InTechOpen uses cookies to offer you the best online experience. By continuing to use our site, you agree to our Privacy Policy.

Agricultural and Biological Sciences » "Plant Ecology - Traditional Approaches to Recent Trends", book edited by Zubaida Yousaf, ISBN 978-953-51-3340-7, Print ISBN 978-953-51-3339-1, Published: September 6, 2017 under CC BY 3.0 license. © The Author(s).

Chapter 6

Plant-Microbe Ecology: Interactions of Plants and Symbiotic Microbial Communities

By Ying-Ning Ho, Dony Chacko Mathew and Chieh-Chen Huang
DOI: 10.5772/intechopen.69088

Article top


Plant soil community feedback in low diversity communities (modified after Bever et al. [16]).
Figure 1. Plant soil community feedback in low diversity communities (modified after Bever et al. [16]).
Factors affecting plant-microbe interactions.
Figure 2. Factors affecting plant-microbe interactions.
Genomic tools to understand major units of the plant-microbe ecological system. Colored boxes indicate technique tools that can be used to characterize key factors for the corresponding unit. (modified after Kroll et al. [167]).
Figure 3. Genomic tools to understand major units of the plant-microbe ecological system. Colored boxes indicate technique tools that can be used to characterize key factors for the corresponding unit. (modified after Kroll et al. [167]).

Plant-Microbe Ecology: Interactions of Plants and Symbiotic Microbial Communities

Ying-Ning Ho1, Dony Chacko Mathew2 and Chieh-Chen Huang2
Show details


Plant community dynamics are driven by the microbial mediation of soil resource partitioning and sharing by the inhibition of other host symbionts or sharing the broadly specific symbiotic fungi. The plant phenotype and ecology can be affected by the impact of the symbiotic microbes on the environment and competition for soil resources.

The advent of modern biotechnology has made it easy to study plant-microbe interactions further. Current genomic technologies applied to natural and artificial systems have shown that the plant genotype has a small but significant effect on the microbial community composition of the phyllosphere, the rhizosphere, and endophytic microbes. In this chapter, we discuss the relationship between the host and its symbiotic microbial community and the role of plant metabolites and root exudates such as organic acids, amino acids, sugars and antimicrobial compounds in shaping a specific rhizosphere community, attracting plant growth promoting rhizobacteria (PGPR) colonization on the plant roots and inhibiting or attracting soil-borne pathogens. In addition, we also review and introduce the functionality of plant symbiotic microbes for increasing the abiotic and biotic stress tolerance of the host. An understanding of the ecosystem function of plant and symbiotic microbes will guide efforts to improve agriculture practices.

Keywords: plant-microbe ecology, symbiotic microbial communities, interactions of host and symbiotic microbes

1. Introduction

Plants have recently been recognized as a metaorganism that possesses a distinct microbiome and close symbiotic relationships with associated microorganisms [1]. Plant ecology is affected by complex interactions with plant-associated microbes. The roles of both plant-associated microbes and the host in ecosystem function have been recognized, but the detailed mechanisms are unclear. Since plants are immobile, they have coevolved with microbes and acquired a number of mechanisms that modulate the outcome of their interactions [2]. Roots can continuously synthesize, accumulate, and secrete a wide range of compounds into the soil [3], which are known as the root exudates. Root exudates contain enzymes, water, H+ ions, mucilage, and carbon-containing primary and secondary compounds [4, 5]. Campbell and Greaves [6, 7] observed that the density of microbes in the rhizosphere was 100 times greater than that in the bulk soil. Recent studies have showed that plant root exudates shape the soil bacterial community [8, 9]. According to a study by Ciccazzo [10], a plant species selects a specific rhizosphere bacterial community. The change in the microbial composition generates feedback on the plant relative performance that defines the long-term effects of the soil microbes on their coexistence with that plant species [11, 12]. The feedback can be of two types; positive plant-soil microbial feedback reinforces the spatial separation of the microbial communities [13], while negative feedback results in plant replacement, which necessitates recolonization of locally specific roots [1416]. Systematic methods such as genome-wide association studies have enabled us to explore the relationships of plant loci and symbiotic communities in detail [17, 18]. How does the microbiome diversity and function potentially affect host plant performance? The presence of microbial hubs in plant microbiome networks plays an important role between a plant and its microbial community [19]. Plant growth–promoting rhizobacteria (PGPR) can produce a complex blend of volatile substances, which are distinct between bacterial species and other closely related species [2022]. Some of these bacterial volatiles can stimulate plant growth [23, 24], suppress disease stimulating ISR [25], or antagonize phytopathogens [26, 27], nematodes, or insects [28, 29].

Worldwide crop production is affected by biotic and abiotic stress factors [3032], which cause millions of dollars in losses. The beginning of the industrial revolution in 1750 and the human activities such as burning fossil fuels and deforestation have altered the global climate. An increase in carbon dioxide and temperature is speeding up the life cycle of grain and oilseed crops [33]. According to Lesk [34], extreme heat waves and droughts have reduced global harvests of cereals such as maize, wheat, and rice by 10% in a span of 50 years, which has become a grave concern of various governments. The impact of a warming climate on spring plant phenology is evident [35, 36]. A longer growing season may increase carbon uptake and potentially mitigate climate change [37, 38], leaf emergence [39], fruiting [40], and germination [41]. Abiotic stress factors include extreme temperature [42], drought, water logging, light, and salinity as major parameters that affect plant growth. Plant-associated microbes or PGPR were found to benefit plants by enhancing nutrient uptake, stimulating root, and shoot growth by producing indole acetic acid [43, 44], 1-aminocyclopropane-1-carboxylate (ACC) deaminases [45], solubilizing phosphate [46], and enhancing the uptake of nutrients from the environment [47, 48]. They also assist and enhance plant resistance to adverse environmental stresses such as drought, heavy metals, salts, and nutrient deficiency [49]. Biotic stress factors include interaction with other organisms and infection by pathogens or damage by insect pests, and some plant growth–promoting bacteria have been used as biocontrol agents against plant pathogens [50, 51]. This chapter explores the relationships between plant hosts and their symbiotic microbial communities. We discuss and review current reports of how the plant-associated microbial community might be shaped by the host and how the plant microbiome affects plant growth, productivity, and host survival in various symbiotic associations. This knowledge will guide efforts to improve agricultural practices and predict how environmental factors will affect the microbial community and plant diversity.

2. Plant community ecology and soil symbiont interactions

Plant ecology can be affected by global climate change in terms of above- and below-ground ecological diversity in a terrestrial ecosystem. The terrestrial plant community drives dynamic changes in the soil microbial ecology that may result in alterations in ecosystem function. The ecologist Dr. Peter Chesson postulated that stabilizing mechanisms are essential for maintenance of species diversity and coexistence [52]. Bever et al. have found evidence that microbially mediated positive and negative feedback might play a crucial role in the entire plant ecosystem and contribute to these mechanisms of plant-plant interactions [16]. Traditionally, competing plant species have been thought to have strong negative intraspecific interactions for the high overlap in resource usage [53]. However, success in finding a mechanism to explain the coexistence of competing plant species in maintaining local diversity [54]. Neglecting soil microbial community feedback might be one reason.

2.1. Soil resources and microbial interactions

Soil resources can govern the coexistence of plant species by resource partitioning and sharing. Studies have found root symbionts that increase the efficiency of nutrient uptake and allow the host to persist in a low nutrient environment, thereby directly contributing to the competitive exclusion of other plants [55]. Rhizosphere microbes can alter the availability of different forms of nitrogen or phosphorus in the soil and affect plant-plant interactions via the mediation of resource partitioning [56]. Soil resources can also be transferred by shared symbiotic fungi called common mycorrhizal networks (CMNs) [57]. In nature, different plant species commonly share the broadly specific mycorrhizal fungi. Simard and Durall demonstrated the direct transfer of resources from one plant to another via CMNs with labeled carbon, nitrogen, and phosphorus [57]. Plant community dynamics are driven by the microbial mediation of soil resource partitioning and sharing.

2.2. Host response to microbes and soil community feedback

The dynamic density and composition of the rhizospheric microbes can affect the coexistence of plant species via indirect feedback (i.e., the competition or inhibition of symbionts) in the plant population [58]. Ecologists have proposed three hypotheses to explain the mechanism that produces low diversity plant communities. The empty niche hypothesis suggests that novel symbionts inhabit the areas invaded by invasive plants [59]. These symbionts are more efficient at resource acquisition and preferentially associated with invasive plants than with other plants. The degraded mutualist hypothesis suggests that invasive plants and their symbionts inhibit the ability of the native symbiotic community to acquire resources, indirectly reducing the performance of native plants [60, 61] (Figure 1). Positive feedback might be exemplified by the enhanced growth and survival of exotic seedlings near native established symbionts [62, 63]. Plant monodominance, coexistence, and invasion ecology have high relation to symbiotic microbial interactions.


Figure 1.

Plant soil community feedback in low diversity communities (modified after Bever et al. [16]).

