Next Article in Journal
The Small Regulatory RNA Spot42 Inhibits Indole Biosynthesis to Negatively Regulate the Locus of Enterocyte Effacement of Enteropathogenic Escherichia coli
Next Article in Special Issue
Bacterial Microbiota of Rice Roots: 16S-Based Taxonomic Profiling of Endophytic and Rhizospheric Diversity, Endophytes Isolation and Simplified Endophytic Community
Previous Article in Journal
Biotechnological Applications of Microbial (Per)chlorate Reduction
Previous Article in Special Issue
Combating Fusarium Infection Using Bacillus-Based Antimicrobials
Open AccessReview

Bacterial Endophyte Colonization and Distribution within Plants

School of Environmental and Forest Sciences, College of the Environment, University of Washington, Seattle, WA 98195-2100, USA
Author to whom correspondence should be addressed.
Present address: USDA-ARS, Crop Improvement and Research Unit, 1636 E. Alisal St., Salinas, CA 93905, USA.
Microorganisms 2017, 5(4), 77;
Received: 3 November 2017 / Revised: 21 November 2017 / Accepted: 23 November 2017 / Published: 25 November 2017
(This article belongs to the Special Issue Symbiotic Plant-Bacterial Endospheric Interactions)


The plant endosphere contains a diverse group of microbial communities. There is general consensus that these microbial communities make significant contributions to plant health. Both recently adopted genomic approaches and classical microbiology techniques continue to develop the science of plant-microbe interactions. Endophytes are microbial symbionts residing within the plant for the majority of their life cycle without any detrimental impact to the host plant. The use of these natural symbionts offers an opportunity to maximize crop productivity while reducing the environmental impacts of agriculture. Endophytes promote plant growth through nitrogen fixation, phytohormone production, nutrient acquisition, and by conferring tolerance to abiotic and biotic stresses. Colonization by endophytes is crucial for providing these benefits to the host plant. Endophytic colonization refers to the entry, growth and multiplication of endophyte populations within the host plant. Lately, plant microbiome research has gained considerable attention but the mechanism allowing plants to recruit endophytes is largely unknown. This review summarizes currently available knowledge about endophytic colonization by bacteria in various plant species, and specifically discusses the colonization of maize plants by Populus endophytes.
Keywords: bacterial endophytes; colonization; microscopy; Populus endophytes bacterial endophytes; colonization; microscopy; Populus endophytes

1. Introduction

The term “endophyte” is derived from the Greek words “endon” meaning within, and “phyton” meaning plant. Previously, endophytes were defined as microorganisms such as bacteria and fungi that inhabit the plant endosphere during all or part of their life cycle without causing any apparent harm to the host plant [1,2]. However, the definition of endophytes has been revised multiple times by different authors [1,3,4]. More recently, Hardoim et al. [4] defined endophytes as microbes including bacteria, archaea, fungi, and protists that colonize the plant interior regardless of the outcome of the association. Conventionally, endophytes were isolated from surface sterilized plant tissue and cultivated in nutrient rich medium. In recent years, many endophytes have been identified through culture-independent approaches such as sequencing of the 16S rRNA gene, the internal transcribed spacer regions, ITS1 and ITS2, or through whole genome sequencing of endophyte communities [5,6,7,8].
Bacterial endophytes that are beneficial to plant growth and development are the focus of this review. They are found across many phyla, including the Proteobacteria, Actinobacteria, Firmicutes and Bacteroidetes [4,9,10,11]. Increased biomass and height in inoculated plants have been reported as a result of colonization by many endophytic genera such as Azoarcus, Burkholderia, Gluconobacter, Klebsiella, Pantoea, Herbaspirillum, Rahnella, and Pseudomonas [12,13,14,15,16,17,18,19]. Common characteristics of endophytes include the ability to synthesize plant hormones such as indole-3-acetic acid, solubilize phosphate, secrete siderophores, and confer plant tolerance to biotic and abiotic stresses [20,21,22,23]. Additionally, some bacterial endophytes carry genes necessary for biological nitrogen fixation (BNF), potentially enabling them to convert dinitrogen gas (N2) into usable forms of nitrogen such as ammonium and nitrate within the host plant [24,25].
Symbiotic N-fixation by rhizobia in legume plants or Frankia in actinorhizal plants, respectively, has been an active area of research for decades. However, the discovery of N-fixing bacterial endophytes in the non-nodulating plants such as sugarcane during the late 1980′s has expanded the area of BNF research [26,27]. Bacterial endophytes in several genera such as Azoarcus, Burkholderia, Gluconobacter, Herbaspirillum, Klebsiella, Pantoea, and Rahnella were found in many different plants, facilitating the growth of the host plant in nutrient-poor conditions [10,22,28,29]. N-fixation involves reducing the triple bonds of N2 molecules, which requires substantial amounts of energy. Given this energy demand, free-living N-fixers likely have relatively limited applications in agriculture compared to plant-associated N-fixers, which can overcome the energy requirement of N-fixation by deriving energy from the host plant [30]. Bacterial endophytes reside in the internal plant tissues which may be a favorable environment for N-fixation that minimizes competition with other microbes in the rhizosphere as well as possibly providing a microaerobic environment that is necessary for nitrogenase activity [31,32,33].
The use of bacterial endophytes in agriculture has immense potential to reduce the environmental impacts caused by chemical fertilizers, especially N fertilizers. Several studies have shown that a significant portion of N used in agriculture is lost to the environment. It is estimated that only 17 Tg N of every 100 Tg N used in global agriculture is utilized [34,35,36]. The N lost from farmlands eventually accumulates in lakes, rivers or marine systems causing excessive growth of algae, which has serious impacts on aquatic ecosystems. Greater atmospheric N, in the form of ammonia or ammonium, also coincides with areas of eutrophication in the downwind regions of farmland. Elevated concentrations of N in the form of ammonium, nitrate or nitric acid vapors in the atmosphere can reduce air quality, reduce visibility and impact plant growth [37,38]. In addition, microorganisms convert excess ammonium or nitrate in the soil into nitrous oxide, which is a potent greenhouse gas. The use of natural symbionts such as bacterial endophytes could reduce the need for fertilizer inputs in the growth of crop plants and potentially lead to making farming more environmentally sustainable in the future.
Bacterial endophyte strains promote plant growth by synthesizing phytohormones including indole-3-acetic acid (IAA), cytokinins and gibberellins or through regulating internal hormone levels in the plant body [4,39,40]. IAA produced by endophytes within plants increases the number of lateral and adventitious roots, facilitating access to nutrients, and improving root exudation, offering more resources for soil microbes to interact with roots [40,41]. Growth enhancement by increasing plant height and/or biomass has been reported in many studies when plants were inoculated with bacterial endophytes capable of producing IAA [39,42,43,44,45]. Furthermore, bacterial endophytes secrete siderophores and solubilize phosphorus in soil while initiating the symbiotic interactions with host plants [4,41]. Siderophores are organic compounds secreted by microorganisms and plants in iron limited conditions enabling them to chelate iron from the environment for microbial and plant cells to uptake [4,46]. Similarly, phosphorus-solubilizing bacteria can solubilize immobile phosphorus in soil, which is potentially available for plants to absorb, an important trait for plant growth promotion [47,48,49,50]. Many recent reviews highlighted the mechanisms and importance of phosphorus solubilizing microorganisms in agriculture [4,51].
Bacterial endophytes can confer resistance or tolerance to the host plant from biotic and abiotic stresses by releasing antimicrobial compounds, producing siderophores, competing for space and nutrients, and modulating the plant resistance response [39,52,53]. Some bacterial strains can relieve plant stress by blocking the pathway of ethylene synthesis in plants. These bacteria utilize 1-aminocyclopropane-1-carboxylate deaminase, which helps to reduce ethylene concentrations accumulated in response to different stresses in plants, otherwise lethal to plant health [54]. Endophytic strains of Bacillus, Burkholderia, Enterobacter, Pseudomonas, and Serratia were found to be effective in suppressing the growth of pathogenic microorganisms in in vivo and in vitro conditions [53,55,56,57]. Moreover, endophyte strains in the genera Bacillus, Enterobacter, Pseudomonas, Azotobacter, Arthrobacter, Streptomyces, and Isoptericola were successful in alleviating drought, heat, and salt stress in different crop plants. More importantly, symbiotic plants with these endophytes were not only capable of relieving the stress but also significantly increased plant biomass and height [58,59,60,61,62]. However, the mechanisms used by bacterial endophytes to mitigate abiotic stress remain unclear.

2. Recruitment of Bacterial Endophytes by Host Plants

The rhizosphere is defined as the soil-root interface where complex interactions take place between the plant and surrounding soil microorganisms [9,63]. It has been reported that plants can release significant amounts of photosynthates or exudates from its roots, which influence microbial communities in the rhizosphere. Root exudates including organic acids, amino acids, and proteins may be involved in recruiting bacterial endophytes from the rhizosphere [9,64,65]. Root exudates likely contain substrates that initiate early communication between host plants and bacterial endophytes, and consequently steer the colonization process. For example, evidence of the involvement of oxalate in the recruitment of the beneficial bacterial strain Burkholderia phytofirmans PsJNby host plants has been reported [66]. In this study, a Burkholderia phytofirmans strain defective in oxalate utilization was used to inoculate lupine and maize plants that secrete moderate and low levels of oxalate, respectively. The mutant was observed in significantly less numbers in both maize and lupine plants 3 days after inoculation as compared to the wild type strain. Interestingly, inoculation with both wildtype and mutant strains resulted in significant differences in colonization by the two strains in lupine but not in maize. Oxalate was also observed in Brachypodium root exudates, and high numbers of Proteobacteria were detected in the Brachypodium rhizosphere [64].
Moreover, bacterial quorum sensing compounds are likely involved in communication with the plant root and the subsequent colonization process. The importance of these compounds in the colonization and growth promotion of plants by endophytes is supported by a recent study that showed that a quorum sensing mutant of Bukholderia phytofirmans PsJN could no longer efficiently colonize Arabidopsis thaliana and did not promote its growth [67]. Plants are likely directly involved in quorum sensing as well, given that some plant extracts have been shown to have quorum quenching capabilities which could protect them against pathogens and some quorum sensing molecules have been shown to have direct plant growth promoting effects [68]. Additionally, several endophytes of Populus deltoides were found to have LuxR homologs hypothesized to be involved in responding to plant derived compounds [69]. This study also found that many of the surveyed endophyte genomes contained LuxR-LuxI type quorum sensing gene pairs pointing to their importance in the endophytic lifestyle. The importance of quorum sensing compounds for plant-microbe interactions has been reviewed in detail by Hartmann et al. [70].
The native soil composition and host plant genotype are also considered important in the recruitment of bacterial endophytes by the host plant. A detailed study of root endophytes of Arabidopsis plants grown in different soils concluded that soil type likely influences the composition of the bacterial endophyte community found in the host roots. This indicates that different soil types may be inhabited by variable bacterial populations that serve as the initial inocula [9]. In addition, Wagner et al. [71] showed that bacterial communities (epiphytic and endophytic) in Boechera stricta, a perennial wild mustard plant, are highly similar in both leaves and roots supporting the hypothesis that the communities are recruited from the soil. This study also showed that environmental conditions such as soil nutrition, moisture, temperature, and host genotype and age have a direct influence on root and leaf bacterial communities. Diverse bacterial communities were reported in grass species Dactylis glomerata, Festuca rubra, and Lolium perenne under different management regimes, such as fertilizer application and mowing frequencies, indicating that agronomic operations may influence bacterial endophyte recruitment in cultivated plants. Interestingly, in these grasses, the functional profile of the bacterial communities was not correlated with changes in community composition at the species-level, suggesting that selection of endophytes by the plant may be functionally driven rather than driven by phylogeny [11]. Furthermore, direct influence of crop genotype and N fertilizer application on the diversity of N-fixing (diazotrophic) endophytes was detected in maize and rice plants [72,73]. A detailed study of the root microbiome of Arabidopsis showed that only a narrow subset of rhizosphere communities was able to colonize and establish in the root endosphere [74]. Overall, molecular mechanisms by which plants select specific bacterial endophytes over others remain largely unknown [66,70].

3. Attachment of Bacterial Endophytes to the Host Plant Surface

The attachment or adhesion of bacterial cells to the plant surface is considered the first step of the colonization process. Bacteria in the vicinity of the plant roots most likely swim towards the roots, using chemotactic affinities for root exudates. This is followed by attachment to the root surface, which is likely important in getting access to potential entry sites at lateral root emergence areas or other openings caused by wounds or mechanical injuries. The exopolysaccharides (EPS) synthesized by bacterial cells may facilitate the attachment of bacterial cells onto the root surface and may be important in the early stages of endophytic colonization. The EPS produced by endophytic bacterium Gluconacetobacter diazotrophicus Pal5 was reported as an essential factor for rice root surface attachment and colonization [75]. A recent colonization study in rice plants using G. diazotrophicus Pal5 showed that bacterial cells were shielded from oxidative damage by exopolysaccharides, which may be crucial for colonization. Additionally, free radical concentrations in planta were decreased by the application of EPS. Colonization was reduced in an EPS knockout strain of G. diazotrophicus. Interestingly, this reduction in colonization was rescued by the addition of EPS produced by the wild type strain [76]. In another study, Balsanelli et al. analyzed the mutant strains of Herbaspirillum seropedicae that are deficient in EPS production and concluded that EPS is not required for plant colonization, which could potentially point to a variation in the genes required for colonization across different endophyte species [77]. The biology of bacterial EPS including its synthesis, chemistry and functions were reviewed elsewhere [78].
Bacterial structures such as flagella, fimbriae or cell surface polysaccharides are also likely involved in the attachment of bacteria to the plant surface. While studying colonization of maize plants by endophyte H. seropedicae, Balsanelli et al. reported that bacterial lipopolysaccharide (LPS) is necessary for attachment and subsequent endophytic colonization of plant roots [79]. Later, it was also demonstrated that binding of N-acetyl glucosamine of LPS with maize root lectins is required for bacterial attachment and subsequent colonization inside the roots [80]. Bacterial adherence and colonization of the root interior likely happen in close succession given how quickly colonization is observed in roots after inoculation with bacterial endophytes [81,82,83]. The process of adherence of Rhizobia on legume roots, plant pathogenic bacteria on plant leaf or root surfaces, and Agrobacterium on roots of the host plant has been thoroughly studied in the past [84,85,86]. However, the mechanisms by which bacterial endophytes attach on plant surfaces remain relatively unexplored [87].

