the plantlets inoculated with the bacterium displayed higher concentrations of the sugars known to be involved in low-temperature tolerance, such glucose, sucrose, and raffinose with its precursor, galactinol.

Positive effect of the B. phytofirmans PsJN strain on metabolic balance and reduced effect of drought stress was demonstrated in wheat plants grown under reduced irrigation conditions (Naveed et al. 2014). Inoculation with the bacterium resulted in higher antioxidant activity of plants compared to control under drought stress. However, in contrast to the grapevine plants in the study by Fernandez et al. (2012), the bacterium had no effect on sugar contents of the wheat, and phenolic contents decreased in the bacterized plants as compared to control.

Another endophytic bacterium, Bacillus subtilis B26, reduced a phenotypic effect of drought stress in Brachypodium distachyon grass compared to plants not harboring the bacterium (Gagne-Bourque et al. 2015). The protection from drought stress was associated with increase in total soluble sugars, glucose, fructose, and starch contents. However, no accumulation of stress response-related raffinose family carbohydrates was observed in either inoculated or control plants.

Pandey et al. (2012) evaluated cross-species stress reducing effect of wheat endophytic bacterium Pseudomonas aeruginosa PW09 in cucumber. Application of the PW09 strain induced increase in accumulation of proline and total phenolics under NaCl stress and pathogen Sclerotium rolfsii inoculation. Also, increase in activities of the enzymes involved biosynthesis of phenolic compounds, polyphenol oxidase, and phenylalanine ammonia lyase, as well as the antioxidative enzyme superoxide dismutase (SOD) was observed under biotic and abiotic stress conditions. Similarly, effect of six bacterial strains on stress-related biochemical traits of gladiolus plants was assessed in another study (Damodaran et al. 2014). The bacteria strains were shown to induce increase in activities of SOD, phenylalanine lyase, catalase, peroxidase enzymes, and accumulation of higher concentrations of proline and phenolic compounds in gladiolus plants grown in soil with high concentration of sodium. However, the capability of the different bacterial strains, isolated from soil, roots, culms, and leaves of grasses, to colonize endophytic niche was not explicitly confirmed.

A proline accumulation stimulating effect by endophytic strains of Arthrobacter sp. and Bacillus sp. was reported in pepper (Capsicum annuum L.) plants in vitro (Sziderics et al. 2007). Osmotic stress caused a similar increase in the content of free proline in the leaves of both inoculated and non-inoculated plants. However, higher concentration of proline was accumulated in leaves of unstressed plants inoculated with either of the two strains compared with unstressed non-inoculated plants. The bacterization resulted in a significantly reduced upregulation or downregulation of the stress-inducible genes suggesting that both strains reduced abiotic stress in pepper under osmotic stress conditions.

Endophytic bacteria Pseudomonas pseudoalcaligenes was shown to induce accumulation of higher concentrations of glycine betaine-like compounds leading to improved salinity stress tolerance in rice (Jha et al. 2011). At higher salinity levels, bacterization with mixture of both P. pseudoalcaligenes and rhizospheric Bacillus pumilus showed better response against the adverse effects of salinity. In this study, bacterization with either P. pseudoalcaligenes or both P. pseudoalcaligenes and B. pumilus resulted in lower levels of proline accumulation under the stress conditions, suggesting that different strategies of accumulation of osmoprotectant proteins in endophyte-inoculated plants were either plant or bacterium genotype-specific phenomena. Related study demonstrated that both of the bacterial strains induced production of defense-related enzymes, chitinase, peroxidase, and polyphenol oxidase, under biotic stress conditions in the presence of Magnaporthe grisea pathogen (Jha and Subramanian 2009).

Chen et al. (2014) demonstrated that endophytic bacteria Sphingomonas SaMR12 influenced the contents of root exudates, which were important for chelating cadmium ions and resulted in alleviation of the toxic metal stress in Sedum alfredii. Exudation of oxalic acid, malic acid, and tartaric acid was significantly affected by the inoculation of the endophytic bacterium in a manner dependent on cadmium treatment levels.