3. Plants shape the microbial community

Microbial interactions play a crucial role in plant community ecology and performance. How do plants harbor unique microbial communities? How do plants shape a unique rhizosphere microbial community? These are the questions that must be addressed. Modern genomic technologies (e.g., high throughput sequencing) can provide clues to the answer. Lundberg et al. attempted to define the core Arabidopsis thaliana root microbiome [64]. They collected more than 600 A. thaliana plants and compared the bacterial communities using 16S rRNA gene sequencing. They observed that the root microbial communities of plants are sufficiently dependent on the host genotype to vary between inbred A. accessions. However, the mechanisms were not clear but included differences in the host physiology and immune responses.

3.1. Plant genes responsible for defense affect the variation of the microbial community

Several studies showed that plant genotype has a small but significant effect on the composition of the endophytic, rhizosphere, or phyllosphere microbial communities [17, 6467]. A quantitative trait locus (QTL) analysis and a genome-wide association study (GWAS) were used to identify taxa linked to host genes in humans, mice, plants, and flies [17, 6870]. A GWAS of the A. thaliana leaf microbial community suggested that the A. thaliana loci are responsible for defense and that cell wall integrity affected the composition of this community [17]. Furthermore, host genetic variation shaped species richness in the bacterial community. Horton et al. showed that defense response associated genes against pathogens shaped this microbial ecosystem. In Matthew's study, 196 accessions of A. thaliana were sown in a greenhouse and transferred to a field site. The field experiment data suggested that the plant tissue structure (i.e., the cell wall integrity) might affect the leaf microbial community. To understand the plant host genetic factors that affect the associated microbial population, Bodenhausen et al. used a candidate gene approach to investigate the host effects on the composition and abundance of the A. thaliana phyllosphere community [67]. A panel of 55 A. thaliana mutants with alterations in the cell wall, surface structure, defense signaling, secondary metabolism, and pathogen recognition was constructed to reveal the effect on the microbiota composition and/or abundance in a small number of single host mutations. The results showed that lacs and pec1 mutants affected cuticle formation, which led to an increased bacterial abundance and community composition. Moreover, the ethylene signaling gene ein2 was observed to be a host factor that modulated the community composition. Peiffer et al. also noted that approximately 19% of the interline variation in species richness could be attributed to the host genotype in different maize lines grown in the same geographical regions [65].

3.2. Role of root exudates in shaping rhizosphere microbial community

More than a century ago, Lorenz Hiltner defined the term “rhizosphere” as the soil compartment affected by plant roots [71]. Soil microbes are chemotactically attracted to plant root exudates, volatile organic carbon, and rhizodeposition, and then proliferate in this carbon-rich environment [72]. Plant root exudates differ between plant species, so differences in rhizosphere microbiomes of different plant species are expected [73]. More recent studies have provided strong evidence for plant species-specific microbiomes [74, 75]. Plants can also shape the microbial community via root exudates. Root exudates can be categorized as sugars, amino acids, organic acids, nucleotides, flavonoids, antimicrobial compounds, and enzymes [4, 73].

3.2.1. The types of root exudate Organic acids and amino acids

The composition of root exudates from different cultivars affects the growth of soil-borne pathogens. The susceptible peanut cultivar Ganhua-5 (GH) and the mid-resistant cultivar Quanhua-7 (QH) were chosen for a root exudate analysis and evaluated for the responses of the soil-borne pathogens Fusarium oxysporum and Fusarium solani [76]. The contents of total amino acids, alanine, and sugars in the root exudate of susceptible cultivars were significantly higher than in the mid-resistant cultivar, whereas the contents of total phenolic acids, p-hydroxybenzoic acid, benzoic acid, and p-coumaric acid were significantly lower than in mid-resistant cultivars. These differences in the root exudate composition of susceptible and resistant cultivars might be assumed to regulate the resistance mechanism in the peanut rhizosphere. However, the spore germination and mycelial growth of the soil-borne pathogens F. oxysporum and F. solani were significantly enhanced by treatment with the root exudates from both the susceptible and mid-resistant cultivars compared with a control. If root exudates do not directly inhibit the growth of pathogens, the effects of other factors must be considered. A previous report showed that organic acids modulated the colonization and enhanced the biofilm formation of the root microbiome. Yuan et al. demonstrated that organic acids from banana root exudates facilitated the root colonization by Bacillus amyloliquefaciens [77]. Fumaric acid significantly induced biofilm formation, whereas malic acid evoked the greatest chemotactic response. The results showed that organic acids from banana root exudates played a crucial role in attracting and initiating PGPR colonization on the plant roots. Rice exudates that primarily contained the amino acid residues of histidine, proline, valine, alanine, and glycine, and the carbohydrates glucose, arabinose, mannose, galactose, and glucuronic acid may induce a higher chemotactic response by the endophytic bacteria Corynebacterium flavescens and Bacillus pumilus [78]. Sugars

The amount of sugar secretion might affect infection by plant pathogens. Gou et al. showed that the Arabidopsis vacuolar sugar transporter SWEET2 limited the Glc-derived carbon efflux from roots and inhibited Pythium infection [79]. They proposed that the expression of SWEET2 modulated sugar secretion, limiting the carbon loss to the rhizosphere. The reduction of available substrates in the rhizosphere contributed to the resistance to Pythium. Antimicrobial compounds

Root exudates can also participate in belowground plant defense. Low-molecular-weight antimicrobial chemicals can be divided into “phytoanticipins” and “phytoalexins” [80]. Phytoanticipins are defensive compounds that are constitutively produced and released by the plant root prior to a biotic stress such as pathogen infection. In a recent study, Arabidopsis roots deficient in diterpene rhizathalene A production were found to be more susceptible to insect herbivory [81]. Therefore, rhizathalene A was considered as a part of a constitutive direct defense system of the roots. Phytoalexins were defined as inducible defensive compounds that are not detected in healthy plants [80]. Five phenylpropanoid root-derived aromatic root exudates were induced by the attack of the soil-borne pathogen Fusarium graminearum and exhibited antifungal activity [82]. In general, root-secreted terpenoid and phenolic defensive compounds have strong antibacterial and antifungal activity [83, 84]. The largest class of plant defensive chemicals above- and below ground is terpenoids. Nonvolatile terpenoids can be secreted into the rhizosphere [85], and volatile organic compounds (VOCs) can be emitted from the roots as plant defensive compounds. Phenylpropanoids are a group of plant defensive phenolic root exudates. After a Fusarium graminearum infection, barley rapidly accumulated and secreted phenylpropanoids, which are cinnamic acid derivatives to resist a fungal attack [82]. Phenolic root exudates not only have antimicrobial activity but also beneficially attract soil-borne microorganisms that affect the native soil microbial community [86]. We have found that the same chemical compound, for example, the amino acid canavanine, can stimulate a specific group of microbes but suppress many other soil microbes. Plants can shape the specific rhizosphere microbial community via root exudates.

3.2.2. Environmental factors effects on root exudates

Plants with different genotypes produce root exudates with different compositions. Abiotic and biotic factors also affect root exudates. Physico-chemical soil properties such as nutrient availability, organic matter content, pH, structure, and texture can affect the availability of root exudates and microbial recruitment by the plant roots. Some biotic factors such as soil microbial secondary metabolism can also affect the exudates. Temperature

Since the onset of climate change and global warming, the resultant extreme heat and cold have affected the harvest of several crops. To elucidate the effects of temperature on root exudates, Husain and McKeen grew strawberry plants at 5–10°C and compared them with plants grown at 20–30°C. They found more amino acids in exudates in plants grown at a low soil temperature that markedly affected the pathogenicity of Rhizoctonia fragariae [87]. Pramanik demonstrated that in Japanese cucumber grown hydroponically in a growth chamber at high and low temperatures, the organic acid content increased with the elevation of temperature, and some of the compounds identified significantly inhibited plant root growth and/or germination of cucumber. Soil moisture

Flood and drought have reduced global cereal harvests. Several reports have demonstrated that the soil moisture affects the release of root exudates. The temporarily wilting of plants increased the release of amino acids from the plant roots, which might be related to the incidence of pathogens in the rhizosphere [88]. Plants such as peas, soybeans, wheat, barley, and tomatoes were grown in normal moist sand and dried, remoistened sand for the liberation of amino acids. The total amount of amino nitrogen in the temporarily dried sand was many times higher than in the normal moist sand. Soil pH and nutrition

The soil pH status and the availability of nutrients such as carbon, nitrogen, and phosphate have been found to affect the release of plant root exudates and the creation of specific chemical niches in the soil, as well as the abundance of plant pathogens and beneficial microbes [8991]. Bowen first demonstrated a marked effect of nutrient status on the exudation of amides and amino acids from roots of Pinus radiate seedlings [89]. The results indicated a doubling of amides/amino acids in exudates from phosphate deficient plants. Toljander et al. analyzed the community of arbuscular mycorrhizal (AM) fungi in maize in a long-term fertilization trial and indicated the composition of AM fungi and bacteria was significantly affected and correlated with changes in pH, phosphate, and the soil carbon content [90]. Dumbrell et al. surveyed the AM fungal community of 425 individual plants from 28 plant species. The results showed the strong support for the hypothesis that niche differentiation was based on the structuring of the AM fungal community by soil pH [91]. Root secretion of phenolics was induced in Fe-deficient soil and altered the microbial community in the rhizosphere [92]. Microorganisms

Soil microorganisms play a crucial role in plant growth and plant exudates. Microorganisms can affect exudation by affecting the permeability of root cells and root metabolism. Microorganisms can also absorb certain compounds in root exudates and excrete other compounds. Soil microbes can produce secondary metabolites that affect plant signaling and metabolism and can be considered as a “plant secondary genome” that provides plant hosts with microbe-derived compounds [93]. Some microbes and also some antibiotics (e.g., penicillin and polymyxin) increased the exudation of organic materials, altered cell permeability, and increased leakage [94, 95]. Soil microbes can also induce the exudation of phenolic compounds for enhancing plant Fe absorption in low-Fe availability soil [96].