4. Entry of Bacterial Endophytes into the Host Plant

Bacterial endophytes initially attach to the root surface also called rhizoplane, and explore the potential entry sites to access the internal plant tissues. Openings in the roots where root hairs or lateral roots emerge, as well as stomata, wounds and hydathodes in the shoots are considered the main entry points that endophytes use to enter the host plant [4]. Endophytic bacteria likely utilize these natural discontinuities in the plant body to access the internal plant tissues. Moreover, some bacterial endophytes may modify the plant cell wall by secreting cell wall cellulolytic enzymes such as cellulases, xylanases, pectinases, and endoglucanases, which facilitate bacterial entry and spread within the plant tissues [81,88,89]. One study supported this hypothesis by observing that the frequency of entry of an endoglucanase mutant of Azoarcus sp. BH72 into rice roots was decreased as compared to the wild type strain and the mutant was unable to spread to the aerial plant parts [88]. Many colonization studies suggested that natural cracks at the lateral root emergence site are the most common entry sites for endophytic bacteria [4,14,81]. Furthermore, some bacteria use root apex and root hairs as entry points followed by endophytic colonization in root cortex and vascular tissues [90,91].

5. Bacterial Niches inside the Host Plant

Bacterial endophytes most often occupy intercellular spaces in the plant, most likely because these areas have an abundance of carbohydrates, amino acids, and inorganic nutrients [4,12,27]. They likely exclusively colonize the intercellular spaces of various plant parts including roots, leaves, stems, flowers, and seeds [14,18,81,92,93,94]. Colonization can be localized at the tissue level or systemically throughout the plant body. In the early stages of endophytic colonization, endophytes are first observed in root hairs, and subsequently in the root cortex [83,90,95]. Inoculated Burkholderia sp. strain PsJN was observed in cortical cells, endodermis, and xylem vessels, and colonization was especially strong at primary and secondary roots and at the base of lateral roots and root tips. Interestingly, in this study, both intracellular and intercellular colonization was observed [81]. In maize plants, bacterial endophytic colonization was stronger in the lower stem compared to the stem closer to the shoot apex [96]. The mobility of bacterial cells accompanied by the synthesis of cellulolytic enzyme may help endophytes to spread to aerial plant parts including leaves and stems [12,25,81].
In leaves, bacterial endophytes have been observed in the intercellular spaces of mesophyll, and xylem tissues and substomatal areas. Using green fluorescent protein (GFP) labeling and β-glucuronidase (GUS) staining, Burkholderia sp. strain PsJN was observed in xylem and substomatal chambers of inoculated leaves of grape vine plants. Interestingly, bacterial cells leaving through the stomatal aperture were also observed in grapevine leaves [81]. The demand for nitrogen in the production of rubisco and other photosynthetic enzymes may suggest an important role for BNF by bacterial endophytes in the leaves. For example, studies have shown that diazotrophic endophytes Klebsiella variicola colonized the mesophyll cells of sugarcane leaves; Herbaspirillum sp. colonized young leaves and shoots of wild rice; Herbaspirillum seropedicae Z67 colonized leaf vein, mesophyll cells, and substomatal cavities of rice leaves; and Serratia marcescens colonized the leaf sheaths and leaf aerenchyma of rice plants [12,97,98,99]. Niches of indigenous bacterial endophytes in different sections of grapevine leaf pieces were found by florescence in situ hybridization (FISH) and confocal laser scanning microscopy. Bacterial microcolonies were observed in leaf veins, trichomes, and cut sections of leaf pieces. Colonization was strong in various layers of the leaf tissue [100].
One relatively new area of research that remains poorly studied is intracellular colonization of plant cells by endophytes. Endophytes are known to typically colonize the intercellular spaces of plants but several examples of intracellular colonization of plants by bacteria have been reported recently [101]. These examples include the presence of intracellular bacteria in shoot-tips of banana, shoot meristem of Scotch pine, seedling roots of switchgrass and in micro propagated peach palm [102,103,104,105]. While this area of research is relatively new and unexplored, several hypotheses exist as to the potential colonization pathway intracellular endophytes use. Root hairs offer a logical point of entry for these endophytes as many cases of intracellular plant-microbe interactions begin with colonization of the microbe through intracellular access to root hairs. This is the case in the very well-studied legume-rhizobium symbioses and is one method reported to be used by some endophytes [90,106]. The role of each symbiotic partner in intracellular colonization remains unclear. Endophytes may be capable of gaining access to the intracellular space directly by secreting cell wall degrading enzymes or through a phenomenon known as rhizophagy [104,107]. Rhizophagy is a recently observed process in which roots of certain plants actively bring microbes in the soil into their cells, possibly in order to digest them and acquire essential nutrients from them [108].
The advantages to this peculiar kind of endophytic colonization remain unclear. One possible hypothesis is linked to the observation that intracellular colonization by endophytes is associated with a bombardment of the colonizing endophytes by intracellular hydrogen peroxide. This allowed the authors to use a hydrogen peroxide stain to detect the intracellular bacteria but also points to a potential advantage of this interaction for the plant [104]. Briefly, increasing intracellular reactive oxygen species (ROS) concentrations in the plant could acclimate the plant to ROS stress, which could increase its tolerance to stressors linked to ROS stress such as drought, heat and salt stress [109]. Survival in the intracellular environment is likely a specific adaptation of the endophytes to this environment and could provide the endophyte with a niche with low competition. The specificity of this adaptation is supported by a change of shape of the intracellular endophytes of switchgrass to an L-form lacking a cell wall as well as the fact that many of these endophytes are not currently culturable [102,104]. While this phenomenon seems widespread, the difficulty of culturing intracellular endophytes makes them very difficult to study [102]. Classic microbiology methods relying on culturing the endophytes, including fluorescent tagging, may be difficult to implement in the study of these intracellular endophytes. It is possible that a stronger reliance on next generation sequencing, metagenomics and FISH may be necessary to further study the life cycle and ecology of these endophytes.

6. Bacterial Genes Involved in Plant Colonization

The production of ROS, mainly superoxide (O2), hydrogen peroxide (H2O2), and hydroxyl radicals (OH), are well understood as being an important immediate plant defense response in plant-microbe interactions [110,111,112]. During the plant-endophyte interaction, ROS-detoxification occurs early on, after entry of the endophyte into the plant. During the early stages of rice root colonization, endophytic diazotrophic bacterium Gluconacetobacter diazotrophicus expressed ROS-deactivating genes such as superoxide dismutase (SOD) and glutathione reductase (GR) in greater amounts. Furthermore, SOD and GR mutants of G. diazotrophicus could not colonize rice roots supporting the hypothesis that ROS-deactivating genes are important during the initial stages of colonization [113]. In addition, a gum gene cluster, gumD, in G. diazotrophicus, involved in EPS production, was shown to be required for biofilm formation and plant colonization. A genomic survey using comparative genomics of endophyte strains hypothesized that many genes involved in biofilm production, adhesion, and motility contribute to plant colonization and the endophytic life style within the host plant [6,114,115,116,117]. The metabolic adaptations required for root attachment, modification of the plant cell wall and life in the microaerobic environment within the plant was reported in the endophyte strain Herbaspirillum seropedicae. Increased gene expression of genes linked to N-fixation, auxin production and ABC transporters during interaction with the host plant was reported in this strain [87]. Many genes involved in bacterial chemotaxis and secretion systems were found in bacterial groups colonizing the Brachypodium rhizosphere and may be expressed during the colonization of roots by these endophytes [64].

7. Colonization Cycle of Bacterial Endophytes in the Host Plant

Bacterial endophytes are capable of colonizing different seed parts including the embryo. These endophytes likely mobilize and grow in the developing seedlings during germination and early seedling growth [118,119,120]. As seedlings emerge and plant growth begins, interactions between the roots and the soil microbiome commence. Plant exudates fuel microbial activities in the rhizosphere, which facilitate the attachment and entry of bacteria into the plant roots. Eventually, certain endophytes initiate colonization of tissues beyond the roots such as the stems and leaves, and ultimately throughout the plant endosphere. The colonization pattern and growth promoting characteristics of bacterial endophytes in different plant species are presented in Table 1. Some bacterial endophytes also colonize flowers and seeds, and most likely get transferred vertically from the maternal endophyte community into the offspring [93,120]. Additionally, a recent study showed that endophytes could colonize corresponding seeds after the flowers were inoculated. Moreover, endophytes passed on to seeds resumed endophytic activity after the seeds were planted [93,120,121].
Because of their sessile lifestyle, plants are continuously challenged by different biotic and abiotic stresses including diseases, herbivory, heat, drought, and salinity. Endophytes likely manipulate their functional traits that allow them to interact with the host plant and respond rapidly to mitigate the consequences of adverse growth conditions [122,123]. The presence of distinct endophyte communities in different environmental conditions and different stages of the host life cycle indicates that specific functional groups of bacteria are likely to be active in response to a particular stress. In addition to vertically transmitted endophytes, “alien endophytes” (new cohorts of endophytes) accrue in the plant endosphere during plant growth. The “alien endophytes” can colonize various plant parts and incorporate new functional traits to the phytobiome through horizontal gene transfer with other microorganisms and can also eventually result in the loss of traits which may no longer be useful to the plant [124]. The hypothesized colonization cycle of bacterial endophytes in different growth stages of host plant is summarized in Figure 1.

8. Methods Used in Colonization Studies

Plating studies to determine the number of colony forming units (CFU) of endophytes within the plant in addition to microscopy based techniques used to visualize individual bacterial cells and/or microcolonies, as well as modern genomic sequencing-based approaches are all common techniques used to investigate the colonization of inoculated or indigenous bacterial endophytes in plants. They are briefly summarized here but have been extensively reviewed recently [14,18,92,100,123].

8.1. Cultivation Based Studies

In this method, selective or semi-selective culture medium is used to grow bacteria taken from plant extracts in order to determine the number of viable cells found in the plant tissue. The CFU count of bacterial endophytes from surface sterilized above ground and below ground tissues are used as an estimate of the internal populations of endophytes in the host plant [18,95,137,155]. The culturable population of bacterial endophytes can be quantified as the number of CFU per gram of root, shoot or leaf. Despite the ease and usefulness of this method, a portion of surface inhabiting epiphytes that are resistant to sterilizing agents such as ethanol or bleach can cause overestimation of endophyte counts. Additionally, this technique is only applicable to culturable bacterial endophytes. Recent studies based on genomic approaches suggest that a significant portion of bacterial communities is omitted by culture dependent approaches.

8.2. Microscopy Based Studies

Various types of microscopy such as bright-field microscopy, florescence microscopy, laser scanning confocal microscopy, and transmission electron microscopy have been commonly used to capture the colonization patterns of bacterial endophytes. The combination of microscopy with distinguishing fluorochromes or fluorescent dyes used to label or stain specific bacterial strains or bacterial communities allows the detection of endophytic colonization inside the plant tissues. FISH, GFP tagging, GUS staining, and fluorogenic dye staining are common techniques associated with microscopy to investigate the colonization of bacterial endophytes in plants [14,18,95,155]. In FISH, universal oligonucleotide probes targeting a conserved region of the 16S rRNA gene or species-specific probes are used to facilitate the observation of individual bacterial cells or microcolonies in the plant endosphere [95,99]. The use of broad host range plasmids containing constitutively expressed GUS or GFP genes are useful for tracking bacterial colonization inside the plants [63,89,104,137]. Bacterial endophytes tagged with GFP constitutively express the fluorescent proteins in situ, which allows entire bacterial cells to fluoresce in the presence of ultraviolet light or blue light, and oxygen [156,157]. In situ fluorescence of bacterial cells in plant tissue allows the localization and elucidation of the dynamics of colonization in different plant parts. The use of GFP tagged endophytes helps to assess the success of colonization, determine sites of bacterial entry, and investigate the microhabitat colonized inside the plant tissues [12]. In contrast to GUS staining, GFP is preferable for observing live cells. With GFP, plant tissues do not need to be fixed and no substrate or cofactor is necessary [158,159,160].
In many colonization studies, the combination of different techniques such as FISH, GFP labeling and GUS staining have been used [94,95,100]. By using a GFP gene fusion to a gene of interest, it is also possible to study and quantify the expression of a specific bacterial gene in planta. Egener et al. observed high levels of expression of nitrogenase in the rice root using GFP and immunogold labeling in the Kallar grass endophyte Azoarcus sp. BH72 [161]. Different microscopy based techniques can also be useful to study signaling pathways of plant endophyte interactions, mechanisms of host specificity, and, in general, the life style of endophytes within plants. Auto-fluorescence produced from the plant cell wall or organelles particularly in the leaf tissues may limit the use of these techniques but treating the specimens with low concentrations of bleaching agents may improve the image quality.