1.4.2 Effect on Phytohormone Balance

Ethylene (ET) is important for plant growth and development and has been extensively studied as mediator of plant stress response signaling (Gamalero and Glick 2015). Stress-induced accumulation of ET is usually deleterious to plant growth and health. ET is formed from methionine via S-adenosyl-L-methionine, which is converted into 1-aminocyclopropane-1-carboxylic acid (ACC) by the enzyme ACC oxidase (Bleecker and Kende 2000). ET is a key mediator of the plant defense response pathways that regulate colonization of plant tissue by endophytic bacteria (Iniguez et al. 2005). Endophytes may produce the enzyme ACC deaminase that has no function in bacteria but contributes to plant growth promotion and improved stress tolerance by cleaving the ET precursor ACC (Campbell and Thompson 1996). There are numerous reports on ACC deaminase-containing plant-associated bacteria and their role in improved plant growth and stress tolerance that has been recently reviewed by (Glick 2014).

Qin et al. (2014) isolated 13 ACC deaminase-producing putative endophytic bacteria of genera Bacillus, Pseudomonas, Klebsiella, Serratia, Arthrobacter, Streptomyces, Isoptericola, and Microbacterium from the halophyte plant Limonium sinense. It was suggested that the bacteria might play an important role in higher salinity tolerance of the plant as four of the selected ACC deaminase-producing strains were shown to stimulate growth of the host plants. An improved growth of Catharanthus roseus plant in 150 mM NaCl-containing soils was demonstrated for the plants inoculated with the Achromobacter xylosoxidans AUM54 strain (Karthikeyan et al. 2012). The bacterium was one of the four isolates isolated from C. roseus grown in saline soil and was shown to produce ACC deaminase.

In another study, tomato plants bacterized with ACC deaminase-containing endophytic Pseudomonas fluorescens YsS6 and Pseudomonas migulae 8R6 strains exhibited higher gain of biomass and a greater number of flowers and buds when grown under 165 mM and 185 mM NaCl levels as compared to the plants treated with ACC deaminase-deficient mutants of the bacteria or control with no bacterial treatment (Ali et al. 2014). Intriguingly, the study suggested the presence of different mechanisms of salt tolerance that might be plant genotype specific or stimulated by ACC deaminase-producing bacteria. It was shown that endophytic Pseudomonas sp. used in the study limited the concentration of sodium in tomato plant shoots (Ali et al. 2014). This was in contrast to previously reported rhizospheric Pseudomonas putida UW4 strain that was shown to be able to reduce ET levels in canola plants due to ACC deaminase activity (Cheng et al. 2007). In this case, sodium accumulated in root tissues and presumably partitioned into the vacuole.

In addition to salt stress tolerance, ACC deaminase-producing P. agglomerans Jp3-3 and Achromobacter xylosoxidans strain Ax10 were shown to alleviate stress of Brassica sp. plants grown in copper-contaminated soils and improved copper uptake by the plants (Ma et al. 2009; Zhang et al. 2011a). ACC deaminase-producing isolates from Commelina communis plants grown on lead and zinc mine soils were shown to improve growth of rape plants in the lead-contaminated soil (Zhang et al. 2011b).

Abscisic acid (ABA) is another phytohormone involved in plant stress response and is important for regulation of plant water balance and osmotic stress tolerance (Tuteja 2007). Information about role of ABA in endophytic bacteria-mediated stress tolerance is limited. It was described that endophytic bacteria Bacillus licheniformis Rt4M10 and Pseudomonas fluorescens Rt6M10 had drought stress reducing activity on plants grown in vitro that was associated with accumulation of high ABA levels in leaves of bacterized plants (Salomon et al. 2014). Cohen et al. (2009) showed that bacterization with Azospirillum lipoferum enhanced ABA accumulation and drought stress tolerance in maize plants. It was also suggested that plant performance under stress conditions was further enhanced by A. lipoferum-produced gibberellins (GAs). It is an intriguing observation as it is commonly believed that response to abiotic stress is associated with reduced plant growth-promoting hormone GA levels. However, GA signaling is closely integrated to ABA and ET signaling during the response to abiotic stress (Colebrook et al. 2014), and the interaction of the stress response pathways and exogenous hormone produced by plant growth-promoting bacteria remains ambiguous.