4. Microbial community diversity and plant performances

4.1. Variation of microbial community in plant life cycle

Plant and rhizosphere microbial diversity varies throughout the plant life cycle. The factors influencing the composition and diversity of the microbial community can be classified as four processes: dispersal, drift, speciation, and selection [97]. For seed plants, the life cycle begins with a seed. Seed dispersal is an important ecological process. Seeds carry associated microbes that originate from their parent and the environment, thereby increasing the microbial diversity in a new environment. Recent studies have suggested that bacterial seed coatings can protect against pathogens [98]. Microbial seed epiphytes have an advantage over soil bacteria during plant colonization. Seed coating methods are a major area of research, and numerous patents have been filed (i.e., approximately 4000 results were found by a Google patent search for the key word “microbial seed coating” [99]. After seed dispersal, during seed germination, seed-bone microbes might gain a competitive advantage over other microbes to colonize after germination, and opportunistic microbes from the surrounding soil might have access to a novel niche as the plant develops. Microbial diversity and the community dynamically change throughout the plant life cycle.

4.2. Networking of plant-microbes (hub and edge microbes)

Plant microbiota forms a complex network. A wide range of studies has demonstrated that plant-associated microbes live either inside plant tissue or on the surface of plant organs such as the leaves and roots [100, 101]. Agler et al. characterized the microbiome of A. thaliana leaves [102]. Field experiments showed that both plant genotype and abiotic factors affected the microbiome composition. In addition, they observed that specific species (e.g., the plant pathogen Albugo and the fungus Dioszegia) significantly affected the microbial community structure. Agler used the term “microbial hubs” for the presence of these specific species, which were strongly interconnected with other species in the microbial network of the plants. Microbial hubs might be responsible for mediating defense signals among plants and the effectiveness of biological control agents [19]. The term “keystone species” has been proposed for the presence of a kind of hub species that would be a determinant of colonization of widely microbial taxa. These microbial hubs and keystone species have a large impact on plant performance. A number of hypothetical relationships between plant performance and microbial diversity and composition have been proposed [19].

Microbial hubs might indirectly affect other taxa by changing host performance, response, or metabolites without directly interacting with other microbes. How can the microbial hubs be identified and how can the interaction of plants and microbes be understood? The requirement of new techniques to analyze whether a microbe has successfully entered a plant, and the observation of changes in the genotypic and phenotypic expression will be an added advantage in the study of plant-microbe interactions.

5. Plant growth–promoting microbes

The soil constitutes a pool of microscopic life forms including bacteria, fungi, actinomycetes, protozoa, and algae, and of these, bacteria are by far the most common. The highest numbers of bacteria are found in the rhizosphere, the region around the plant roots, as differentiated from the bulk soil [103]. Regardless of the concentration of bacteria in the soil, the bacteria may affect a plant in one of three ways. From the perspective of the plant, the interaction between the soil bacteria and a plant may be beneficial, harmful, or neutral [104]. Plant growth-promoting bacteria (PGPB) include those that are free living, those that form specific symbiotic relationships with plants (e.g., Rhizobia spp. and Frankia spp.), bacterial endophytes that can colonize some, or a portion of a plant's interior tissues and cyanobacteria. PGPB can promote plant growth directly by facilitating the acquisition of compounds or modulating plant hormone levels and indirectly by reducing the inhibitory effect of pathogenicity and plant growth by acting as biocontrol agents [105].

5.1. PGPB and abiotic stress

In nature, all living organisms are affected by environmental factors such as abiotic stress. Some plants have internal mechanisms to cope up with such stress, while others overcome. Abiotic stress factors include water deficit, excessive water, extreme temperatures, and salinity. The association of PGPB with certain plants can help the plants combat certain abiotic stresses and prevent the plants from dying. In the past decade, bacteria belonging to different genera including Rhizobium, Bacillus, Pseudomonas, Pantoea, Paenibacillus, Burkholderia, Achromobacter, Azospirillum, Microbacterium, Methylobacterium, Variovorax, and Enterobacter have been reported to endow host plants under different abiotic stress environments [106].

5.1.1. Cold stress

Maize plants exposed to low temperatures show reduced shoot and root growth that has been attributed to severe oxidative damage induced by cold stress [107, 108]. Treatment with Pseudomonas sp. DSMZ 13134, B. amyloliquefaciens subsp. plantarum, Bacillus simplex strain R41 with micronutrients (Zn/Mn), or seaweed extracts proved to be beneficial cold stress protectant [109]. Inoculation of tomato seeds with plant growth–promoting psychrotolerant bacteria from the genera Arthrobacter, Flavobacterium, Flavimonas, Pedobacter, and Pseudomonas significantly improved plant height, root length, and membrane damage in leaf tissues as evidenced by electrolyte leakage and the malondialdehyde content [110]. A cold-tolerant PGPB Methylobacterium phyllosphaerae strain IARI-HHS2-67, isolated using a leaf imprinting method from phyllosphere of wheat (Triticum aestivum L.), showed improved survival, growth, and nutrient uptake compared to a noninoculated control at 60 days under low-temperature conditions [111]. The chilling resistance of grapevine plantlets was enhanced when inoculated with a plant growth–promoting rhizobacteria, Burkholderia phytofirmans strain PsJN. The root growth increased by 11.8- and 10.7-fold at 26 and 4°C, respectively, and plantlet biomass increased by 6- and 2.2-fold at 26 and 4°C, respectively [112].

5.1.2. Heat stress

The effects of global warming in recent years can be felt with the increase in global temperature. A thermo tolerant plant growth–promoting Pseudomonas putida strain AKMP7 was proven to be beneficial for the growth of wheat (Triticum spp.) under heat stress [113]. The bacterium significantly increased the root and shoot length and dry biomass of wheat as compared to uninoculated plants. Inoculation improved the level of cellular metabolites and reduced the activity of several antioxidant enzymes and membrane injury. Sorghum seedlings showed enhanced tolerance to increased temperature with the association of Pseudomonas sp. strain AKM-P6 [114]. Inoculation induced the biosynthesis of high-molecular-weight proteins in the leaves at elevated temperatures, reduced membrane injury, and improved the levels of cellular metabolites such as proline, chlorophyll, sugars, amino acids, and proteins.

5.1.3. Salinity

Approximately 20–50% of crop yields are lost to drought and high soil salinity [115]. The United Nations Population Fund estimates that the global human population may well reach 10 billion by 2050 ( Crop plants are very sensitive to soil salinity, and it is one of the harshest environmental factors that limits the productivity of crops. Plant-microbe associations have been found to be beneficial against abiotic salt stress in Zea mays upon coinoculation with Rhizobium, while Pseudomonas was correlated with decreased electrolyte leakage and the maintenance of leaf water content [116]. Salinity resistant Pseudomonas fluorescens, P. aeruginosa, and P. stutzeri ameliorated sodium chloride stress in tomato plants, and an increase in roots and length were observed [117]. Jha et al. demonstrated that the endophytic bacteria Pseudomonas pseudoalcaligenes induced the accumulation of higher concentrations of glycine betain-like compounds, leading to improved salinity stress tolerance in rice [118]. Dietzia natronolimnaea, a plant growth–promoting rhizobacteria, was seen to modulate a stress response gene, which led to the protection of wheat from salinity stress [119]. Staphylococcus saprophyticus ST1 and Oceanobacillus profundus Pmt2 inoculants were able to produce a biofilm and an extracellular EPS, thus helping Lens esculenta Var. Masoor-93 to cope with salt stress [120]. Salt-stressed Arabidopsis plants treated with volatile organic compounds (VOCs) from B. amyloliquefaciens GB03 showed higher biomass production and less Na+ accumulation compared to salt-stressed plants without VOC treatment [121].

5.1.4. Water stress resistance

Water scarcity constrains plant productivity, and more crop productivity is lost due to water scarcity than any other abiotic stresses [122]. Achromobacter piechaudii ARV8 reduced the production of ethylene by tomato seedlings following water stress, and ARV8 did not affect the reduction of the relative water content during water deprivation. ARV8 significantly improved the recovery of plants when watering was resumed [123]. Water stress resistance was enhanced in green gram when treated with P. fluorescens Pf1 compared to untreated plants. P. fluorescens Pf1 was also found to produce the enzyme catalase under stress conditions, which helped to detoxify the compounds accumulated in green gram during adverse conditions [124].