8.3. Genomics Based Studies

Recent advances in genetic tools and resources provide an important opportunity to improve our understanding of plant-endophyte interactions. Next generation sequencing technologies and bioinformatics tools allow the characterization of many endophyte communities from a variety of plant species [114,115,116,162]. Many recent studies have analyzed 16S rRNA gene sequences to study bacterial communities associated with the plant body [4,20,71,163,164]. The ubiquity of the 16S rRNA gene and its distinct evolutionary pattern allow its wide application in studying bacterial communities existing in different environments [165]. Due to the increasing accessibility of the technology, it is now becoming possible to analyze thousands of rRNA gene sequences of bacterial endophytes present in host plants. Genomics based studies have uncovered many novel bacterial communities in various plant parts. In these studies, the bacterial endophytes are described as operational taxonomic units based on sequence identity of the 16S rRNA gene or grouped into particular taxonomic units by phylogenetic analysis [9,71,74,164]. Modern techniques such as metagenomics and transcriptomics can provide information about the functional characteristics of endophyte species [166]. However, some bacterial traits are less conserved across phylogenetic lineages and differ in closely related strains of >98% identical in 16S rRNA sequence [124]. Further improvements in these techniques could possibly allow the identification of individual species or strains or a putative functional unit in a bacterial community that is critical for interaction with host plants and subsequent growth-promotion.

9. Poplar Endophytes and Their Colonization Efficiency in Crop Plants

To illustrate the methodology used in studying plant colonization by endophytes, we provide here an example of cross-species colonization of poplar tree endophytes with the monocot grass, maize. The Salicaceae (poplar and willow) endophytes have especially broad host ranges, and with the importance of the trees in environmental applications and bioenergy, and in genomics research as the first sequenced tree genome, poplar makes an excellent model system for the study of plant-microbe interactions. Poplar trees (Populus spp.) are early colonizers of nutrient poor habitats particularly wetlands, riparian areas, or other frequently disturbed areas. They can rapidly colonize open spaces made available after disturbances [167]. Because of their rapid and hardy growth, they are considered important plants for biomass production in the bioenergy industry. In addition, they provide various environmental services including conservation of soil, water, and biodiversity, and help to clean the contaminated sites by toxic chemicals [135,167,168]. Many endophyte strains are known to colonize and reside in poplar trees. The majority of the endophytic strains are members of the Alphaproteobacteria, Betaproteobacteria and Gammaproteobacteria classes but also include some yeast species. The majority of endophyte strains isolated from wild poplar in western Washington, USA, were identified as Burkholderia, Curtobacterium, Rahnella, Pseudomonas, Acinetobacter, Pantoea, Rhodotorula, and Rhizobium species [10,43,169]. Many of them can grow in N limited medium, possess a nifH gene, and are positive for the acetylene reduction assay, a common assay used to assess nitrogenase activity [10,43,57]. In addition, many of these strains produce substantial amounts of the plant growth hormone, indole-3-acetic acid [43,57]. Hacquard and Schadt recently reviewed the microbial communities of above ground and below ground tissues of Populus trees [170]. They highlighted the contribution to host plant health of microbial communities residing in the endosphere or in the phyllosphere.
Using the 15N dilution assay, it has been shown that endophytes in poplar plants contributed approximately 65% of the total N in leaves and increased plant biomass through biological N-fixation [152]. Khan et al. showed that inoculation of various crop plants with endophytes from poplar and willow trees resulted in earlier flowering and greater fruit yield in tomato and pepper, and higher biomass in maize, tomato, pepper, and squash in N limited conditions [171]. Additionally, sweet corn plants inoculated with endophytes showed increased plant biomass and improved photosynthetic capacity in leaves [19]. Furthermore, it has been shown that these endophytes colonized rice and maize plants effectively and resulted in greater biomass under nutrient limited conditions [172].
In this review, we present a novel example of a study of colonization by endophytes using a poplar endophyte. Here we provide further details on the colonization pattern of GFP-labeled strain, WP5gfp (Rahnella sp.) in two maize hybrids 29B17 and 14A91. Maize seedlings were germinated aseptically in the growth chamber after being surface sterilized. One-week-old seedlings were then inoculated by overnight co-cultivation with endophyte culture, and grown aseptically in the growth chamber in N free growth medium for 2 or 3 weeks. At the end of the experiments, inoculated seedlings were harvested, and rinsed multiple times with sterile water. Fresh root and shoot biomass were recorded and then used to determine colonization by CFU count and microscopy.
Fluorescent microscopy was used to observe the in planta population of WP5gfp in inoculated maize seedlings. Root systems including root hairs, lateral seminal roots, and leaf lamina were observed under the microscope to detect the colonization pattern of endophytes in the plant endosphere. The photographs were taken at 400 or 630 times magnification using transmission light or a GFP filter to visualize GFP fluorescence. For negative controls, mock-inoculated plant tissues were used. The endophytic population of WP5gfp was estimated in surface sterilized roots and shoots (stem and leaves) by cultivating bacterial cells in Mannitol Glutamate/Luria (MG/L) medium with 100 μg mL−1 of gentamycin and carbenicillin [173]. Dilution plates were incubated overnight at 30 °C, colonies were counted, and results were expressed as CFU per gram of plant biomass.
Multiple samples were thoroughly checked under the microscope and nearly all inoculated plants were found to be colonized by WP5gfp. WP5gfp populations were observed repeatedly in elongation and differentiation zones of lateral seminal roots. They were often observed in between cells, in the intercellular spaces of cell layers in the longitudinal direction (Figure 2 and Figure 4), and in middle lamella areas of the transverse wall between two adjacent cells (Figure 3). They extensively used intercellular spaces and cell junctures as microhabitats for colonization in both roots and leaves. Bacterial cell growth adjoined to the plant cell wall was ubiquitous in all observed samples. In leaves, colonization was not detected in the midrib area but strong colonization was observed in the intercellular spaces of mesophyll cells (Figure 5A,B), and stomatal chambers in leaves (Figure 5C,D).
WP5gfp was recovered from surface sterilized maize root, leaf and stem samples. Higher WP5gfp CFU was observed in leaves and stems in contrast to root samples (Figure 6). Average WP5gfp CFU counts were 2.9 × 107 per gram of roots, and 3.9 × 107 per gram of leaves and stems. No colonies were observed in the mock-inoculated control plants. In another study, significantly higher numbers of CFUs were also observed in shoots than roots [12]. The bigger areas of leaves and stems may allow higher numbers of endophytes to colonize compared to the roots.
Fresh root biomass as well as combined root and shoot biomass (g plant−1) were significantly higher in inoculated plants as compared to the mock control groups (p = 0.011 and p = 0.021, respectively). Root weight was 20% higher in inoculated plants, and combined root and shoot weight was 16% higher (Figure 7). WP5gfp inoculated plants had greater root bulk and bigger overall plant stature as compared to mock inoculated plants.
As reported in other colonization studies, WP5gfp can colonize crop plants such as maize and rice beyond its native host plant poplar. Bacterial endophytes can colonize a variety of plants regardless of taxonomic isolation [4,22,174]. WP5gfp colonized roots, leaves, and stems with high populations and resulted in increased plant growth as compared to mock-inoculated control plants. WP5gfp probably promptly attached to the plant surface and entered into the internal tissues as soon as they were exposed to the maize plants, and subsequently multiplied in intercellular spaces, and xylem tissues. Since colonization was widespread and resulted in positive growth response in maize seedlings, WP5 is expected to be a suitable strain to use in the production of maize with reduced addition of synthetic fertilizers. Plant growth promoting activities of other endophyte strains in the Rahnella genus have been described in many native and inoculated host plants, which supports the results presented here [18,19,175].

10. Conclusions

The focus of this review is to summarize the colonization, from recruitment, attachment, and entry to the distribution patterns of bacterial endophytes in the plant endosphere. The rhizosphere serves as a hub for plant-endophyte communication during the early stages of the colonization process and likely facilitates access to the inside of the plant tissues through openings in the plant. Some bacterial endophytes have the potential to colonize all plant parts and interact beneficially with the host plant. As an illustration of the methods used to study colonization, a specific case of this interaction is presented using Populus endophytes and the colonization of maize plants. While effective colonization and increased biomass are demonstrated, many questions remain. The early signaling mechanisms and the exchange of signaling molecules between endophyte strains and host plants, as well as the temporal and spatial dimensions of the endophytic colonization process at the molecular level, have yet to be deciphered. Further studies on the molecular and biochemical basis of plant-endophyte interactions may uncover more details about the process of bacterial endophyte colonization.


We want to express our sincere appreciation to USDA-NIFA Award # 2012-68002-19824 for funding support. We are grateful to Manindra Sthapit for his help in figure preparation. PMJ was partially supported by the Byron and Alice Lockwood Foundation.

Author Contributions

SLK and SLD conceptualized the study, and designed the experiments. SLK performed the experiments; SLK and PMJ wrote the manuscript; SLD edited the manuscript and provided intellectual advice for the research.

Conflicts of Interest

The authors declare no conflict of interest.