1.4.3 Induced Systemic Resistance and Priming of Response to Biotic Stress

Pathogen defense response priming, termed as induced systemic resistance, is activated by nonpathogenic plant-associated microorganisms. The ISR primes plant defense mechanisms and protects non-exposed plant parts against a future attack by pathogenic microbes and herbivorous insects. Plant hormones jasmonic acid (JA) and ET play a major regulatory role in the network of interconnected signaling pathways involved in ISR induction; however, the details of mechanism of the defense priming during ISR remain vague (Pieterse et al. 2014). There is an evidence for the role of transcription co-regulator NPR1 in the JA-/ET-dependent ISR and its cytosol-specific function that is different from the function involved in pathogen-induced systemic acquired resistance (SAR) (Spoel et al. 2003; Stein et al. 2008). Further, the role of transcription factors MYB72 and MYC2 in establishment of the ISR induced by rhizobacteria and priming of JA-/ET-dependent defense genes has been demonstrated (Pozo et al. 2008; Van Der Ent et al. 2008). In addition to the JA-/ET-mediated ISR activation pathway, an evidence that salicylic acid produced by plant growth-promoting bacteria could elicit ISR response has been discussed (Bakker et al. 2014).

Many studies have been dedicated to the ISR mediated by free-living rhizobacterial strains (Choudhary and Johri 2009); however, a number of endophytic bacteria have been reported to have the ISR-inducing activity as well. The first study demonstrating that endophytic bacteria could elicit ISR in plants was published in 1991 and showed that inoculation of cucumber roots with endophytic Pseudomonas fluorescens strain 89B-61 could induce resistance against cucumber anthracnose in the plant leaves (Kloepper and Ryu 2006; Wei et al. 1991). Subsequently attention was drawn to ISR mediated by several other endophytic species of genus Pseudomonas and the effect was characterized in different plant–pathogen systems. Pseudomonas sp. strain PsJN isolated from onion roots (Frommel et al. 1991) was shown to suppress verticillium wilt (Verticillium dahliae) on tomato seedlings and tissue culture plantlets grown in vitro, and it was proposed that the protection was mediated through the ISR activation (Sharma and Nowak 1998). Pseudomonas sp. strain 63–28 was shown to induce systemic resistance in tomato and pea plants leading to reduced damage by Fusarium oxysporum root pathogen (Benhamou et al. 1996; M’Piga et al. 1997). Pseudomonas putida MGY2 was isolated from papaya fruits and had reducing effect on postharvest decay of papaya fruit caused by Colletotrichum gloeosporioides (Shi et al. 2011). It was established that bacterization with the endophytic pseudomonad upregulated expression of enzymes involved in plant defense response, phenylalanine ammonia lyase, catalase, and peroxidase. A study by Ardanov et al. (2011) demonstrated that Pseudomonas sp. IMBG294 reduced symptoms of soft rot disease caused by bacterial pathogen Pectobacterium atrosepticum in potato plants. The assessment of expression of PR2 and PDF1.2, the molecular markers of the SAR and ISR, respectively, in Arabidopsis–Pseudomonas syringae model revealed that the endophytic bacterium was able to induce disease resistance via defense priming.