Heavy metals are defined as metals with a density higher than 5 g/cm3 [125]. Heavy metals cause a significant decrease in plant growth and protein content at high concentrations. The most common heavy metal contaminants are Hg, Cd, Cr, Cu, Pb, and Zn [126]. All of these elements are toxic to crop plants at high tissue concentrations. Heavy metal toxicity in plants leads to the production of reactive oxygen species that block essential functional groups of biomolecules. This reaction has been noted in Hg and Cd toxicity and causes oxidative injury in plants. Increasing concentrations of Hg (5–20 mg/kg soil) in tomato plant showed deleterious effects on survival percentage, germination, flowering, pollen viability, and reduced plant height. P. putida enhanced the Cd uptake potential of Eruca sativa and favored healthy growth under Cd stress by increasing the shoot length up to 27%, the root length up to 32%, the wet weight up to 40%, the dry weight up to 22%, and the chlorophyll content up to 26% [127]. Canola seeds inoculated with Kluyvera ascorbata SUD165 and grown under gnotobiotic conditions in the presence of high concentrations of nickel chloride were partially protected against nickel toxicity because the bacteria could lower ethylene-induced stress due to nickel toxicity [128]. Photobacterium halotolerans MELD1 facilitated the phytoprotection of Vigna Unguiculata Sesquipedalis against Hg at a concentration of 25 ppm, thus increasing productivity as well as reducing the translocation of Hg to the bean pods [121]. A plant-microbe phytoremediation system was created with the combination of vetiver grass and the functional endophytic bacterium Achromobacter xylosoxidans F3B for the removal of toluene in Ho et al. [129]. It was observed that A. xylosoxidans F3B improved the degradation of toluene in vetiver, resulting in a decrease in phytotoxicity and a 30% reduction of evapotranspiration through the leaves. Another study conducted by Ho et al. [130] observed that when A. xylosoxidans strain F3B was inoculated in A. thaliana, it helped the plant tolerate a lethal concentration of catechol and phenol and enhanced the phytoremediation and phytoprotection of the plant.

5.2. PGPB against biotic stress

Plants must withstand adverse abiotic and biotic stresses when they are sessile (Figure. 2). Biotic stress in plants mainly includes damage caused by other living organisms such as insects, bacteria, fungi, nematodes, viruses, viroids, and protists. Biotic stress by PGPR can affect plant growth in two different ways; by the direct promotion of plant growth by the production of phytohormones or by facilitating the uptake of certain nutrients [45]. The indirect promotion of plant growth occurs when PGPR lessens or prevents the deleterious effects of phytopathogens. P. fluorescens produces 2,4-diacetyl phloroglucinol, which inhibits the growth of phytopathogenic fungi [131]. Extracellular chitinase and laminarinase were produced by P. stutzeri, which caused the lysis of mycelia of F. solani, which causes root rot [132]. The endophytic B. cenocepacia 869T2 decreased the disease incidence of Fusarium wilt in treated banana plants to 3.4%, compared to 24.5% in noninoculated plants infected in a field test during a 7-month period [50]. The antibiotic Pyrrolnitrin, produced by P. fluorescens BL915 could prevent the damage from Rhizoctonia solani during the damping off of cotton plants [133].


Figure 2.

Factors affecting plant-microbe interactions.

Van Peer et al. [134] described a mechanism called “Induced Systemic Resistance” in carnation plants that were systematically protected by P. fluorescens strain WCS417r against F. oxysporum f. sp. Dianthi and by Ardebili et al. in tomato plants, in which P. fluorescens CHA0 protected against F. oxysporum f. sp. Lycopersici acted as a bio agent that induced resistance in tomato [135]. B. amyloliquefaciens strain FZB42, a plant root colonizing isolate, was seen to have the ability to stimulate plant growth and suppress plant pathogens [136]. In another study, endophytes were seen to protect cucumber plants against cucumber anthracnose induced by P. fluorescens strain 89B-61 [137] and Achromobacter sp. F2feb.44. Streptomyces sp. Zapt10, and Bacillus licheniformis AE6 were exploited to induce systemic resistance in cucumber against the foliar disease of downy mildew caused by the phytopathogen Pseudoperonospora cubensis, which enhanced yield [138].

Pest management has become an issue over time because more and more pests are becoming immune to pesticides. The global pesticide market is growing at a pace of 3.6% per year and is valued around $47 billion [139]. Development of entomopathogenic bacteria for pest management has been a new approach to handle resilient pests. Species belonging to the genera Aschersonia, Agerata, Verticillium, Sphaerostilbe, Podonectria, Myriangium, Hirsutella, and Metarhizium [140] are fungal species involved in the biological control of pests. Bacillus thuringiensis is the most well-known Bacillus species on which the efforts of the scientific community and industry have been focused [141]. Brevibacillus laterosporus Laubach action has been reported to be effective against insects such as Coleoptera [142], Lepidoptera [143], nematodes [144, 145], and phytopathogenic fungi [146].

6. Future development of application

6.1. Techniques used to understand plant microbe interaction

Plants have been an integral part of our diet since humans began to farm and were no longer nomads. Since then, the world has faced a continuous challenge to feed the ever-growing population. The excess use of fertilizer is causing eutrophication [147], and genetic engineering of plants is an expensive and tedious process. The role of microbes in plant-microbe interactions has been studied in detail during the past decade [148, 149]. The results of extensive studies suggest that the exploitation of beneficial microbes is a better strategy in the long run to increase crop yield, which will play an important role in disease dissemination and control [150]. Three types of plant-microbe interactions have been studied–symbiosis between plants and mycorrhizae [151], between plants and rhizobacteria [152], and pathogenesis [153]. Omics technologies such as transcriptomics, proteomics, and metabolomics coupled with bioinformatics have been extensively applied in plant abiotic stress studies [154]. The proteomics approach has been largely adopted to investigate the protein profiles in plants in response to abiotic stresses that might lead to the development of new strategies for improving stress tolerance [155]. Microbial metabolomics is another technique that has been used to study the set of metabolites present in microbial communities [156]. A rhizosphere metabolomics–driven approach was used in the study of plant-microbe interactions for the removal of polychlorinated biphenyls as demonstrated by Lee et al. [157].

Pathogens and their emergence have been a great threat to food security, agricultural practices, and the conservation of food species, and it has become a significant task to understand the emergence of new pathogens and their role [158]. In the past, plant pathosystems were best studied one gene at a time or one protein at a time; however, the genomic era marked the beginning of the in-depth study of plant-pathogen associations [159]. Commonly known pathogen genomes have been sequenced, and the analysis of these sequences has revealed the forces that have shaped pathogen evolution and has brought to light the unexpected aspects of pathogen biology [160, 161]. The genome scale reconstruction model (GSRM) is based on metabolic reconstructions on a genomic scale for the analysis and interpretation of metabolite concentrations under specific conditions [162]. GSRM has been successfully developed for many organisms including plants, bacteria, fungi, and animals [163165].

Various techniques to study plant-microbe interactions are sequencing, chromatography, mass spectrometry, phospholipid fatty acid (PLFA), microscopy, Fourier transform infrared spectroscopy (FTIR), nuclear magnetic resonance, and real-time PCR (RT-PCR) [166]. Further advances in the postgenomic era will pave the way for a better understanding of the interactions of endophytes, plant-pathogen, and plant immunity. Genomic tools to understand major units of the host-microbiota ecology are shown in Figure 3.


Figure 3.

Genomic tools to understand major units of the plant-microbe ecological system. Colored boxes indicate technique tools that can be used to characterize key factors for the corresponding unit. (modified after Kroll et al. [167]).

7. Conclusions

In the face of pressure from climate change, contaminated environments, and crop pathogens, agricultural material and food production are currently at risk. Plant-associated microorganisms have important consequences for host health and performance. However, efforts to utilize beneficial microbes in the field have failed to consistently improve crops. The current understanding of interactions between plants and symbiotic microbial communities, the ecological consequences of plant-associated microorganisms and plant-microbial metabolic dynamics are limited. The advent of genomic approaches has helped a great deal in the understanding of the plant-bacterial interactions, but genomic approaches are still insufficient to clearly explain the interactions between plants and pathogens [168]. Approaches using metagenomics and amplicon sequencing coupled with other omics technologies [169] and the development of databases (PHI-based) [170], and metabolomics have enhanced our understanding of plant-bacterial interactions. Plant-microbe ecological communities are affected by plant genotype and environmental factors. The difference between genotypes causes different physiological and immune responses and leads to host-specific microbial communities. Plant root exudates (i.e., sugars, amino acids, organic acids, nucleotides, flavonoids, antimicrobial compounds, and enzymes) shape specific communities, attract plant growth-promoting colonization, and pathogen infections.

In the complex microbial community, we found that specific species could significantly affect the microbial community structure. Via a systems' framework of microbial network analysis, we could identify the “hub species” and “milestone species”, which are candidate microbial assemblages for disease management. Network models of plant-associated microbiomes provide new opportunities for enhancing disease management.