  1. Wilson, D. Endophyte: The evolution of a term, and clarification of its use and definition. Oikos 1995, 73, 274–276. [Google Scholar] [CrossRef]
  2. Dobereiner, J. History and new perspectives of diazotrophs in association with non-leguminous plants. Symbiosis 1992, 13, 1–13. [Google Scholar]
  3. Schulz, B.; Boyle, C. What are endophytes? In Microbial Root Endophytes; Schulz, B., Boyle, C., Sieber, T., Eds.; Springer: Berlin/Heidelberg, Germany, 2006; pp. 1–14. [Google Scholar]
  4. Hardoim, P.R.; van Overbeek, L.S.; Berg, G.; Pirttilä, A.M.; Compant, S.; Campisano, A.; Döring, M.; Sessitsch, A. The hidden world within Plants: Ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol. Mol. Biol. Rev. 2015, 79, 293–320. [Google Scholar] [CrossRef] [PubMed]
  5. Sessitsch, A.; Hardoim, P.; Döring, J.; Weilharter, A.; Krause, A.; Woyke, T.; Mitter, B.; Hauberg-Lotte, L.; Friedrich, F.; Rahalkar, M.; et al. Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenomic analysis. Mol. Plant Microbe Interact. 2012, 25, 28–36. [Google Scholar] [CrossRef] [PubMed]
  6. Taghavi, S.; Garafola, C.; Monchy, S.; Newman, L.; Hoffman, A.; Weyens, N.; Barac, T.; Vangronsveld, J.; Van Der Lelie, D. Genome survey and characterization of endophytic bacteria exhibiting a beneficial effect on growth and development of poplar trees. Appl. Environ. Microbiol. 2009, 75, 748–757. [Google Scholar] [CrossRef] [PubMed]
  7. Ikeda, S.; Okubo, T.; Anda, M.; Nakashita, H.; Yasuda, M.; Sato, S.; Kaneko, T.; Tabata, S.; Eda, S.; Momiyama, A.; et al. Community-and genome-based views of plant-associated bacteria: Plant-bacterial interactions in soybean and rice. Plant Cell Physiol. 2010, 51, 1398–1410. [Google Scholar] [CrossRef] [PubMed]
  8. Turner, T.R.; James, E.K.; Poole, P.S. The plant microbiome. Genome Biol. 2013, 14, 209. [Google Scholar] [CrossRef] [PubMed]
  9. Bulgarelli, D.; Rott, M.; Schlaeppi, K.; Ver Loren van Themaat, E.; Ahmadinejad, N.; Assenza, F.; Rauf, P.; Huettel, B.; Reinhardt, R.; Schmelzer, E.; et al. Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 2012, 488, 91–95. [Google Scholar] [CrossRef] [PubMed]
  10. Doty, S.L.; Oakley, B.; Xin, G.; Kang, J.W.; Singleton, G.; Khan, Z.; Vajzovic, A.; Staley, J.T. Diazotrophic endophytes of native black cottonwood and willow. Symbiosis 2009, 47, 23–33. [Google Scholar] [CrossRef]
  11. Wemheuer, F.; Kaiser, K.; Karlovsky, P.; Daniel, R.; Vidal, S.; Wemheuer, B. Bacterial endophyte communities of three agricultural important grass species differ in their response towards management regimes. Sci. Rep. 2017, 7, 40914. [Google Scholar] [CrossRef] [PubMed]
  12. Elbeltagy, A.; Nishioka, K.; Sato, T.; Suzuki, H.; Ye, B.; Hamada, T.; Isawa, T.; Mitsui, H. Endophytic colonization and in planta nitrogen fixation by a Herbaspirillum sp. isolated from wild rice species. Appl. Environ. Microbiol. 2001, 67, 5285–5293. [Google Scholar] [CrossRef] [PubMed]
  13. Hurek, T.; Handley, L.L.; Reinhold-Hurek, B.; Piché, Y.; De, C.; Pavillon, C.; Laval, U.; Gk-p, C. Azoarcus grass endophytes contribute fixed nitrogen to the plant in an unculturable state. Mol. Plant Microbe Interact. 2002, 15, 233–242. [Google Scholar] [CrossRef] [PubMed]
  14. Iniguez, A.L.; Dong, Y.; Triplett, E.W. Nitrogen fixation in wheat provided by Klebsiella pneumoniae 342. Mol. Plant Microbe Interact. 2004, 17, 1078–1085. [Google Scholar] [CrossRef] [PubMed]
  15. Feng, Y.; Shen, D.; Song, W. Rice endophyte Pantoea agglomerans YS19 promotes host plant growth and affects allocations of host photosynthates. J. Appl. Microbiol. 2006, 100, 938–945. [Google Scholar] [CrossRef] [PubMed]
  16. Momose, A.; Ohtake, N.; Sueyoshi, K.; Sato, T.; Nakanishi, Y.; Akao, S.; Ohyama, T. Nitrogen Fixation and Translocation in Young Sugarcane (Saccharum officinarum L.) Plants Associated with Endophytic Nitrogen-Fixing Bacteria. Microbes Environ. 2009, 24, 224–230. [Google Scholar] [CrossRef] [PubMed]
  17. Botta, A.L.; Santacecilia, A.; Ercole, C.; Cacchio, P.; Del Gallo, M. In vitro and in vivo inoculation of four endophytic bacteria on Lycopersicon esculentum. N. Biotechnol. 2013, 30, 666–674. [Google Scholar] [CrossRef] [PubMed]
  18. Kandel, S.L.; Herschberger, N.; Kim, S.H.; Doty, S.L. Diazotrophic endophytes of poplar and willow for growth promotion of rice plants in nitrogen-limited conditions. Crop Sci. 2015, 55, 1765–1772. [Google Scholar] [CrossRef]
  19. Knoth, J.L.; Kim, S.-H.; Ettl, G.J.; Doty, S.L. Effects of cross host species inoculation of nitrogen-fixing endophytes on growth and leaf physiology of maize. GCB Bioenergy 2012, 5, 408–418. [Google Scholar] [CrossRef]
  20. Gaiero, J.R.; McCall, C.A.; Thompson, K.A.; Day, N.J.; Best, A.S.; Dunfield, K.E. Inside the root microbiome: Bacterial root endophytes and plant growth promotion. Am. J. Bot. 2013, 100, 1738–1750. [Google Scholar] [CrossRef] [PubMed]
  21. Lebeis, S.L. The potential for give and take in plant-microbiome relationships. Front. Plant Sci. 2014, 5, 287. [Google Scholar] [CrossRef] [PubMed]
  22. Rosenblueth, M.; Martínez-Romero, E. Bacterial endophytes and their interactions with hosts. Mol. Plant Microbe Interact. 2006, 19, 827–837. [Google Scholar] [CrossRef] [PubMed]
  23. Bastian, F.; Cohen, A.; Piccoli, P.; Luna, V.; Baraldi, R.; Bottini, R. Production of indole-3-acetic acid and gibberellins A1 and A3 by Acetobacter diazotrophicus and Herbaspirillum seropedicae in chemically-defined culture media. Plant Growth Regul. 1998, 24, 7–11. [Google Scholar] [CrossRef]
  24. Bhattacharjee, R.B.; Singh, A.; Mukhopadhyay, S.N. Use of nitrogen-fixing bacteria as biofertiliser for non-legumes: Prospects and challenges. Appl. Microbiol. Biotechnol. 2008, 80, 199–209. [Google Scholar] [CrossRef] [PubMed]
  25. Santi, C.; Bogusz, D.; Franche, C. Biological nitrogen fixation in non-legume plants. Ann. Bot. 2013, 111, 743–767. [Google Scholar] [CrossRef] [PubMed]
  26. Gillis, M.; Kersters, K.; Hoste, B.; Janssens, D.; Kroppenstedt, R.M.; Stephan, M.P. Acetobacter diazotrophicus sp. nov., a Nitrogen-Fixing Acetic Acid Bacterium Associated with Sugarcane. Int. J. Syst. Bacteriol. 1989, 39, 361–364. [Google Scholar] [CrossRef]
  27. Dong, Z.; Canny, M.J.; McCully, M.E.; Roboredo, M.R.; Cabadilla, C.F.; Ortega, E.; Rodes, R. A Nitrogen-Fixing Endophyte of Sugarcane Stems (A New Role for the Apoplast). Plant Physiol. 1994, 105, 1139–1147. [Google Scholar] [CrossRef] [PubMed]
  28. Reinhold-Hurek, B.; Hurek, T.; Gillis, M.; Hoste, B.; Vancanneyt, M.; Kersters, K.; De Ley, J. Azoarcus gen. nov., Nitrogen-Fixing Proteobacteria Associated with Roots of Kallar Grass (Leptochloa fusca (L.) Kunth), and Description of Two Species, Azoarcus indigens sp. nov. and Azoarcus communis sp. nov. Int. J. Syst. Bacteriol. 1993, 43, 574–584. [Google Scholar] [CrossRef]
  29. Riggs, P.J.; Chelius, M.K.; Iniguez, A.L.; Kaeppler, S.M.; Triplett, E.W. Enhanced maize productivity by inoculation with diazotrophic bacteria. Aust. J. Plant Physiol. 2001, 28, 829–836. [Google Scholar]
  30. Olivares, J.; Bedmar, E.J.; Sanjuán, J. Biological nitrogen fixation in the context of global change. Mol. Plant Microbe Interact. 2013, 26, 486–494. [Google Scholar] [CrossRef] [PubMed]
  31. Reinhold-Hurek, B.; Hurek, T. Life in grasses: Diazotrophic endophytes. Trends Microbiol. 1998, 6, 139–144. [Google Scholar] [CrossRef]
  32. Doty, S.L.; Sher, A.W.; Fleck, N.D.; Khorasani, M.; Bumgarner, R.E.; Khan, Z.; Ko, A.W.K.; Kim, S.-H.; DeLuca, T.H. Variable Nitrogen Fixation in Wild Populus. PLoS ONE 2016, 11, e0155979. [Google Scholar] [CrossRef] [PubMed]
  33. Doty, S.L. Endophytic N-Fixation: Controversy and a Path Forward. In Functional Importance of the Plant Microbiome; Doty, S.L., Ed.; Springer International Publishing: New York, NY, USA, 2017; pp. 17–58. [Google Scholar]
  34. Erisman, J.W.; Sutton, M.A.; Galloway, J.; Klimont, Z.; Winiwarter, W. How a century of ammonia synthesis changed the world. Nat. Geosci. 2008, 1, 636–639. [Google Scholar] [CrossRef]
  35. Howarth, R.W. Coastal nitrogen pollution: A review of sources and trends globally and regionally. Harmful Algae 2008, 8, 14–20. [Google Scholar] [CrossRef]
  36. Reay, D.S.; Davidson, E.A.; Smith, K.A.; Smith, P.; Melillo, J.M.; Dentener, F.; Crutzen, P.J. Global agriculture and nitrous oxide emissions. Nat. Clim. Chang. 2012, 2, 410–416. [Google Scholar] [CrossRef]
  37. Robarge, W.P.; Walker, J.T.; McCulloch, R.B.; Murray, G. Atmospheric concentrations of ammonia and ammonium at an agricultural site in the southeast United States. Atmos. Environ. 2002, 36, 1661–1674. [Google Scholar] [CrossRef]
  38. Driscoll, C.T.; Whitall, D.; Aber, J.; Boyer, E.; Castro, M.; Cronan, C.; Goodale, C.L.; Groffman, P.; Hopkinson, C.; Lambert, K.; et al. Nitrogen Pollution in the Northeastern United States: Sources, Effects, and Management Options. Bioscience 2003, 53, 357. [Google Scholar] [CrossRef]
  39. Santoyo, G.; Moreno-Hagelsieb, G.; del Carmen Orozco-Mosqueda, M.; Glick, B.R. Plant growth-promoting bacterial endophytes. Microbiol. Res. 2016, 183, 92–99. [Google Scholar] [CrossRef] [PubMed]
  40. Spaepen, S.; Vanderleyden, J. Auxin and plant-microbe interactions. Cold Spring Harb. Perspect. Biol. 2011, 3, 1–13. [Google Scholar] [CrossRef] [PubMed]
  41. Gamalero, E.; Glick, B.R. Mechanisms used by plant growth-promoting bacteria. In Bacteria in Agrobiology: Plant Nutrient Management; Maheshwari, D.K.K., Ed.; Springer: Berlin/Heidelberg, Germany, 2011; pp. 17–47. ISBN 978-3-642-21060-0. [Google Scholar]
  42. Shi, Y.; Lou, K.; Li, C. Promotion of plant growth by phytohormone-producing endophytic microbes of sugar beet. Biol. Fertil. Soils 2009, 45, 645–653. [Google Scholar] [CrossRef]
  43. Xin, G.; Zhang, G.; Kang, J.W.; Staley, J.T.; Doty, S.L. A diazotrophic, indole-3-acetic acid-producing endophyte from wild cottonwood. Biol. Fertil. Soils 2009, 45, 669–674. [Google Scholar] [CrossRef]
  44. Barra, P.J.; Inostroza, N.G.; Acuña, J.J.; Mora, M.L.; Crowley, D.E.; Jorquera, M.A. Formulation of bacterial consortia from avocado (Persea americana Mill.) and their effect on growth, biomass and superoxide dismutase activity of wheat seedlings under salt stress. Appl. Soil Ecol. 2016, 102, 80–91. [Google Scholar] [CrossRef]
  45. Khan, Z.; Rho, H.; Firrincieli, A.; Hung, S.H.; Luna, V.; Masciarelli, O.; Kim, S.H.; Doty, S.L. Growth enhancement and drought tolerance of hybrid poplar upon inoculation with endophyte consortia. Curr. Plant Biol. 2016, 6, 38–47. [Google Scholar] [CrossRef]
  46. Ahmed, E.; Holmström, S.J.M. Siderophores in environmental research: Roles and applications. Microb. Biotechnol. 2014, 7, 196–208. [Google Scholar] [CrossRef] [PubMed]
  47. Dias, A.C.F.; Costa, F.E.C.; Andreote, F.D.; Lacava, P.T.; Teixeira, M.A.; Assumpção, L.C.; Araújo, W.L.; Azevedo, J.L.; et al. Isolation of micropropagated strawberry endophytic bacteria and assessment of their potential for plant growth promotion. World J. Microbiol. Biotechnol. 2009, 25, 189–195. [Google Scholar] [CrossRef]
  48. Oteino, N.; Lally, R.D.; Kiwanuka, S.; Lloyd, A.; Ryan, D.; Germaine, K.J.; Dowling, D.N. Plant growth promotion induced by phosphate solubilizing endophytic Pseudomonas isolates. Front. Microbiol. 2015, 6, 1–9. [Google Scholar] [CrossRef] [PubMed]
  49. Passari, A.K.; Mishra, V.K.; Gupta, V.K.; Yadav, M.K.; Saikia, R.; Singh, B.P. In Vitro and In Vivo Plant Growth Promoting Activities and DNA Fingerprinting of Antagonistic Endophytic Actinomycetes Associates with Medicinal Plants. PLoS ONE 2015, 10, e0139468. [Google Scholar] [CrossRef] [PubMed]