The asporogenous pseudomonads demonstrated poor performance when used in commercial plant protection products due to lack of long-term viability; therefore, subsequently much attention was drawn by plant growth-promoting strains of Bacillus sp. (Kloepper et al. 2004). ISR mediated by endophytic Bacillus pumilus strain SE34 was described by Benhamou et al. (1996; 1998). The bacterial strain reduced symptoms of root-rotting fungus Fusarium oxysporum infection in pea through induction of plant defense mechanism leading to accumulation of callose and phenolic compounds in the root epidermal and cortical cell walls and formation of the barriers beyond the infection sites (Benhamou et al. 1996). The same B. pumilus SE34 strain induced resistance to Fusarium oxysporum infection in tomato plants (Benhamou et al. 1998).

In addition, ISR mediated by endophytic Serratia sp. (Benhamou et al. 2000), Methylobacterium sp. (Ardanov et al. 2011), and actinobacteria Streptomyces sp. (Conn et al. 2008) was described. The early study by Benhamou et al. (2000) demonstrated that Serratia plymuthica strain R1GC4 sensitized susceptible cucumber seedlings to react more rapidly and more efficiently to infection by soilborne pathogen Pythium ultimum (Benhamou et al. 2000). The defense reaction was associated with deposition of enlarged callose-enriched wall appositions, also containing pectin, cellulose, and phenolic compounds.

The capability of endophytic actinobacteria Streptomyces sp. strains, isolated from wheat tissues, to activate the SAR or ISR pathways was assessed using Arabidopsis thaliana (Conn et al. 2008). It was demonstrated that the Streptomyces sp. EN27 was able to prime both pathways depending on the infecting pathogen. Resistance to Erwinia carotovora subsp. carotovora occurred via an NPR1-independent pathway and required salicylic acid, whereas the JA/ET signaling molecules were not essential. In contrast, induction of resistance to Fusarium oxysporum was mediated by NPR1-dependent pathway but also required salicylic acid and it was JA/ET independent.

Intriguingly, the study on induction of disease resistance to soft rot pathogen Pectobacterium atrosepticum in potato plants demonstrated that priming capacities of Methylobacterium sp. IMBG290 was inversely proportional to bacterial inoculants size (Ardanov et al. 2011). The difference in plant response mechanisms was associated with different patterns of activity of reactive oxygen species scavenging enzymes SOD and catalase. Plants treated with a low titer of Methylobacterium sp. showed higher SOD activity and unchanged catalase activity resulting in the development of ISR; meanwhile higher Methylobacterium sp. density caused SOD inactivation and catalase activation after inoculation with the pathogen and was followed by hypersensitive response.

1.5 Concluding Remarks

Several decades of research on endophytes in agricultural plants have revealed an immense taxonomic diversity of the endophytic bacteria. The endophytic species have been mostly reported throughout α-, β-, and γ-subgroups of phylum Proteobacteria, the latter being the most diverse and dominant group that includes common soil and endophytic bacteria of Pseudomonas sp. Next to the pseudomonads, much attention has been dedicated to members of Bacillus sp. that belongs to phylum Firmicutes. A number of other species of phyla Firmicutes and Actinobacteria have been identified as endophytic bacteria as well. During the last decade, development of metagenomic analysis techniques has brought to light new aspects of the diversity of endophytic bacteria including identification of new unculturable species and establishment of the dynamics of endophyte diversity that provide hints about physiological significance and ecological functions of the complex host plant and endophytic bacteria interactions.

Composition of the endophytic microbiome depends on plant genotype as well as environmental factors. Evidence has been presented that agricultural practices play an important role in shaping structure of the endophytic microbial community of agricultural crop plants. Therefore, assessment of the capability of modern agronomical techniques to maintain natural diversity of plant endophytic bacteria should become an important element in the development of sustainable agricultural practices. In addition, numerous studies have demonstrated beneficial effects of the endophytic bacteria on plant growth and adaptability to biotic or abiotic stresses through modulation of phytohormone signaling, production of metabolites involved in stress response, and priming of plant defense response pathways. The endophytes play an integral role in balancing plant physiology and functioning of agroecosystems; thus, understanding of composition and functioning of the plant-associated microbial communities has a large potential for improvement of performance of agricultural crops and development of integrated plant disease management systems.