7.1. Future perspective

The understanding of plant-microbe and microbe-microbe interactions will provide a helpful future perspective as a modulating microbiome for minimizing disease incidence and enhancing gross plant productivity. Further, beneficial plant-associated bacteria could act as counterparts against pathogens within the microbial ecosystem, as well as stabilize the ecosystem, enhance biodiversity, avoid pathogen outbreaks, and increase plant productivity. A well-studied plant-microbe partnership in the future will also help increase crop productivity at little expense and could, in turn, lead to another “Green Revolution”.


The authors are grateful to the National Chung Hsing University, College of Life Science. The research work has been done with the financial support by Council of Agriculture, Executive Yuan (grant 104AS-16.3.1-ST-aB) and the Ministry of Science and Technology of Taiwan (grant MOST 104-2321-B-001-060-MY3).


1 - Mendes R, Garbeva P, Raaijmakers JM. The rhizosphere microbiome: Significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiology Reviews. 2013;37(5):634-663
2 - Oldroyd GE. Speak, friend, and enter: Signalling systems that promote beneficial symbiotic associations in plants. Nature Reviews Microbiology. 2013;11(4):252-263
3 - Jones JD, Dangl JL. The plant immune system. Nature. 2006;444(7117):323-329
4 - Baetz U, Martinoia E. Root exudates: The hidden part of plant defense. Trends in Plant Science. 2014;19(2):90-98
5 - Wen F, VanEtten HD, Tsaprailis G, Hawes MC. Extracellular proteins in pea root tip and border cell exudates. Plant Physiology. 2007;143(2):773-783
6 - Faure D, Vereecke D, Leveau JH. Molecular communication in the rhizosphere. Plant and Soil. 2009;321(1-2):279-303
7 - Campbell R, Greaves M. Anatomy and community structure of the rhizosphere. The Rhizosphere. 1990:11-34
8 - Haichar FZ, Marol C, Berge O, Rangel-Castro JI, Prosser JI, Balesdent J, et al. Plant host habitat and root exudates shape soil bacterial community structure. The ISME Journal. 2008;2(12):1221-1230
9 - Lareen A, Burton F, Schäfer P. Plant root-microbe communication in shaping root microbiomes. Plant Molecular Biology. 2016;90(6):575-587
10 - Ciccazzo S, Esposito A, Rolli E, Zerbe S, Daffonchio D, Brusetti L. Different pioneer plant species select specific rhizosphere bacterial communities in a high mountain environment. SpringerPlus. 2014;3(1):391
11 - Bever JD. Soil community feedback and the coexistence of competitors: Conceptual frameworks and empirical tests. New Phytologist. 2003;157(3):465-473
12 - Bever JD, Westover KM, Antonovics J. Incorporating the soil community into plant population dynamics: The utility of the feedback approach. Journal of Ecology. 1997;85(5):561-573
13 - Alexander I, Lee S. Mycorrhizas and Ecosystem Processes in Tropical Rain Forest: Implications for Diversity. Biotic Interactions in the Tropics: Their Role in the Maintenance of Species Diversity. Cambridge University Press: New York. 2005. pp. 165-203
14 - Waller F, Mueller MJ, Pedrotti L. Piriformospora indica root colonization triggers local and systemic root responses and inhibits secondary colonization of distal roots. PloS one. 2013;8(7):e69352
15 - Wagg C, Boller B, Schneider S, Widmer F, van der Heijden MG. Intraspecific and intergenerational differences in plant–soil feedbacks. Oikos. 2015;124(8):994-1004
16 - Bever JD, Dickie IA, Facelli E, Facelli JM, Klironomos J, Moora M, et al. Rooting theories of plant community ecology in microbial interactions. Trends in Ecology & Evolution. 2010;25(8):468-478
17 - Horton MW, Bodenhausen N, Beilsmith K, Meng D, Muegge BD, Subramanian S, et al. Genome-wide association study of Arabidopsis thaliana's leaf microbial community. Nature Communications. 2014;5:5320
18 - Herrera Paredes S, Lebeis SL. Giving back to the community: microbial mechanisms of plant–soil interactions. Functional Ecology. 2016;30(7):1043-1052
19 - van der Heijden MG, Hartmann M. Networking in the plant microbiome. PLoS Biology. 2016;14(2):e1002378
20 - Garbeva P, Hordijk C, Gerards S, de Boer W. Volatile-mediated interactions between phylogenetically different soil bacteria. Frontiers in Microbiology. 2014;5:285-290
21 - Garbeva P, Hordijk C, Gerards S, De Boer W. Volatiles produced by the mycophagous soil bacterium Collimonas. FEMS Microbiology Ecology. 2014;87(3):639-649
22 - Groenhagen U, Baumgartner R, Bailly A, Gardiner A, Eberl L, Schulz S, et al. Production of bioactive volatiles by different Burkholderia ambifaria strains. Journal of Chemical Ecology. 2013;39(7):892-906
23 - Ryu C-M, Farag MA, Hu C-H, Reddy MS, Wei H-X, Paré PW, et al. Bacterial volatiles promote growth in Arabidopsis. Proceedings of the National Academy of Sciences. 2003;100(8):4927-4932
24 - Peñuelas J, Asensio D, Tholl D, Wenke K, Rosenkranz M, Piechulla B, et al. Biogenic volatile emissions from the soil. Plant, Cell & Environment. 2014;37(8):1866-1891
25 - Yi H-S, Yang JW, Ryu C-M. ISR meets SAR outside: Additive action of the endophyte Bacillus pumilus INR7 and the chemical inducer, benzothiadiazole, on induced resistance against bacterial spot in field-grown pepper. Frontiers in Plant Science. 2013;4:122
26 - Pineda A, Dicke M, Pieterse CM, Pozo MJ. Beneficial microbes in a changing environment: Are they always helping plants to deal with insects? Functional Ecology. 2013;27(3):574-586
27 - Kai M, Haustein M, Molina F, Petri A, Scholz B, Piechulla B. Bacterial volatiles and their action potential. Applied Microbiology and Biotechnology. 2009;81(6):1001-1012
28 - Boyer JS. Plant productivity and environment. Science. 1982;218(4571):443-448
29 - Bray EA, Bailey-Serres J, Weretilnyk E. Responses to abiotic stresses. Biochemistry and Molecular Biology of Plants. 2000;1158:e1203
30 - Suzuki N, Rivero RM, Shulaev V, Blumwald E, Mittler R. Abiotic and biotic stress combinations. New Phytologist. 2014;203(1):32-43
31 - Hua J. Modulation of plant immunity by light, circadian rhythm, and temperature. Current Opinion in Plant Biology. 2013;16(4):406-413
32 - Sachdev DP, Chaudhari HG, Kasture VM, Dhavale DD, Chopade BA. Isolation and characterization of indole acetic acid (IAA) producing Klebsiella pneumoniae strains from rhizosphere of wheat (Triticum aestivum) and their effect on plant growth. Indian Journal of Experimental Biology. 2009;47:993-1000
33 - Backlund P, Janetos A, Schimel D. The effects of climate change on agriculture, land resources, water resources, and biodiversity in the United States. Washington, DC: United States Climate Change Science Program. 2008
34 - Lesk C, Rowhani P, Ramankutty N. Influence of extreme weather disasters on global crop production. Nature. 2016;529(7584):84-87
35 - Ma T, Zhou C. Climate-associated changes in spring plant phenology in China. International Journal of Biometeorology. 2012;56(2):269-275
36 - Allstadt AJ, Vavrus SJ, Heglund PJ, Pidgeon AM, Thogmartin WE, Radeloff VC. Spring plant phenology and false springs in the conterminous US during the 21st century. Environmental Research Letters. 2015;10(10):104008
37 - Black T, Chen W, Barr A, Arain M, Chen Z, Nesic Z, et al. Increased carbon sequestration by a boreal deciduous forest in years with a warm spring. Geophysical Research Letters. 2000;27(9):1271-1274
38 - Dragoni D, Schmid HP, Wayson CA, Potter H, Grimmond CSB, Randolph JC. Evidence of increased net ecosystem productivity associated with a longer vegetated season in a deciduous forest in south‐central Indiana, USA. Global Change Biology. 2011;17(2):886-897
39 - Jeong SJ, Ho CH, Gim HJ, Brown ME. Phenology shifts at start vs. end of growing season in temperate vegetation over the Northern Hemisphere for the period 1982-2008. Global Change Biology. 2011;17(7):2385-2399
40 - Xia J, Wan S. Independent effects of warming and nitrogen addition on plant phenology in the Inner Mongolian steppe. Annals of Botany. 2013;111(6):1207-1217
41 - Orsenigo S, Abeli T, Rossi G, Bonasoni P, Pasquaretta C, Gandini M, et al. Effects of autumn and spring heat waves on seed germination of high mountain plants. PLoS One. 2015;10(7):e0133626