  50. Joe, M.M.; Devaraj, S.; Benson, A.; Sa, T. Isolation of phosphate solubilizing endophytic bacteria from Phyllanthus amarus Schum & Thonn: Evaluation of plant growth promotion and antioxidant activity under salt stress. J. Appl. Res. Med. Aromat. Plants 2016. [Google Scholar] [CrossRef]
  51. Khan, M.S.; Zaidi, A.; Ahmad, E. Mechanism of phosphate solubilization and physiological functions of phosphate-solubilizing microorganisms. In Phosphate Solubilizing Microorganisms: Principles and Applications of Microphos Technology; Khan, M.S., Zaidi, A., Musarrat, J., Eds.; Springer International Publishing: Cham, Switzerland, 2014; Volume 108, ISBN 978-3-319-08215-8. [Google Scholar]
  52. Friesen, M.L.; Porter, S.S.; Stark, S.C.; Von Wettberg, E.J.; Sachs, J.L. Microbially Mediated Plant Functional Traits-2011.pdf. Annu. Rev. Ecol. Evol. Syst. 2011, 42, 23–46. [Google Scholar] [CrossRef]
  53. Mercado-Blanco, J.; Lugtenberg, B. Biotechnological Applications of Bacterial Endophytes. Curr. Biotechnol. 2014, 3, 60–75. [Google Scholar] [CrossRef]
  54. Glick, B.R. Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol. Res. 2014, 169, 30–39. [Google Scholar] [CrossRef] [PubMed]
  55. Esmaeel, Q.; Pupin, M.; Kieu, N.P.; Chataigné, G.; Béchet, M.; Deravel, J.; Krier, F.; Höfte, M.; Jacques, P.; Leclère, V. Burkholderia genome mining for nonribosomal peptide synthetases reveals a great potential for novel siderophores and lipopeptides synthesis. Microbiologyopen 2016, 1–15. [Google Scholar]
  56. Larran, S.; Simon, M.R.; Moreno, M.V.; Siurana, M.P.S.; Perell, A. Endophytes from wheat as biocontrol agents against tan spot disease. Biol. Control 2016, 92, 17–23. [Google Scholar] [CrossRef]
  57. Kandel, S.L.; Firrincieli, A.; Joubert, P.M.; Okubara, P.A.; Leston, N.D.; McGeorge, K.M.; Mugnozza, G.S.; Harfouche, A.; Kim, S.H.; Doty, S.L. An in vitro study of bio-control and plant growth promotion potential of salicaceae endophytes. Front. Microbiol. 2017, 8, 1–16. [Google Scholar] [CrossRef] [PubMed]
  58. Rojas-Tapias, D.; Moreno-Galvan, A.; Pardo-Diaz, S.; Obando, M.; Rivera, D.; Bonilla, R. Effect of inoculation with plant growth-promoting bacteria (PGPB) on amelioration of saline stress in maize (Zea mays). Appl. Soil Ecol. 2012, 61, 264–272. [Google Scholar] [CrossRef]
  59. Ali, S.; Charles, T.C.; Glick, B.R. Amelioration of high salinity stress damage by plant growth-promoting bacterial endophytes that contain ACC deaminase. Plant Physiol. Biochem. 2014, 80, 160–167. [Google Scholar] [CrossRef] [PubMed]
  60. Naveed, M.; Mitter, B.; Reichenauer, T.G.; Wieczorek, K.; Sessitsch, A. Increased drought stress resilience of maize through endophytic colonization by Burkholderia phytofirmans PsJN and Enterobacter sp. FD17. Environ. Exp. Bot. 2014, 97, 30–39. [Google Scholar] [CrossRef]
  61. Qin, S.; Zhang, Y.J.; Yuan, B.; Xu, P.Y.; Xing, K.; Wang, J.; Jiang, J.H. Isolation of ACC deaminase-producing habitat-adapted symbiotic bacteria associated with halophyte Limonium sinense (Girard) Kuntze and evaluating their plant growth-promoting activity under salt stress. Plant Soil 2014, 374, 753–766. [Google Scholar] [CrossRef]
  62. Yaish, M.W.; Antony, I.; Glick, B.R. Isolation and characterization of endophytic plant growth-promoting bacteria from date palm tree (Phoenix dactylifera L.) and their potential role in salinity tolerance. Antonie Van Leeuwenhoek 2015, 107, 1519–1532. [Google Scholar] [CrossRef] [PubMed]
  63. Senga, R.-A.; Alegria Terrazas, S.; Balbirnie, K.; Blank, M.; Janiak, A.; Szarejko, I.; Chmielewska, B.; Karcz, J.; Morris, J.; Hedley, P.E.; et al. Root Hair Mutations Displace the Barley Rhizosphere Microbiota. Front. Plant Sci. 2017, 8, 1–15. [Google Scholar]
  64. Kawasaki, A.; Donn, S.; Ryan, P.R.; Mathesius, U.; Devilla, R.; Jones, A.; Watt, M. Microbiome and exudates of the root and rhizosphere of brachypodium distachyon, a model for wheat. PLoS ONE 2016, 11, e0164533. [Google Scholar] [CrossRef] [PubMed]
  65. Pétriacq, P.; Williams, A.; Cotton, A.; McFarlane, A.E.; Rolfe, S.A.; Ton, J. Metabolite profiling of non-sterile rhizosphere soil. Plant J. 2017, 1–16. [Google Scholar] [CrossRef] [PubMed]
  66. Kost, T.; Stopnisek, N.; Agnoli, K.; Eberl, L.; Weisskopf, L. Oxalotrophy, a widespread trait of plant-associated Burkholderia species, is involved in successful root colonization of lupin and maize by Burkholderia phytofirmans. Front. Microbiol. 2014, 4, 1–9. [Google Scholar] [CrossRef] [PubMed][Green Version]
  67. Zúñiga, A.; Poupin, M.J.; Donoso, R.; Ledger, T.; Guiliani, N.; Gutiérrez, R.A.; González, B. Quorum sensing and indole-3-acetic acid degradation play a role in colonization and plant growth promotion of Arabidopsis thaliana by Burkholderia phytofirmans PsJN. Mol. Plant Microbe Interact. 2013, 26, 546–553. [Google Scholar] [CrossRef] [PubMed]
  68. Schikora, A.; Schenk, S.T.; Hartmann, A. Beneficial effects of bacteria-plant communication based on quorum sensing molecules of the N-acyl homoserine lactone group. Plant Mol. Biol. 2016, 90, 605–612. [Google Scholar] [CrossRef] [PubMed]
  69. Schaefer, A.L.; Lappala, C.R.; Morlen, R.P.; Pelletier, D.A.; Lu, T.Y.S.; Lankford, P.K.; Harwood, C.S.; Greenberg, E.P. LuxR- and luxI-type quorum-sensing circuits are prevalent in members of the populus deltoides microbiome. Appl. Environ. Microbiol. 2013, 79, 5745–5752. [Google Scholar] [CrossRef] [PubMed]
  70. Hartmann, A.; Rothballer, M.; Hense, B.A.; SchrÃder, P. Bacterial quorum sensing compounds are important modulators of microbe-plant interactions. Front. Plant Sci. 2014, 5, 1–4. [Google Scholar] [CrossRef] [PubMed]
  71. Wagner, M.R.; Lundberg, D.S.; del Rio, T.G.; Tringe, S.G.; Dangl, J.L.; Mitchell-Olds, T. Host genotype and age shape the leaf and root microbiomes of a wild perennial plant. Nat. Commun. 2016, 7, 12151. [Google Scholar] [CrossRef] [PubMed]
  72. Tan, Z.; Hurek, T.; Reinhold-Hurek, B. Effect of N-fertilization, plant genotype and environmental conditions on nifH gene pools in roots of rice. Environ. Microbiol. 2003, 5, 1009–1015. [Google Scholar] [CrossRef] [PubMed]
  73. Rodríguez-Blanco, A.; Sicardi, M.; Frioni, L. Plant genotype and nitrogen fertilization effects on abundance and diversity of diazotrophic bacteria associated with maize (Zea mays L.). Biol. Fertil. Soils 2015, 51, 391–402. [Google Scholar] [CrossRef]
  74. Lundberg, D.S.; Lebeis, S.L.; Paredes, S.H.; Yourstone, S.; Gehring, J.; Malfatti, S.; Tremblay, J.; Engelbrektson, A.; Kunin, V.; del Rio, T.G.; et al. Defining the core Arabidopsis thaliana root microbiome. Nature 2012, 488, 86–90. [Google Scholar] [CrossRef] [PubMed]
  75. Meneses, C.H.S.G.; Rouws, L.F.M.; Simoes-Araujo, J.L.; Vidal, M.S.; Baldani, J.I. Exopolysaccharide production is required for biofilm formation and plant colonization by the nitrogen-fixing endophyte Gluconacetobacter diazotrophicus. Mol. Plant Microbe Interact. 2011, 24, 1448–1458. [Google Scholar] [CrossRef] [PubMed]
  76. Meneses, C.; Gonçalves, T.; Alquéres, S.; Rouws, L.; Serrato, R.; Vidal, M.; Baldani, J.I. Gluconacetobacter diazotrophicus exopolysaccharide protects bacterial cells against oxidative stress in vitro and during rice plant colonization. Plant Soil 2017, 416, 133–147. [Google Scholar] [CrossRef]
  77. Balsanelli, E.; De Baura, V.A.; De Oliveira Pedrosa, F.; De Souza, E.M.; Monteiro, R.A. Exopolysaccharide biosynthesis enables mature biofilm formation on abiotic surfaces by Herbaspirillum seropedicae. PLoS ONE 2014, 9. [Google Scholar] [CrossRef] [PubMed]
  78. Liu, J.; Wang, X.; Pu, H.; Liu, S.; Kan, J.; Jin, C. Recent advances in endophytic exopolysaccharides: Production, structural characterization, physiological role and biological activity. Carbohydr. Polym. 2017, 157, 1113–1124. [Google Scholar] [CrossRef] [PubMed]
  79. Balsanelli, E.; Serrato, R.V.; de Baura, V.A.; Sassaki, G.; Yates, M.G.; Rigo, L.U.; Pedrosa, F.O.; de Souza, E.M.; Monteiro, R.A. Herbaspirillum seropedicae rfbB and rfbC genes are required for maize colonization. Environ. Microbiol. 2010, 12, 2233–2244. [Google Scholar] [PubMed]
  80. Balsanelli, E.; Tuleski, T.R.; de Baura, V.A.; Yates, M.G.; Chubatsu, L.S.; de Oliveira Pedrosa, F.; de Souza, E.M.; Monteiro, R.A. Maize Root Lectins Mediate the Interaction with Herbaspirillum seropedicae via N-Acetyl Glucosamine Residues of Lipopolysaccharides. PLoS ONE 2013, 8. [Google Scholar] [CrossRef] [PubMed]
  81. Compant, S.; Reiter, B.; Nowak, J.; Sessitsch, A.; Clément, C.; Barka, E.A. Endophytic Colonization of Vitis vinifera L. by Plant Growth- Promoting Bacterium Burkholderia sp. Strain PsJN. Appl. Environ. Microbiol. 2005, 71, 1685–1693. [Google Scholar] [CrossRef] [PubMed]
  82. Vargas, L.; de Carvalho, T.L.G.; Ferreira, P.C.G.; Baldani, V.L.D.; Baldani, J.I.; Hemerly, A.S. Early responses of rice (Oryza sativa L.) seedlings to inoculation with beneficial diazotrophic bacteria are dependent on plant and bacterial genotypes. Plant Soil 2012, 356, 127–137. [Google Scholar] [CrossRef]
  83. Rangjaroen, C.; Sungthong, R.; Rerkasem, B.; Teaumroong, N.; Noisangiam, R.; Lumyong, S. Untapped Endophytic Colonization and Plant Growth-Promoting Potential of the Genus Novosphingobium to Optimize Rice Cultivation. Microbes Environ. 2017, 32, 84–87. [Google Scholar] [CrossRef] [PubMed]
  84. Romanstchuk, M. Plant pathogenic bacteria attach to surface. Annu. Rev. Phytopathol 1992, 30, 225–243. [Google Scholar] [CrossRef] [PubMed]
  85. Rodríguez-Navarro, D.N.; Dardanelli, M.S.; Ruíz-Saínz, J.E. Attachment of bacteria to the roots of higher plants. FEMS Microbiol. Lett. 2007, 272, 127–136. [Google Scholar] [CrossRef] [PubMed]
  86. Matthysse, A.G. Attachment of Agrobacterium to plant surfaces. Front. Plant Sci. 2014, 5, 1–8. [Google Scholar] [CrossRef] [PubMed]
  87. Pankievicz, V.C.S.; Camilios-Neto, D.; Bonato, P.; Balsanelli, E.; Tadra-Sfeir, M.Z.; Faoro, H.; Chubatsu, L.S.; Donatti, L.; Wajnberg, G.; Passetti, F.; et al. RNA-seq transcriptional profiling of Herbaspirillum seropedicae colonizing wheat (Triticum aestivum) roots. Plant Mol. Biol. 2016, 90, 589–603. [Google Scholar] [CrossRef] [PubMed]
  88. Reinhold-Hurek, B.; Maes, T.; Gemmer, S.; Van Montagu, M.; Hurek, T. An endoglucanase is involved in infection of rice roots by the not-cellulose-metabolizing endophyte Azoarcus sp. strain BH72. Mol. Plant Microbe Interact. 2006, 19, 181–188. [Google Scholar] [CrossRef] [PubMed]
  89. Naveed, M.; Mitter, B.; Yousaf, S.; Pastar, M.; Afzal, M.; Sessitsch, A. The endophyte Enterobacter sp. FD17: A maize growth enhancer selected based on rigorous testing of plant beneficial traits and colonization characteristics. Biol. Fertil. Soils 2014, 50, 249–262. [Google Scholar] [CrossRef]
  90. Prieto, P.; Schilirò, E.; Maldonado-González, M.M.; Valderrama, R.; Barroso-Albarracín, J.B.; Mercado-Blanco, J. Root hairs play a key role in the endophytic colonization of olive roots by Pseudomonas spp. with biocontrol activity. Microb. Ecol. 2011, 62, 435–445. [Google Scholar] [CrossRef] [PubMed][Green Version]
  91. Rangel de Souza, A.L.S.; De Souza, S.A.; De Oliveira, M.V.V.; Ferraz, T.M.; Figueiredo, F.A.M.M.A.; Da Silva, N.D.; Rangel, P.L.; Panisset, C.R.S.; Olivares, F.L.; Campostrini, E.; et al. Endophytic colonization of Arabidopsis thaliana by Gluconacetobacter diazotrophicus and its effect on plant growth promotion, plant physiology, and activation of plant defense. Plant Soil 2016, 399, 257–270. [Google Scholar] [CrossRef]