42 - Majeed A, Abbasi MK, Hameed S, Imran A, Rahim N. Isolation and characterization of plant growth-promoting rhizobacteria from wheat rhizosphere and their effect on plant growth promotion. Frontiers in Microbiology. 2015;6:198
43 - Honma M, Shimomura T. Metabolism of 1-aminocyclopropane-1-carboxylic acid. Agricultural and Biological Chemistry. 1978;42(10):1825-1831
44 - Otieno N, Lally RD, Kiwanuka S, Lloyd A, Ryan D, Germaine KJ, et al. Plant growth promotion induced by phosphate solubilizing endophytic Pseudomonas isolates. Frontiers in Microbiology. 2015;6:745
45 - Glick BR. The enhancement of plant growth by free-living bacteria. Canadian Journal of Microbiology. 1995;41(2):109-117
46 - Glick BR, Patten CL, Holguin G, Penrose D. Biochemical and genetic mechanisms used by plant growth promoting bacteria. Imperial College Press, London, UK. 1999
47 - Egamberdieva D, Jabborova D, Hashem A. Pseudomonas induces salinity tolerance in cotton (Gossypium hirsutum) and resistance to Fusarium root rot through the modulation of indole-3-acetic acid. Saudi Journal of Biological Sciences. 2015;22(6):773-779
48 - Bano A, Fatima M. Salt tolerance in Zea mays (L). following inoculation with Rhizobium and Pseudomonas. Biology and Fertility of Soils. 2009;45(4):405-413
49 - Zhang H, Kim M-S, Sun Y, Dowd SE, Shi H, Paré PW. Soil bacteria confer plant salt tolerance by tissue-specific regulation of the sodium transporter HKT1. Molecular Plant-Microbe Interactions. 2008;21(6):737-744
50 - Ho Y-N, Chiang H-M, Chao C-P, Su C-C, Hsu H-F, Guo C-t, et al. In planta biocontrol of soilborne Fusarium wilt of banana through a plant endophytic bacterium, Burkholderia cenocepacia 869T2. Plant and Soil. 2015;387(1-2):295-306
51 - Prashar P, Kapoor N, Sachdeva S. Biocontrol of plant pathogens using plant growth promoting bacteria. In: Sustainable Agriculture Reviews: Springer Netherlands. 2013;12:319-360
52 - Chesson P. Mechanisms of maintenance of species diversity. Annual Review of Ecology and Systematics. 2000;31(1):343-366
53 - Tilman D. Resource Competition and Community Structure. Princeton University Press, Princeton, New Jersey, U.S.A. 1982
54 - Chase JM, Abrams PA, Grover JP, Diehl S, Chesson P, Holt RD, et al. The interaction between predation and competition: A review and synthesis. Ecology Letters. 2002;5(2):302-315
55 - O’Connor PJ, Smith SE, Smith FA. Arbuscular mycorrhizas influence plant diversity and community structure in a semiarid herbland. New Phytologist. 2002;154(1):209-218
56 - Reynolds HL, Packer A, Bever JD, Clay K. Grassroots ecology: Plant–microbe–soil interactions as drivers of plant community structure and dynamics. Ecology. 2003;84(9):2281-2291
57 - Simard SW, Durall DM. Mycorrhizal networks: A review of their extent, function, and importance. Canadian Journal of Botany. 2004;82(8):1140-1165
58 - Pietikäinen A, KYTÖVIITA MM. Defoliation changes mycorrhizal benefit and competitive interactions between seedlings and adult plants. Journal of Ecology. 2007;95(4):639-647
59 - Mitchell CE, Agrawal AA, Bever JD, Gilbert GS, Hufbauer RA, Klironomos JN, et al. Biotic interactions and plant invasions. Ecology Letters. 2006;9(6):726-740
60 - Stinson KA, Campbell SA, Powell JR, Wolfe BE, Callaway RM, Thelen GC, et al. Invasive plant suppresses the growth of native tree seedlings by disrupting belowground mutualisms. PLoS Biology. 2006;4(5):e140
61 - Vogelsang KM, Bever JD. Mycorrhizal densities decline in association with nonnative plants and contribute to plant invasion. Ecology. 2009;90(2):399-407
62 - Dickie IA, Schnitzer SA, Reich PB, Hobbie SE. Spatially disjunct effects of co‐occurring competition and facilitation. Ecology Letters. 2005;8(11):1191-1200
63 - Reinhart KO, Callaway RM. Soil biota and invasive plants. New Phytologist. 2006;170(3):445-457
64 - Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, et al. Defining the core Arabidopsis thaliana root microbiome. Nature. 2012;488(7409):86-90
65 - Peiffer JA, Spor A, Koren O, Jin Z, Tringe SG, Dangl JL, et al. Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proceedings of the National Academy of Sciences. 2013;110(16):6548-6553
66 - Bokulich NA, Thorngate JH, Richardson PM, Mills DA. Microbial biogeography of wine grapes is conditioned by cultivar, vintage, and climate. Proceedings of the National Academy of Sciences. 2014;111(1):E139-E148
67 - Bodenhausen N, Bortfeld-Miller M, Ackermann M, Vorholt JA. A synthetic community approach reveals plant genotypes affecting the phyllosphere microbiota. PLoS Genetics. 2014;10(4):e1004283
68 - Consortium HMP. Structure, function and diversity of the healthy human microbiome. Nature. 2012;486(7402):207-214
69 - Benson AK, Kelly SA, Legge R, Ma F, Low SJ, Kim J, et al. Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors. Proceedings of the National Academy of Sciences. 2010;107(44):18933-18938
70 - Chaston JM, Dobson AJ, Newell PD, Douglas AE. Host genetic control of the microbiota mediates the Drosophila nutritional phenotype. Applied and Environmental Microbiology. 2016;82(2):671-679
71 - Hartmann A, Rothballer M, Schmid M. Lorenz Hiltner, a pioneer in rhizosphere microbial ecology and soil bacteriology research. Plant and Soil. 2008;312(1-2):7-14
72 - Lugtenberg B, Kamilova F. Plant-growth-promoting rhizobacteria. Annual Review of Microbiology. 2009;63:541-556
73 - Rovira AD. Plant root exudates. The Botanical Review. 1969;35(1):35-57
74 - Kirk JL, Klironomos JN, Lee H, Trevors JT. The effects of perennial ryegrass and alfalfa on microbial abundance and diversity in petroleum contaminated soil. Environmental Pollution. 2005;133(3):455-465
75 - İnceoğlu Ö, van Overbeek LS, Salles JF, van Elsas JD. Normal operating range of bacterial communities in soil used for potato cropping. Applied and Environmental Microbiology. 2013;79(4):1160-1170
76 - Li X, Zhang T, Wang X, Hua K, Zhao L, Han Z. The composition of root exudates from two different resistant peanut cultivars and their effects on the growth of soil-borne pathogen. International Journal of Biological Sciences. 2013;9(2):164-173
77 - Yuan J, Zhang N, Huang Q, Raza W, Li R, Vivanco JM, et al. Organic acids from root exudates of banana help root colonization of PGPR strain Bacillus amyloliquefaciens NJN-6. Scientific Reports. 2015;5:13438
78 - Bacilio-Jiménez M, Aguilar-Flores S, Ventura-Zapata E, Pérez-Campos E, Bouquelet S, Zenteno E. Chemical characterization of root exudates from rice (Oryza sativa) and their effects on the chemotactic response of endophytic bacteria. Plant and Soil. 2003;249(2):271-277
79 - Chen HY, Huh JH, Yu YC, Ho LH, Chen LQ, Tholl D, et al. The Arabidopsis vacuolar sugar transporter SWEET2 limits carbon sequestration from roots and restricts Pythium infection. The Plant Journal. 2015;83(6):1046-1058
80 - VanEtten HD, Mansfield JW, Bailey JA, Farmer EE. Two classes of plant antibiotics: Phytoalexins versus "Phytoanticipins". The Plant Cell. 1994;6(9):1191
81 - Vaughan MM, Wang Q, Webster FX, Kiemle D, Hong YJ, Tantillo DJ, et al. Formation of the unusual semivolatile diterpene rhizathalene by the Arabidopsis class I terpene synthase TPS08 in the root stele is involved in defense against belowground herbivory. The Plant Cell. 2013;25(3):1108-1125
82 - Lanoue A, Burlat V, Henkes GJ, Koch I, Schurr U, Röse US. De novo biosynthesis of defense root exudates in response to Fusarium attack in barley. New Phytologist. 2010;185(2):577-588
83 - Vuković R, Bauer N, Ćurković-Perica M. Genetic elicitation by inducible expression of β-cryptogein stimulates secretion of phenolics from Coleus blumei hairy roots. Plant Science. 2013;199:18-28
84 - Bais HP, Walker TS, Schweizer HP, Vivanco JM. Root specific elicitation and antimicrobial activity of rosmarinic acid in hairy root cultures of Ocimum basilicum. Plant Physiology and Biochemistry. 2002;40(11):983-995