  92. Germaine, K.; Keogh, E.; Garcia-Cabellos, G.; Borremans, B.; Lelie, D.; Barac, T.; Oeyen, L.; Vangronsveld, J.; Moore, F.P.; Moore, E.R.B.; et al. Colonisation of poplar trees by gfp expressing bacterial endophytes. FEMS Microbiol. Ecol. 2004, 48, 109–118. [Google Scholar] [CrossRef] [PubMed]
  93. Mitter, B.; Pfaffenbichler, N.; Flavell, R.; Compant, S.; Antonielli, L.; Petric, A.; Berninger, T.; Naveed, M.; Sheibani-Tezerji, R.; von Maltzahn, G.; et al. A new approach to modify plant microbiomes and traits by introducing beneficial bacteria at flowering into progeny seeds. Front. Microbiol. 2017, 8, 1–10. [Google Scholar] [CrossRef] [PubMed]
  94. Glassner, H.; Zchori-Fein, E.; Yaron, S.; Sessitsch, A.; Sauer, U.; Compant, S. Bacterial niches inside seeds of Cucumis melo L. Plant Soil 2017. [Google Scholar] [CrossRef]
  95. Castanheira, N.L.; Dourado, A.C.; Pais, I.; Semedo, J.; Scotti-Campos, P.; Borges, N.; Carvalho, G.; Barreto Crespo, M.T.; Fareleira, P. Colonization and beneficial effects on annual ryegrass by mixed inoculation with plant growth promoting bacteria. Microbiol. Res. 2017, 198, 47–55. [Google Scholar] [CrossRef] [PubMed]
  96. Fisher, P.J.; Petrini, O.; Lappin Scott, H.M. The distribution of some fungal and bacterial endophytes in maize (Zea mays L.). New Phytol. 1992, 122, 299–305. [Google Scholar] [CrossRef]
  97. Wei, C.-Y.; Lin, L.; Luo, L.-J.; Xing, Y.-X.; Hu, C.-J.; Yang, L.-T.; Li, Y.-R.; An, Q. Endophytic nitrogen-fixing Klebsiella variicola strain DX120E promotes sugarcane growth. Biol. Fertil. Soils 2013, 50, 657–666. [Google Scholar] [CrossRef]
  98. Gyaneshwar, P.; James, E.K.; Mathan, N.; Reddy, P.M.; Reinhold-hurek, B.; Jagdish, K. Endophytic Colonization of Rice by a Diazotrophic Strain of Serratia marcescens. J. Bacteriol. 2001, 183, 2634–2645. [Google Scholar] [CrossRef] [PubMed]
  99. James, E.K.; Gyaneshwar, P.; Mathan, N.; Barraquio, W.L.; Reddy, P.M.; Iannetta, P.P.M.; Olivares, F.L.; Ladha, J.K. Infection and colonization of rice seedlings by the plant growth-promoting bacterium Herbaspirillum seropedicae Z67. Mol. Plant Microbe Interact. 2002, 15, 894–906. [Google Scholar] [CrossRef] [PubMed]
  100. Lo Piccolo, S.; Ferraro, V.; Alfonzo, A.; Settanni, L.; Ercolini, D.; Burruano, S.; Moschetti, G. Presence of endophytic bacteria in Vitis vinifera leaves as detected by fluorescence in situ hybridization. Ann. Microbiol. 2010, 60, 161–167. [Google Scholar] [CrossRef]
  101. Frank, A.; Saldierna Guzmán, J.; Shay, J. Transmission of Bacterial Endophytes. Microorganisms 2017, 5, 70. [Google Scholar] [CrossRef] [PubMed]
  102. Thomas, P.; Reddy, K.M. Microscopic elucidation of abundant endophytic bacteria colonizing the cell wall-plasma membrane peri-space in the shoot-tip tissue of banana. AoB Plants 2013, 5, 1–12. [Google Scholar] [CrossRef]
  103. Pirttilä, A.M.; Laukkanen, H.; Pospiech, H. Detection of Intracellular Bacteria in the Buds of Scotch Pine (Pinus sylvestris L.) by In Situ Hybridization Detection of Intracellular Bacteria in the Buds of Scotch Pine (Pinus sylvestris L.) by In Situ Hybridization. Appl. Environ. Microbiol. 2000, 66, 3073–3077. [Google Scholar] [CrossRef] [PubMed]
  104. White, J.F.; Torres, M.S.; Somu, M.P.; Johnson, H.; Irizarry, I.; Chen, Q.; Zhang, N.; Walsh, E.; Tadych, M.; Bergen, M. Hydrogen peroxide staining to visualize intracellular bacterial infections of seedling root cells. Microsc. Res. Tech. 2014, 77, 566–573. [Google Scholar] [CrossRef] [PubMed]
  105. De Almeida, C.V.; Andreote, F.D.; Yara, R.; Tanaka, F.A.O.; Azevedo, J.L.; de Almeida, M. Bacteriosomes in axenic plants: Endophytes as stable endosymbionts. World J. Microbiol. Biotechnol. 2009, 25, 1757–1764. [Google Scholar] [CrossRef]
  106. Perrine-Walker, F.M.; Prayitno, J.; Rolfe, B.G.; Weinman, J.J.; Hocart, C.H. Infection process and the interaction of rice roots with rhizobia. J. Exp. Bot. 2007, 58, 3343–3350. [Google Scholar] [CrossRef] [PubMed]
  107. Paungfoo-Lonhienne, C.; Rentsch, D.; Robatzek, S.; Webb, R.I.; Sagulenko, E.; Näsholm, T.; Schmidt, S.; Lonhienne, T.G.A. Turning the table: Plants consume microbes as a source of nutrients. PLoS ONE 2010, 5, e11915. [Google Scholar] [CrossRef] [PubMed][Green Version]
  108. Paungfoo-lonhienne, C.; Schmidt, S.; Webb, R.I.; Interactions, P.M. Rhizophagy—A new dimension of plant—Microbe interactions. In Molecular Microbial Ecology of the Rhizosphere; de Bruijn, F.J., Ed.; Wiley-Blackwell: Hoboken, NJ, USA, 2013; Volume 2, pp. 1201–1207. [Google Scholar]
  109. Choudhury, F.K.; Rivero, R.M.; Blumwald, E.; Mittler, R. Reactive Oxygen species, abiotic stress and stress combination. Plant J. 2017, 90, 856–867. [Google Scholar] [CrossRef] [PubMed]
  110. Baker, C.J.; Orlandi, E.W. Active oxygen in plant pathogenesis. Annu. Rev. Phytopathol. 1993, 33, 299–321. [Google Scholar] [CrossRef] [PubMed]
  111. Chen, Z.; Silva, H.; Klessig, D.F. Active Oxygen Species in the Induction of Plant Systemic Acquired Resistance by Salicylic Acid. Science 1993, 262, 1883–1886. [Google Scholar] [CrossRef] [PubMed]
  112. Mehdy, M.C. Active Oxygen Species in Plant Defense against Pathogens. Plant Physiol. 1994, 105, 467–472. [Google Scholar] [CrossRef] [PubMed]
  113. Alquéres, S.; Meneses, C.; Rouws, L.; Rothballer, M.; Baldani, I.; Schmid, M.; Hartmann, A. The bacterial superoxide dismutase and glutathione reductase are crucial for endophytic colonization of rice roots by Gluconacetobacter diazotrophicus PAL5. Mol. Plant Microbe Interact. 2013, 26, 937–945. [Google Scholar] [CrossRef] [PubMed]
  114. Krause, A.; Ramakumar, A.; Bartels, D.; Battistoni, F.; Bekel, T.; Boch, J.; Böhm, M.; Friedrich, F.; Hurek, T.; Krause, L.; et al. Complete genome of the mutualistic, N2-fixing grass endophyte Azoarcus sp. strain BH72. Nat. Biotechnol. 2006, 24, 1385–1391. [Google Scholar] [CrossRef] [PubMed]
  115. Taghavi, S.; van der Lelie, D. Genome Sequence of the Plant Growth-Promoting Endophytic Bacterium Enterobacter sp. 638. Mol. Microb. Ecol. Rhizosph. 2013, 2, 899–908. [Google Scholar] [CrossRef] [PubMed]
  116. Mitter, B.; Petric, A.; Shin, M.W.; Chain, P.S.G.; Hauberg-Lotte, L.; Reinhold-Hurek, B.; Nowak, J.; Sessitsch, A. Comparative genome analysis of Burkholderia phytofirmans PsJN reveals a wide spectrum of endophytic lifestyles based on interaction strategies with host plants. Front. Plant Sci. 2013, 4, 1–15. [Google Scholar] [CrossRef] [PubMed]
  117. Ali, S.; Duan, J.; Charles, T.C.; Glick, B.R. A bioinformatics approach to the determination of genes involved in endophytic behavior in Burkholderia spp. J. Theor. Biol. 2014, 343, 193–198. [Google Scholar] [CrossRef] [PubMed]
  118. Nelson, E.B. The seed microbiome: Origins, interactions, and impacts. Plant Soil 2017, 1–28. [Google Scholar] [CrossRef]
  119. Shade, A.; Jacques, M.A.; Barret, M. Ecological patterns of seed microbiome diversity, transmission, and assembly. Curr. Opin. Microbiol. 2017, 37, 15–22. [Google Scholar] [CrossRef] [PubMed]
  120. Truyens, S.; Weyens, N.; Cuypers, A.; Vangronsveld, J. Bacterial seed endophytes: Genera, vertical transmission and interaction with plants. Environ. Microbiol. Rep. 2015, 7, 40–50. [Google Scholar] [CrossRef]
  121. Johnston-Monje, D.; Raizada, M.N. Conservation and diversity of seed associated endophytes in Zea across boundaries of evolution, ethnography and ecology. PLoS ONE 2011, 6. [Google Scholar] [CrossRef] [PubMed]
  122. Doty, S.L. Functional Importance of the Plant Endophytic Microbiome: Implications for Agriculture, Forestry, and Bioenergy. In Functional Importance of the Plant Microbiome; Doty, S.L., Ed.; Springer International Publishing: New York, NY, USA, 2017; pp. 1–5. [Google Scholar]
  123. Compant, S.; Clément, C.; Sessitsch, A. Plant growth-promoting bacteria in the rhizo- and endosphere of plants: Their role, colonization, mechanisms involved and prospects for utilization. Soil Biol. Biochem. 2010, 42, 669–678. [Google Scholar] [CrossRef][Green Version]
  124. Martiny, J.B.H.; Jones, S.E.; Lennon, J.T.; Martiny, A.C. Microbiomes in light of traits: A phylogenetic perspective. Science 2015, 350, aac9323. [Google Scholar] [CrossRef] [PubMed]
  125. Patel, J.K.; Archana, G. Diverse culturable diazotrophic endophytic bacteria from Poaceae plants show cross-colonization and plant growth promotion in wheat. Plant Soil 2017, 417, 99–116. [Google Scholar] [CrossRef]
  126. Hurek, T.; Reinhold-Hurek, B.; Van Montagu, M.; Kellenberger, E. Root colonization and systemic spreading of Azoarcus sp. strain BH72 in grasses. J. Bacteriol. 1994, 176, 1913–1923. [Google Scholar] [CrossRef] [PubMed]
  127. Liu, X.; Zhao, H.; Chen, S. Colonization of maize and rice plants by strain Bacillus megaterium C4. Curr. Microbiol. 2006, 52, 186–190. [Google Scholar] [CrossRef] [PubMed]
  128. Bacilio-Jiménez, M.; Aguilar-Flores, S.; Del Valle, M.V.; Pérez, A.; Zepeda, A.; Zenteno, E. Endophytic bacteria in rice seeds inhibit early colonization of roots by Azospirillum brasilense. Soil Biol. Biochem. 2001, 33, 167–172. [Google Scholar] [CrossRef]
  129. Tian, B.; Zhang, C.; Ye, Y.; Wen, J.; Wu, Y.; Wang, H.; Li, H.; Cai, S.; Cai, W.; Cheng, Z.; et al. Beneficial traits of bacterial endophytes belonging to the core communities of the tomato root microbiome. Agric. Ecosyst. Environ. 2017, 247, 149–156. [Google Scholar] [CrossRef]
  130. Ji, X.; Lu, G.; Gai, Y.; Zheng, C.; Mu, Z. Biological control against bacterial wilt and colonization of mulberry by an endophytic Bacillus subtilis strain. FEMS Microbiol. Ecol. 2008, 65, 565–573. [Google Scholar] [CrossRef] [PubMed]
  131. Compant, S.; Kaplan, H.; Sessitsch, A.; Nowak, J.; Ait Barka, E.; Clement, C. Endophytic colonization of Vitis vinifera L. by Burkholderia phytofirmans strain PsJN: From the rhizosphere to inflorescence tissues. FEMS Microbiol. Ecol. 2008, 63, 84–93. [Google Scholar] [CrossRef] [PubMed]
  132. Kim, S.; Lowman, S.; Hou, G.; Nowak, J.; Flinn, B.; Mei, C. Growth promotion and colonization of switchgrass (Panicum virgatum) cv. Alamo by bacterial endophyte Burkholderia phytofirmans strain PsJN. Biotechnol. Biofuels 2012, 5, 37. [Google Scholar] [CrossRef] [PubMed]
  133. Govindarajan, M.; Balandreau, J.; Kwon, S.W.; Weon, H.Y.; Lakshminarasimhan, C. Effects of the inoculation of Burkholderia vietnamensis and related endophytic diazotrophic bacteria on grain yield of rice. Microb. Ecol. 2008, 55, 21–37. [Google Scholar] [CrossRef] [PubMed]
  134. Govindarajan, M.; Balandreau, J.; Muthukumarasamy, R.; Revathi, G.; Lakshminarasimhan, C. Improved yield of micropropagated sugarcane following inoculation by endophytic Burkholderia vietnamiensis. Plant Soil 2006, 280, 239–252. [Google Scholar] [CrossRef]
  135. Doty, S.L.; Freeman, J.L.; Cohu, C.M.; Burken, J.G.; Firrincieli, A.; Simon, A.; Khan, Z.; Isebrands, J.G.; Lukas, J.; Blaylock, M.J. Enhanced Degradation of TCE on a Superfund Site Using Endophyte-Assisted Poplar Tree Phytoremediation. Environ. Sci. Technol. 2017, 51, 10050–10058. [Google Scholar] [CrossRef] [PubMed]
  136. Luna, M.F.; Galar, M.L.; Aprea, J.; Molinari, M.L.; Boiardi, J.L. Colonization of sorghum and wheat by seed inoculation with Gluconacetobacter diazotrophicus. Biotechnol. Lett. 2010, 32, 1071–1076. [Google Scholar] [CrossRef] [PubMed]
  137. Rouws, L.F.M.; Meneses, C.H.S.G.; Guedes, H.V.; Vidal, M.S.; Baldani, J.I.; Schwab, S. Monitoring the colonization of sugarcane and rice plants by the endophytic diazotrophic bacterium Gluconacetobacter diazotrophicus marked with gfp and gusA reporter genes. Lett. Appl. Microbiol. 2010, 51, 325–330. [Google Scholar] [CrossRef] [PubMed]
  138. Amaral, F.P.; Bueno, J.C.F.; Hermes, V.S.; Arisi, A.C.M. Gene expression analysis of maize seedlings (DKB240 variety) inoculated with plant growth promoting bacterium Herbaspirillum seropedicae. Symbiosis 2014, 62, 41–50. [Google Scholar] [CrossRef]
  139. Roncato-Maccari, L.D.B.; Ramos, H.J.O.; Pedrosa, F.O.; Alquini, Y.; Chubatsu, L.S.; Yates, M.G.; Rigo, L.U.; Steffens, M.B.R.; Souza, E.M. Endophytic Herbaspirillum seropedicae expresses nif genes in gramineous plants. FEMS Microbiol. Ecol. 2003, 45, 39–47. [Google Scholar] [CrossRef]
  140. Brusamarello-Santos, L.C.; Gilard, F.; Brulé, L.; Quilleré, I.; Gourion, B.; Ratet, P.; De Souza, E.M.; Lea, P.J.; Hirel, B. Metabolic profiling of two maize (Zea mays L.) inbred lines inoculated with the nitrogen fixing plant-interacting bacteria Herbaspirillum seropedicae and Azospirillum brasilense. PLoS ONE 2017, 12, e0174576. [Google Scholar] [CrossRef] [PubMed]
  141. Dong, Y.; Iniguez, A.L.; Ahmer, B.M.M.; Triplett, E.W. Kinetics and strain specificity of rhizosphere and endophytic colonization by enteric bacteria on seedlings of Medicago sativa and Medicago truncatula. Appl. Environ. Microbiol. 2003, 69, 1783–1790. [Google Scholar] [CrossRef] [PubMed]
  142. Sheng, X.F.; Xia, J.J.; Jiang, C.Y.; He, L.Y.; Qian, M. Characterization of heavy metal-resistant endophytic bacteria from rape (Brassica napus) roots and their potential in promoting the growth and lead accumulation of rape. Environ. Pollut. 2008, 156, 1164–1170. [Google Scholar] [CrossRef] [PubMed]
  143. Verma, S.C.; Singh, A.; Chowdhury, S.P.; Tripathi, A.K. Endophytic colonization ability of two deep-water rice endophytes, Pantoea sp. and Ochrobactrum sp. using green fluorescent protein reporter. Biotechnol. Lett. 2004, 26, 425–429. [Google Scholar] [CrossRef] [PubMed]
  144. Verma, S.C.; Ladha, J.K.; Tripathi, A.K. Evaluation of plant growth promoting and colonization ability of endophytic diazotrophs from deep water rice. J. Bacteriol. 2001, 91, 127–141. [Google Scholar] [CrossRef]
  145. Long, H.H.; Schmidt, D.D.; Baldwin, I.T. Native bacterial endophytes promote host growth in a species-specific manner; phytohormone manipulations do not result in common growth responses. PLoS ONE 2008, 3, e2702. [Google Scholar] [CrossRef] [PubMed]
  146. Duijff, B.J.; Gianinazzi-Pearson, V.; Lemanceau, P. Involvement of the outer membrane lipopolysaccharides in the endophytic colonization of tomato roots by biocontrol Pseudomonas fluorescens strain WCS417r. New Phytol. 1997, 135, 325–334. [Google Scholar] [CrossRef]
  147. Khan, Z.; Roman, D.; Kintz, T.; Delas Alas, M.; Yap, R.; Doty, S. Degradation, phytoprotection and phytoremediation of phenanthrene by endophyte Pseudomonas putida, PD1. Environ. Sci. Technol. 2014, 48, 12221–12228. [Google Scholar] [CrossRef] [PubMed]
  148. Andreote, F.D.; De Araújo, W.L.; De Azevedo, J.L.; Van Elsas, J.D.; Da Rocha, U.N.; Van Overbeek, L.S. Endophytic colonization of potato (Solanum tuberosum L.) by a novel competent bacterial endophyte, Pseudomonas putida strain P9, and its effect on associated bacterial communities. Appl. Environ. Microbiol. 2009, 75, 3396–3406. [Google Scholar] [CrossRef] [PubMed]
  149. Germaine, K.J.; Liu, X.; Cabellos, G.G.; Hogan, J.P.; Ryan, D.; Dowling, D.N. Bacterial endophyte-enhanced phytoremediation of the organochlorine herbicide 2,4-dichlorophenoxyacetic acid. FEMS Microbiol. Ecol. 2006, 57, 302–310. [Google Scholar] [CrossRef] [PubMed]
  150. Khan, Z.; Doty, S.L. Characterization of bacterial endophytes of sweet potato plants. Plant Soil 2009, 322, 197–207. [Google Scholar] [CrossRef]
  151. Oliveira, A.L.M.; Urquiaga, S.; Döbereiner, J.; Baldani, J.I. The effect of inoculating endophytic N2-fixing bacteria on micropropagated sugarcane plants. Plant Soil 2002, 242, 205–215. [Google Scholar] [CrossRef]
  152. Knoth, J.L.; Kim, S.; Ettl, G.J.; Doty, S.L. Biological nitrogen fixation and biomass accumulation within poplar clones as a result of inoculations with diazotrophic endophyte consortia. New Phytol. 2014, 201, 599–609. [Google Scholar] [CrossRef] [PubMed]
  153. Oliveira, A.L.M.; Stoffels, M.; Schmid, M.; Reis, V.M.; Baldani, J.I.; Hartmann, A. Colonization of sugarcane plantlets by mixed inoculations with diazotrophic bacteria. Eur. J. Soil Biol. 2009, 45, 106–113. [Google Scholar] [CrossRef]
  154. Khan, Z.; Kandel, S.L.; Ramos, D.N.; Ettl, G.J.; Kim, S.; Doty, S.L. Increased Biomass of Nursery-Grown Douglas-Fir Seedlings upon Inoculation with Diazotrophic Endophytic Consortia. Forests 2015, 6, 3582–3593. [Google Scholar] [CrossRef]
  155. Chen, X.; Miche, L.; Sachs, S.; Wang, Q.; Buschart, A.; Yang, H.; Vera Cruz, C.M.; Hurek, T.; Reinhold-Hurek, B. Rice responds to endophytic colonization which is independent of the common symbiotic signaling pathway. New Phytol. 2015, 208, 531–543. [Google Scholar] [CrossRef] [PubMed]
  156. Rollins, J.A.; Wolpert, T.J.; Johnson, K.B.; Dickman, M.B.; Ciuffetti, L.M.; Lorang, J.M.; Tuori, R.P.; Martinez, J.P.; Sawyer, T.L.; Redman, R.S. Green Fluorescent Protein Is Lighting Up Fungal Biology. Appl. Environ. Microbiol. 2001, 67, 1987–1994. [Google Scholar]
  157. Reinhold-Hurek, B.; Hurek, T. Living inside plants: Bacterial endophytes. Curr. Opin. Plant Biol. 2011, 14, 435–443. [Google Scholar] [CrossRef] [PubMed]
  158. Ryan, R.P.; Germaine, K.; Franks, A.; Ryan, D.J.; Dowling, D.N. Bacterial endophytes: Recent developments and applications. FEMS Microbiol. Lett. 2008, 278, 1–9. [Google Scholar] [CrossRef] [PubMed]
  159. Riedel, G.E.; Ausubel, F.M.; Cannon, F.C. Physical map of chromosomal nitrogen fixation (nif) genes of Klebsiella pneumoniae. Proc. Natl. Acad. Sci. USA 1979, 76, 2866–2870. [Google Scholar] [CrossRef] [PubMed]
  160. Cankar, K.; Kraigher, H.; Ravnikar, M.; Rupnik, M. Bacterial endophytes from seeds of Norway spruce (Picea abies L. Karst). FEMS Microbiol. Lett. 2005, 244, 341–345. [Google Scholar] [CrossRef] [PubMed]
  161. Egener, T.; Hurek, T.; Reinhold-hurek, B.; Mikrobiologie, M.; Symbioseforschung, A. Endophytic Expression of nif Genes of Azoarcus sp. Strain BH72 in Rice Roots. Mol. Plant Microbe Interact. 1999, 12, 813–819. [Google Scholar] [CrossRef]
  162. Weilharter, A.; Mitter, B.; Shin, M.V.; Chain, P.S.G.; Nowak, J.; Sessitsch, A. Complete genome sequence of the plant growth-promoting endophyte Burkholderia phytofirmans strain PsJN. J. Bacteriol. 2011, 193, 3383–3384. [Google Scholar] [CrossRef] [PubMed]
  163. Bulgarelli, D.; Schlaeppi, K.; Spaepen, S.; van Themaat, E.V.L.; Schulze-Lefert, P. Structure and Functions of the Bacterial Microbiota of Plants. Annu. Rev. Plant Biol. 2013, 64, 807–838. [Google Scholar] [CrossRef] [PubMed]
  164. De Souza, R.S.C.; Okura, V.K.; Armanhi, J.S.L.; Jorrín, B.; Lozano, N.; da Silva, M.J.; González-Guerrero, M.; de Araújo, L.M.; Verza, N.C.; Bagheri, H.C.; et al. Unlocking the bacterial and fungal communities assemblages of sugarcane microbiome. Sci. Rep. 2016, 6, 28774. [Google Scholar] [CrossRef] [PubMed]
  165. Case, R.J.; Boucher, Y.; Dahllöf, I.; Holmström, C.; Doolittle, W.F.; Kjelleberg, S. Use of 16S rRNA and rpoB genes as molecular markers for microbial ecology studies. Appl. Environ. Microbiol. 2007, 73, 278–288. [Google Scholar] [CrossRef] [PubMed]
  166. Kaul, S.; Sharma, T.; Dhar, M.K. “Omics” Tools for Better Understanding the Plant–Endophyte Interactions. Front. Plant Sci. 2016, 7, 1–9. [Google Scholar] [CrossRef] [PubMed]
  167. Isebrands, J.G.; Aronsson, P.; Carlson, M.; Ceulemans, R.; Coleman, M.; Dickinson, N.; Dimitriou, J.; Doty, S.; Gardiner, E.; Heinsoo, K.; et al. Environmental Applications of Poplars and Willows. In Poplars and willows: Trees for Society and the Environment; Isebrands, J.G., Richardson, J., Eds.; The Food and Agriculture Organization of the United Nations: Rome, Italy, 2014; pp. 258–336. ISBN 9781780641089. [Google Scholar]
  168. Kang, J.W.; Khan, Z.; Doty, S.L. Biodegradation of trichloroethylene by an endophyte of hybrid poplar. Appl. Environ. Microbiol. 2012, 78, 3504–3507. [Google Scholar] [CrossRef] [PubMed]
  169. Doty, S.L.; Dosher, M.R.; Singleton, G.L.; Moore, A.L.; Van Aken, B.; Stettler, R.F.; Strand, S.E.; Gordon, M.P. Identification of an endophytic Rhizobium in stems of Populus. Symbiosis 2005, 39, 27–35. [Google Scholar]
  170. Hacquard, S.; Schadt, C.W. Towards a holistic understanding of the beneficial interactions across the Populus microbiome. New Phytol. 2015, 205, 1424–1430. [Google Scholar] [CrossRef] [PubMed]
  171. Khan, Z.; Guelich, G.; Phan, H.; Redman, R.; Doty, S. Bacterial and Yeast Endophytes from Poplar and Willow Promote Growth in Crop Plants and Grasses. ISRN Agron. 2012, 1–11. [Google Scholar] [CrossRef]
  172. Kandel, S.L. Salicaceae Enophytes: Growth Promotion Potential in Rice and Maize and Bio-Control of Plant Pathogen. Ph.D. Thesis, University of Washington, Seattle, WA, USA, 2016. [Google Scholar]
  173. Cangelosi, G.A.; Abest, E.; Martinettii, G.; Nester, E.W. Genetic analysis of Agrobacterium. Methods Enzymol. 1991, 204, 384–397. [Google Scholar] [PubMed]
  174. Rho, H.; Hsieh, M.; Kandel, S.L.; Cantillo, J.; Doty, S.L.; Kim, S.H. Do Endophytes Promote Growth of Host Plants Under Stress? A Meta-Analysis on Plant Stress Mitigation by Endophytes. Microb. Ecol. 2017, 1–12. [Google Scholar] [CrossRef] [PubMed]
  175. He, H.; Ye, Z.; Yang, D.; Yan, J.; Xiao, L.; Zhong, T.; Yuan, M.; Cai, X.; Fang, Z.; Jing, Y. Characterization of endophytic Rahnella sp. JN6 from Polygonum pubescens and its potential in promoting growth and Cd, Pb, Zn uptake by Brassica napus. Chemosphere 2013, 90, 1960–1965. [Google Scholar] [CrossRef] [PubMed]
Figure 1. Hypothesized colonization cycle of bacterial endophytes in the host plant. (a) Mobilization of seed endophytes in germinating seedlings. (b) Recruitment of alien endophytes from the soil in developing seedlings. (c) Colonization by alien and inherited endophytes. (d) Whole plant colonization by various endophytes. (e) Variation of endophyte communities in the host plant in response to different biotic and abiotic stresses. (f) Vertical transfer of endophytes into seeds.
Figure 1. Hypothesized colonization cycle of bacterial endophytes in the host plant. (a) Mobilization of seed endophytes in germinating seedlings. (b) Recruitment of alien endophytes from the soil in developing seedlings. (c) Colonization by alien and inherited endophytes. (d) Whole plant colonization by various endophytes. (e) Variation of endophyte communities in the host plant in response to different biotic and abiotic stresses. (f) Vertical transfer of endophytes into seeds.
Microorganisms 05 00077 g001
Figure 2. Maize (hybrid 29B17) roots colonized by WP5gfp visualized under 630× magnification. Image on the left (A,C) were taken with the GFP filter, and images on the right (B,D) were taken without the GFP filter. Groups of WP5gfp cells were observed in the intercellular spaces of cell layers in the longitudinal direction.
Figure 2. Maize (hybrid 29B17) roots colonized by WP5gfp visualized under 630× magnification. Image on the left (A,C) were taken with the GFP filter, and images on the right (B,D) were taken without the GFP filter. Groups of WP5gfp cells were observed in the intercellular spaces of cell layers in the longitudinal direction.