85 - Toyomasu T, Kagahara T, Okada K, Koga J, Hasegawa M, Mitsuhashi W, et al. Diterpene phytoalexins are biosynthesized in and exuded from the roots of rice seedlings. Bioscience, Biotechnology, and Biochemistry. 2008;72(2):562-567
86 - Badri DV, Chaparro JM, Zhang R, Shen Q, Vivanco JM. Application of natural blends of phytochemicals derived from the root exudates of Arabidopsis to the soil reveal that phenolic-related compounds predominantly modulate the soil microbiome. Journal of Biological Chemistry. 2013;288(7):4502-4512
87 - Husain S, McKeen W. Interactions between strawberry roots and Rhizoctonia fragariae. Phytopathology. 1963;53(5):541-545
88 - Katznelson H, Rouatt J, Payne T. The liberation of amino acids and reducing compounds by plant roots. Plant and Soil. 1955;7(1):35-48
89 - Bowen G. Nutrient status effects on loss of amides and amino acids from pine roots. Plant and Soil. 1969;30(1):139-142
90 - Toljander JF, Santos-González JC, Tehler A, Finlay RD. Community analysis of arbuscular mycorrhizal fungi and bacteria in the maize mycorrhizosphere in a long-term fertilization trial. FEMS Microbiology Ecology. 2008;65(2):323-338
91 - Dumbrell AJ, Nelson M, Helgason T, Dytham C, Fitter AH. Relative roles of niche and neutral processes in structuring a soil microbial community. The ISME Journal. 2010;4(3):337-345
92 - Jin CW, Ye YQ, Zheng SJ. An underground tale: contribution of microbial activity to plant iron acquisition via ecological processes. Annals of Botany. 2014;113(1):7-18
93 - Rout ME, Southworth D. The root microbiome influences scales from molecules to ecosystems: The unseen majority. American Journal of Botany. 2013;100(9):1689-1691
94 - Harmsen G, Jager G. Determination of the Quantity of Carbon and Nitrogen in the Rhizosphere of Young Plants. In: Doeksen J, van der Drift J, editors. Soil Organisms. Amsterdam: North Holland; 1963;245-251
95 - Norman AG. Microbial products affecting root development. Transactions of the 7th Congress Wisconsin International Soil Science Society; 1960;2:531-536
96 - Pii Y, Mimmo T, Tomasi N, Terzano R, Cesco S, Crecchio C. Microbial interactions in the rhizosphere: Beneficial influences of plant growth-promoting rhizobacteria on nutrient acquisition process. A review. Biology and Fertility of Soils. 2015;51(4):403-415
97 - Vellend M, Agrawal A. Conceptual synthesis in community ecology. The Quarterly Review of Biology. 2010;85(2):183-206
98 - Hartmann M, Lee S, Hallam SJ, Mohn WW. Bacterial, archaeal and eukaryal community structures throughout soil horizons of harvested and naturally disturbed forest stands. Environmental Microbiology. 2009;11(12):3045-3062
99 - Smith P. Why Tiny Microbes Mean Big Things for Farming. National Geographic. 2014. Available from: http://news/ nationalgeographic com/news/2014/09/140918-soil-bacteria-microbe-farming-technology-ngfood
100 - Berendsen RL, Pieterse CM, Bakker PA. The rhizosphere microbiome and plant health. Trends in Plant Science. 2012;17(8):478-486
101 - Bulgarelli D, Rott M, Schlaeppi K, van Themaat EVL, Ahmadinejad N, Assenza F, et al. Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature. 2012;488(7409):91-95
102 - Agler MT, Ruhe J, Kroll S, Morhenn C, Kim S-T, Weigel D, et al. Microbial hub taxa link host and abiotic factors to plant microbiome variation. PLoS Biology. 2016;14(1):e1002352
103 - Foster R. Microenvironments of soil microorganisms. Biology and Fertility of Soils. 1988;6(3):189-203
104 - Lynch, J.M. The Rhizosphere. John Wiley & Sons, Chichester. 1990
105 - Glick BR. Plant growth-promoting bacteria: Mechanisms and applications. Scientifica. 2012;2012:1-15
106 - Grover M, Ali SZ, Sandhya V, Rasul A, Venkateswarlu B. Role of microorganisms in adaptation of agriculture crops to abiotic stresses. World Journal of Microbiology and Biotechnology. 2011;27(5):1231-1240
107 - Saeidnejad AH, Pouramir F, Naghizadeh M. Improving chilling tolerance of maize seedlings under cold conditions by spermine application. Notulae Scientia Biologicae. 2012;4(3):110
108 - Baek K-H, Skinner DZ. Production of reactive oxygen species by freezing stress and the protective roles of antioxidant enzymes in plants. Journal of Agricultural Chemistry and Environment. 2012;1:34-40
109 - Bradáčová K, Weber NF, Morad-Talab N, Asim M, Imran M, Weinmann M, et al. Micronutrients (Zn/Mn), seaweed extracts, and plant growth-promoting bacteria as cold-stress protectants in maize. Chemical and Biological Technologies in Agriculture. 2016;3(1):19
110 - Subramanian P, Kim K, Krishnamoorthy R, Mageswari A, Selvakumar G, Sa T. Cold stress tolerance in psychrotolerant soil bacteria and their conferred chilling resistance in tomato (Solanum lycopersicum Mill.) under low temperatures. PloS One. 2016;11(8):e0161592
111 - Verma P, Yadav AN, Khannam KS, Panjiar N, Kumar S, Saxena AK, et al. Assessment of genetic diversity and plant growth promoting attributes of psychrotolerant bacteria allied with wheat (Triticum aestivum) from the northern hills zone of India. Annals of Microbiology. 2015;65(4):1885-1899
112 - Barka EA, Nowak J, Clément C. Enhancement of chilling resistance of inoculated grapevine plantlets with a plant growth-promoting rhizobacterium, Burkholderia phytofirmans strain PsJN. Applied and Environmental Microbiology. 2006;72(11):7246-7252
113 - Ali SZ, Sandhya V, Grover M, Linga VR, Bandi V. Effect of inoculation with a thermotolerant plant growth promoting Pseudomonas putida strain AKMP7 on growth of wheat (Triticum spp.) under heat stress. Journal of Plant Interactions. 2011;6(4):239-246
114 - Ali SZ, Sandhya V, Grover M, Kishore N, Rao LV, Venkateswarlu B. Pseudomonas sp. strain AKM-P6 enhances tolerance of sorghum seedlings to elevated temperatures. Biology and Fertility of Soils. 2009;46(1):45-55
115 - Shahbaz M, Ashraf M. Improving salinity tolerance in cereals. Critical Reviews in Plant Sciences. 2013;32(4):237-249
116 - Shekar CC, Sammaiah D, Shasthree T, Reddy KJ. Effect of mercury on tomato growth and yield attributes. International Journal of Pharma and Bio Sciences. 2011;2(2):B358-B364
117 - Tank N, Saraf M. Salinity-resistant plant growth promoting rhizobacteria ameliorates sodium chloride stress on tomato plants. Journal of Plant Interactions. 2010;5(1):51-58
118 - Jha Y, Subramanian R, Patel S. Combination of endophytic and rhizospheric plant growth promoting rhizobacteria in Oryza sativa shows higher accumulation of osmoprotectant against saline stress. Acta Physiologiae Plantarum. 2011;33(3):797-802
119 - Bharti N, Pandey SS, Barnawal D, Patel VK, Kalra A. Plant growth promoting rhizobacteria Dietzia natronolimnaea modulates the expression of stress responsive genes providing protection of wheat from salinity stress. Scientific Reports 2016;6
120 - Qurashi AW, Sabri AN. Osmoadaptation and plant growth promotion by salt tolerant bacteria under salt stress. African Journal of Microbiology Research. 2011;5(21):3546-3554
121 - Mathew DC, Ho Y-N, Gicana RG, Mathew GM, Chien M-C, Huang C-C. A rhizosphere-associated symbiont, Photobacterium spp. strain MELD1, and its targeted synergistic activity for phytoprotection against mercury. PloS One. 2015;10(3):e0121178
122 - Farooq M, Wahid A, Kobayashi N, Fujita D, Basra S. Plant drought stress: effects, mechanisms and management. In: Sustainable Agriculture. Springer Netherlands. 2009;153-188
123 - Mayak S, Tirosh T, Glick BR. Plant growth-promoting bacteria that confer resistance to water stress in tomatoes and peppers. Plant Science. 2004;166(2):525-530
124 - Saravanakumar D, Kavino M, Raguchander T, Subbian P, Samiyappan R. Plant growth promoting bacteria enhance water stress resistance in green gram plants. Acta Physiologiae Plantarum. 2011;33(1):203-209
125 - Weast RC, Astle MJ, Beyer WH. CRC handbook of chemistry and Physics. CRC Press: Boca Raton, FL; 1988
126 - Lasat M. Phytoextraction of metals from contaminated soil: A review of plant/soil/metal interaction and assessment of pertinent agronomic issues. Journal of Hazardous Substance Research. 2000;2(5):1-25