Microorganisms 05 00077 g002
Figure 3. Maize (hybrids 14A91 and 29B17) roots were colonized by WP5gfp and visualized under 630× magnification. Image on the left (A,C) were taken with the GFP filter, and images on the right (B,D) were taken without the GFP filter. WP5gfp cells were observed in the middle lamella areas of the transverse wall between two adjacent cells.
Figure 3. Maize (hybrids 14A91 and 29B17) roots were colonized by WP5gfp and visualized under 630× magnification. Image on the left (A,C) were taken with the GFP filter, and images on the right (B,D) were taken without the GFP filter. WP5gfp cells were observed in the middle lamella areas of the transverse wall between two adjacent cells.
Microorganisms 05 00077 g003
Figure 4. Maize (hybrid 29B17) radicle roots were colonized by WP5gfp and visualized under 630× magnification. Images on the left (A,C) were taken with the GFP filter, and images on the right (B,D) were taken without the GFP filter. Microcolonies of WP5gfp were observed along the plant cell wall areas between two adjacent cells.
Figure 4. Maize (hybrid 29B17) radicle roots were colonized by WP5gfp and visualized under 630× magnification. Images on the left (A,C) were taken with the GFP filter, and images on the right (B,D) were taken without the GFP filter. Microcolonies of WP5gfp were observed along the plant cell wall areas between two adjacent cells.
Microorganisms 05 00077 g004
Figure 5. Maize (hybrid 29B17) leaves were colonized by WP5gfp visualized under 630× magnification. Image on the left (A,C) were taken with the GFP filter, and images on the right (B,D) were taken without the GFP filter. WP5gfp was observed in the intercellular spaces of cell layers and stomatal chambers.
Figure 5. Maize (hybrid 29B17) leaves were colonized by WP5gfp visualized under 630× magnification. Image on the left (A,C) were taken with the GFP filter, and images on the right (B,D) were taken without the GFP filter. WP5gfp was observed in the intercellular spaces of cell layers and stomatal chambers.
Microorganisms 05 00077 g005
Figure 6. Quantification of CFUs of WP5gfp per gram of tissue in shoots, including leaves and stem, and roots. Errors bars represent standard error of the mean.
Figure 6. Quantification of CFUs of WP5gfp per gram of tissue in shoots, including leaves and stem, and roots. Errors bars represent standard error of the mean.
Microorganisms 05 00077 g006
Figure 7. Root, and root and shoot biomass of WP5gfp inoculated and mock-inoculated control plants in maize hybrid 29B17. Error bars represent standard error of the mean. Histograms with different letters are statistically different at p < 0.05.
Figure 7. Root, and root and shoot biomass of WP5gfp inoculated and mock-inoculated control plants in maize hybrid 29B17. Error bars represent standard error of the mean. Histograms with different letters are statistically different at p < 0.05.
Microorganisms 05 00077 g007
Table 1. Colonization of different plants by bacterial endophytes.
Table 1. Colonization of different plants by bacterial endophytes.
Endophyte SpeciesNative HostPlant ColonizedTissues ColonizedEffect on PlantReferences
Acetobacter diazotrophicusSugarcaneSugarcaneStemN/ADong et al., 1994 [27]
Achromobacter sp., and Acinetobacter sp.Poaceae family (maize, wheat, pearl millet, sorghum and rice)WheatRootGrowth enhancementPatel et al., 2017 [125]
Azoarcus sp.Kallar grassRice, and Kallar grassRoot, shootGrowth enhancementHurek et al., 1994 [126]
Azoarcus sp.Kallar grassRiceRootN/AReinhold-Hurek et al., 2006 [88]
Azospirillum sp.MaizeMaizeN/AGrowth enhancementRiggs et al., 2001 [29]
Bacillus megateriumMaizeMaizeRoot, stem, leafN/ALiu et al., 2006 [127]
Bacillus pumilusRiceRiceRootGrowth enhancementBacilio-Jimenez et al., 2001 [128]
Bacillus sp.TomatoWheatN/AGrowth enhancementTian et al., 2017 [129]
Bacillus sp.MaizeMaizeN/AGrowth enhancementRiggs et al., 2001 [29]
Bacillus subtilisMulberryMulberryRoot, stem, leafReduced bacterial wiltJi et al., 2008 [130]
Burkholderia cepaciaMaizeMaizeN/AGrowth enhancementRiggs et al., 2001 [29]
Burkholderia phytofirmansOnionGrapevineRoot, stem, berryN/ACompant et al., 2008 [131]
Burkholderia phytofirmansOnionGrapevineRoot, stem, leafGrowth enhancementCompant et al., 2005 [81]
Burkholderia phytofirmansOnionSwitchgrassRoot, leaf, sheathGrowth enhancementKim et al., 2012 [132]
Burkholderia phytofirmansOnionArabidopsis thalianaRootGrowth enhancement, increased chlorophyll contentZuniga et al., 2013 [67]
Burkholderia phytofirmansOnionWhite lupin, and maizeRoot, seedN/AKost et al., 2014 [66]
Burkholderia phytofirmansOnionMaizeRoot, stem, leafGrowth enhancement, increased drought toleranceNaveed et al., 2014 [60]
Burkholderia sp.TomatoWheatN/AGrowth enhancementTian et al., 2017 [129]
Burkholderia vietnamiensisPoplarKentucky bluegrassRoot, shootGrowth enhancementXin et al., 2009 [43]
Burkholderia vietnamiensisRiceRiceRootGrowth enhancementGovindarajan et al., 2008 [133]
Burkholderia vietnamiensisSugarcaneSugarcaneRootGrowth enhancement, increased yieldGovindarajan et al., 2006 [134]
Corynebacterium flavescensRiceRiceRootGrowth enhancementBacilio-Jimenez et al., 2001 [128]
Enterobacter sp.MaizeMaizeRoot, stem, leafGrowth enhancement, increased drought toleranceNaveed et al., 2014 [60]
Enterobacter sp.Hybrid poplar (Populus deltoides × P. nigra)Hybrid poplarRoot, leaf budGrowth enhancement, reduced phytotoxicity of TCE, degradation of TCEDoty et al., 2017 [135]
Enterobacter sp.TomatoWheatN/AGrowth enhancementTian et al., 2017 [129]
Enterobacter sp.MaizeMaizeN/AGrowth enhancementRiggs et al., 2001 [29]
Gluconacetobacter diazotrophicusSugarcaneWheat, and sorghumRoot, shoot, stem, leafN/ALuna et al., 2010 [136]
Gluconacetobacter diazotrophicusMaizeMaizeN/AGrowth enhancementRiggs et al., 2001 [29]
Gluconacetobacter diazotrophicusSugarcaneRiceRootN/AMeneses et al., 2017 [76]
Gluconacetobacter diazotrophicusSugarcaneSugarcane, and riceRoot, ShootN/ARouws et al., 2010 [137]
Herbaspirillum seropedicaeMaizeMaizeRootN/ABalsanelli et al., 2014 [77]
Herbaspirillum seropedicaeMaizeMaizeN/AGrowth enhancementRiggs et al., 2001 [29]
Herbaspirillum seropedicaeMaizeMaizeRootIncreased rooting, change in gene expressionAmaral et al., 2014 [138]
Herbaspirillum seropedicaeMaizeMaize, wheat, rice and sorghumRoot, stem, leafN/ARoncata-Maccari et al., 2003 [139]
Herbaspirillum seropedicaeRiceRiceRoot, coleoptile, leafGrowth enhancementJames et al., 2002 [99]
Herbaspirillum seropedicaeSorghumMaizeRoot, leafN-fixation, change in metabolic profileBrusamarello-Santos et al., 2017 [140]
Herbaspirillum seropedicaeSorghumWheatRootChange in gene expressionPankievicz et al., 2016 [87]
Herbaspirillum sp.Rice (Oryza officianalis)Rice (Oryza spp.)Shoot, seed, leafGrowth enhancement, N-fixationElbeltagy et al., 2001 [12]
Klebsiella pneumoniaeMaizeAlfalfa, Arabidopsis, wheat, and riceRoot, hypocotylN/ADong et al., 2003 [141]
Klebsiella pneumoniaeMaizeWheatRootGrowth enhancement, increased chlorophyll content, N-fixationIniguez et al. 2004 [14]
Klebsiella pneumoniaeMaizeAlfalfaRoot, hypocotylN/ADong et al., 2003 [141]
Klebsiella sp.MaizeMaizeN/AGrowth enhancementRiggs et al., 2001 [29]
Microbacterium sp.RapeRapeRootGrowth enhancement, increased Pb uptake, root elongation,Sheng et al., 2008 [142]
Ochrobactrum sp.RiceRiceRootN/AVerma et al., 2004 [143]
Pantoea agglomeransMaizeMaizeN/AGrowth enhancementRiggs et al., 2001 [29]
Pantoea agglomeransRiceRiceRootN/AVerma et al., 2001 [144]
Pantoea sp.RiceRiceRootN/AVerma et al., 2004 [143]
Pseudomonas fluorescencesMiscanthusPeaN/AGrowth enhancement in phosphate limited conditionsOteino et al. 2015 [48]
Pseudomonas fluorescensRapeRapeRootGrowth enhancement, increased Pb uptake, root elongation,Sheng et al., 2008 [142]
Pseudomonas fluorescensBlack nightshadeBlack nightshade and tobaccoRootGrowth enhancementLong et al., 2008 [145]
Pseudomonas fluorescensWheatTomatoRootN/ADuijff et al., 1997 [146]
Pseudomonas putidaHybrid poplarWillowRootGrowth enhancement, reduced phytotoxicity of phenanthrene, degradation of phenanthreneKhan et al., 2014 [147]
Pseudomonas putidaPotatoPotatoRoot, stemGrowth enhancement, Phytophthora infestans suppressionAndreote et al., 2009 [148]
Pseudomonas putidaPoplarPeaRoot, stem, leafIncreased accumulation of and tolerance to 2,4-dichlorophenoxyacetic acidGermaine et al., 2006 [149]
Pseudomonas sp.Black nightshadeBlack nightshade and tobaccoRootGrowth enhancementLong et al., 2008 [145]
Pseudomonas sp.TomatoWheatN/AGrowth enhancementTian et al., 2017 [129]
Pseudomonas sp.PoplarPoplarRoot, stem, leafN/AGermaine et al., 2004 [92]
Pseudomonas thivervalensisBlack nightshadeBlack nightshade and tobaccoRootGrowth enhancementLong et al., 2008 [145]
Ralstonia sp.Poaceae family (maize, wheat, pearl millet, sorghum and rice)WheatRootGrowth enhancementPatel et al., 2017 [125]
Rhanella aquatilisSweet potatoHybrid poplarN/AIncreased rootingKhan et al., 2009 [150]
Rhizobium sp.TomatoWheatN/AGrowth enhancementTian et al., 2017 [129]
Rhizobium sp.Poaceae family (maize, wheat, pearl millet, sorghum and rice)WheatRootGrowth enhancementPatel et al., 2017 [125]
Rhizobium sp.MaizeMaizeN/AGrowth enhancementRiggs et al., 2001 [29]
Serratia marcescensRiceRiceRoot, stem, leafGrowth enhancementGyaneshwar et al., 2001 [98]
Staphylococcus sp.TomatoWheatN/AGrowth enhancementTian et al., 2017 [129]
Stenotrophomonas sp.TomatoWheatN/AGrowth enhancementTian et al., 2017 [129]
Consortium (Gluconacetobacter diazotrophicus, Herbaspirillum seropedicae, Herbaspirillum rubrisubalbicans, Azospirillum amazonense and Burkholderia sp.)SugarcaneSugarcaneRoot, shootGrowth enhancement, increased N contentOliveira et al., 2002 [151]
Consortium (Burkholderia vietnamiensis, Rhanella sp., Acinetobacter sp., Herbaspirillum sp., Pseudomonas putida, Sphingomonas spp.Poplar and willowSweet cornRoot, shootGrowth enhancement, increased CO2 assimilationKnoth et al., 2012 [19]
Consortium (Burkholderia vietnamiensis, Rhanella sp., Enterobacter sp., Pseudomonas graminis, Acinetobacter sp., Herbaspirillum sp., Sphingomonas yanoikuyae, Pseudomonas putida, Sphingomonas, Sphingomonas yanoikuyae)Poplar and willowPoplar and hybrid poplarN/AGrowth enhancementKnoth et al., 2014 [152]
Consortium (Burkholderia vietnamiensis, Rhizobium tropici, Acinetobacter calcoaceticus, Rhanella sp., Burkholderia sp., Enterobacter asburiae, Sphingomonas yanoikuyae, Pseudomonas sp., Curtobacterium sp.)Poplar and willowHybrid poplarN/AGrowth enhancement, increased drought toleranceKhan et al., 2016 [45]
Consortium (Burkholderia vietnamiensis, Rhizobium tropici, Acinetobacter calcoaceticus, Rhanella sp., Burkholderia sp., Sphingomonas yanoikuyae, Pseudomonas sp., Sphingomonas sp.)Poplar and willowRiceRoot, shootGrowth enhancement (N-limited conditions)Kandel et al., 2015 [18]
Consortium (Gluconacetobacter diazotrophicus, Herbaspirillum seropedicae, Herbaspirillum rubrisubalbicans, Azospirillum amazonense, Burkholderia tropica)SugarcaneSugarcaneRootN/AOliveira et al., 2009 [153]
Consortium (Pseudomonas spp., Paentbacillus spp., Sphingomonas azotifigens)Ryegrass and riceRyegrassRoot, stem, leafGrowth enhancement, increased TFACastanheira et al., 2017 [95]
Consortium (Rhizobium tropici bv. populus, Acinetobacter calcoaceticus, Rhanella sp., Burkholderia sp., Sphingomonas spp.)Poplar and willowDouglas-firRoot, needlesGrowth enhancement (nutrient limited conditions)Khan et al., 2015 [154]
Back to TopTop