127 - Kamran MA, Syed JH, Eqani SAMAS, Munis MFH, Chaudhary HJ. Effect of plant growth-promoting rhizobacteria inoculation on cadmium (Cd) uptake by Eruca sativa. Environmental Science and Pollution Research. 2015;22(12):9275-9283
128 - Burd GI, Dixon DG, Glick BR. A plant growth-promoting bacterium that decreases nickel toxicity in seedlings. Applied and Environmental Microbiology. 1998;64(10):3663-3668
129 - Ho Y-N, Hsieh J-L, Huang C-C. Construction of a plant–microbe phytoremediation system: Combination of vetiver grass with a functional endophytic bacterium, Achromobacter xylosoxidans F3B, for aromatic pollutants removal. Bioresource Technology 2013;145:43-47
130 - Ho Y-N, Mathew DC, Hsiao S-C, Shih C-H, Chien M-F, Chiang H-M, et al. Selection and application of endophytic bacterium Achromobacter xylosoxidans strain F3B for improving phytoremediation of phenolic pollutants. Journal of Hazardous Materials. 2012;219:43-49
131 - Keel C, Schnider U, Maurhofer M, Voisard C, Laville J, Burger U, et al. Suppression of root diseases by Pseudomonas fluorescens CHA0: importance of the bacterial secondary metabolite 2, 4-diacetylphloroglucinol. Molecular Plant-Microbe Interactions.1992;5(1):4-13
132 - Lim H-S, Kim Y-S, Kim S-D. Pseudomonas stutzeri YPL-1 genetic transformation and antifungal mechanism against Fusarium solani, an agent of plant root rot. Applied and Environmental Microbiology. 1991;57(2):510-516
133 - Hill D, Stein J, Torkewitz N, Morse A, Howell C, Pachlatko J, et al. Cloning of genes involved in the synthesis of pyrrolnitrin from Pseudomonas fluorescens and role of pyrrolnitrin synthesis in biological control of plant disease. Applied and Environmental Microbiology. 1994;60(1):78-85
134 - Van Peer R, Niemann G, Schippers B. Induced resistance and phytoalexin accumulation in biological control of Fusarium wilt of carnation by Pseudomonas sp. strain WCS 417 r. Phytopathology. 1991;81(7):728-734
135 - Ardebili ZO, Ardebili NO, Hamdi SMM. Physiological effects of Pseudomonas fluorescens CHA0 on tomato (Lycopersicon esculentum Mill.) plants and its possible impact on Fusarium oxysporum f. sp. lycopersici. Australian Journal of Crop Science. 2011;5(12):1631
136 - Idriss EE, Makarewicz O, Farouk A, Rosner K, Greiner R, Bochow H, et al. Extracellular phytase activity of Bacillus amyloliquefaciens FZB45 contributes to its plant-growth-promoting effecta. Microbiology. 2002;148(7):2097-2109
137 - Kloepper JW, Ryu C-M. Bacterial endophytes as elicitors of induced systemic resistance. In: Microbial Root Endophytes. Springer Berlin Heidelberg, 2006;9:33-52
138 - Sen K, Sengupta C, Saha J. PGPR consortium alleviating downy mildew of cucumber. International journal of plant, animal and environmental sciences. 2014;4(4):150-159
139 - Lehr P. Biopesticides: The Global Market. Report No: CHM029C. Wellesley, Massachusetts: BCC Research; 2010
140 - Fawcett H. Fungus and bacterial diseases of insects as factors in biological control. The Botanical Review. 1944;10(6):327
141 - Roh JY, Choi JY, Li MS, Jin BR, Je YH. Bacillus thuringiensis as a specific, safe, and effective tool for insect pest control. Journal of Microbiology and Biotechnology. 2007;17(4):547
142 - Boets A, Arnaut G, Van Rie J, Damme N. Toxins. Google Patents; 2004
143 - De Oliveira EJ, Rabinovitch L, Monnerat RG, Passos LKJ, Zahner V. Molecular characterization of Brevibacillus laterosporus and its potential use in biological control. Applied and Environmental Microbiology. 2004;70(11):6657-6664
144 - Bone LW, Singer S. Control of parasitic nematode ova/larvae with a Bacillus laterosporus. Google Patents; 1991
145 - Singer S. The utility of strains of morphological group II Bacillus. Advances in Applied Microbiology. 1996;42:219-261
146 - Saikia R, Gogoi D, Mazumder S, Yadav A, Sarma R, Bora T, et al. Brevibacillus laterosporus strain BPM3, a potential biocontrol agent isolated from a natural hot water spring of Assam, India. Microbiological Research 2011;166(3):216-225
147 - Smith VH, Tilman GD, Nekola JC. Eutrophication: Impacts of excess nutrient inputs on freshwater, marine, and terrestrial ecosystems. Environmental Pollution. 1999;100(1):179-196
148 - Vorholt JA. Microbial life in the phyllosphere. Nature Reviews Microbiology. 2012;10(12):828-840
149 - Bulgarelli D, Schlaeppi K, Spaepen S, van Themaat EVL, Schulze-Lefert P. Structure and functions of the bacterial microbiota of plants. Annual Review of Plant Biology. 2013;64:807-838
150 - Reid A. Microbes helping to improve crop productivity. Microbe. 2011;6(10):435
151 - Denison RF, Kiers ET. Life histories of symbiotic rhizobia and mycorrhizal fungi. Current Biology. 2011;21(18):R775-R785
152 - Vejan P, Abdullah R, Khadiran T, Ismail S, Nasrulhaq Boyce A. Role of plant growth promoting rhizobacteria in agricultural sustainability—A review. Molecules. 2016;21(5):573
153 - de Souza EM, Granada CE, Sperotto RA. Plant pathogens affecting the establishment of plant-symbiont interaction. Frontiers in Plant Science 2016;7
154 - Soda N, Wallace S, Karan R. Omics study for abiotic stress responses in plants. Advances in Plants & Agriculture Research. 2015;2(1):00037
155 - Gupta B, Saha J, Sengupta A, Gupta K. Plant Abiotic Stress: ‘Omics’ Approach. Journal of Plant Biochemistry and Biotechnology. 2013;1:e108
156 - Barkal LJ, Theberge AB, Guo C-J, Spraker J, Rappert L, Berthier J, et al. Microbial metabolomics in open microscale platforms. Nature Communications 2016;7:10610
157 - Narasimhan K, Basheer C, Bajic VB, Swarup S. Enhancement of plant-microbe interactions using a rhizosphere metabolomics-driven approach and its application in the removal of polychlorinated biphenyls. Plant Physiology. 2003;132(1):146-153
158 - Thynne E, McDonald MC, Solomon PS. Phytopathogen emergence in the genomics era. Trends in Plant Science. 2015;20(4):246-255
159 - Schneider DJ, Collmer A. Studying plant-pathogen interactions in the genomics era: Beyond molecular Koch's postulates to systems biology. Annual Review of Phytopathology. 2010;48:457-479
160 - Salanoubat M, Genin S, Artiguenave F, Gouzy J, Mangenot S, Arlat M, et al. Genome sequence of the plant pathogen Ralstonia solanacearum. Nature. 2002;415(6871):497-502
161 - Simpson AJG, Reinach F, Arruda P, Abreu F, Acencio M, Alvarenga R, et al. The genome sequence of the plant pathogen Xylella fastidiosa. Nature. 2000;406(6792):151-157
162 - Durot M, Bourguignon P-Y, Schachter V. Genome-scale models of bacterial metabolism: Reconstruction and applications. FEMS Microbiology Reviews. 2009;33(1):164-190
163 - Magnúsdóttir S, Heinken A, Kutt L, Ravcheev DA, Bauer E, Noronha A, et al. Generation of genome-scale metabolic reconstructions for 773 members of the human gut microbiota. Nature Biotechnology. 2017;35:81-89
164 - Nogales J, Palsson BØ, Thiele I. A genome-scale metabolic reconstruction of Pseudomonas putida KT2440: iJN746 as a cell factory. BMC Systems Biology. 2008;2(1):79
165 - Timm CM, Campbell AG, Utturkar SM, Jun S-R, Parales RE, Tan WA, et al. Metabolic functions of Pseudomonas fluorescens strains from Populus deltoides depend on rhizosphere or endosphere isolation compartment. Frontiers in Microbiology 2015;6:1118
166 - Wu CH, Bernard SM, Andersen GL, Chen W. Developing microbe–plant interactions for applications in plant‐growth promotion and disease control, production of useful compounds, remediation and carbon sequestration. Microbial Biotechnology. 2009;2(4):428-440
167 - Kroll S, Agler MT, Kemen E. Genomic dissection of host–microbe and microbe–microbe interactions for advanced plant breeding. Current Opinion in Plant Biology. 2017;36:71-78
168 - Bender CL. The post-genomic era: New approaches for studying bacterial diseases of plants. Australasian Plant Pathology. 2005;34(4):471-474
169 - Quirino B, Candido E, Campos P, Franco O, Krüger R. Proteomic approaches to study plant–pathogen interactions. Phytochemistry. 2010;71(4):351-362
170 - Winnenburg R, Urban M, Beacham A, Baldwin TK, Holland S, Lindeberg M, et al. PHI-base update: additions to the pathogen–host interaction database. Nucleic Acids Research. 2008;36(Suppl 1):D572–D576