Abstract
Due to the increasing demand for the use of agricultural products, along with new and more restrictive policies regarding the application of fertilizers, the search for alternative ways to increase crop production in a responsible way with respect to the environment is necessary, especially considering that the use of nitrogen-based fertilizers are both very costly and polluting. As regards this chapter focuses on the production of cereals because they represent the most important source of total food consumption, particularly in developing countries with diets based mainly on these types of crops. One possible solution is the application of microbial-based fertilizers (biofertilizers) to enhance crop production. In the literature, bacteria that not only promote plant growth but are also capable of colonizing the interior of plants, known as endophytic bacteria, have been described. Several studies have characterized the different ways of locating these bacteria inside plants, as well as the effects of their colonization. In addition, some entophytes are able to fix nitrogen for their hosts, produce phytohormones (auxins, cytokinins, gibberellins), degrade harmful compounds, decrease the effects of saline stress and improve seed germination, among others benefits. Several companies have attempted to exploit the positive effects caused by endophytic bacteria on their hosts by developing different products, used worldwide (e.g. Inogro®, QuickRoots®), that are based on these types of bacteria. The application of these products occurs despite the governing legislation of the different countries where it is used, and there are usually no specific regulations controlling the process of production, security and marketing of these biofertilizers.
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7.1 Introduction
The United Nations Food and Agriculture Organization (FAO) estimates that the total demand for agricultural products will be ~60% higher in 2030 than it is today. Remarkably, developing countries comprise ~85% of the global food demand. For over half a century, the world population has relied on modern agriculture for enhancing crop yields. Cereals are the most important source of total food consumption, especially in developing countries, where diets are based mainly on these types of crops. World cereal production has significantly increased during the last two decades, and during this time, the grain yields of several cereal crops has increased to ~122% all over the world, responding to this ever-increasing demand for food. However, this trend in grain production cannot be maintained due to the decrease in the number of hectares of cultivable land, which has been dedicated to rapidly growing urbanization (Mia and Shamsuddin 2010; Meena et al. 2013a, 2016a; Bahadur et al. 2014; Maurya et al. 2014; Jat et al. 2015; Kumar et al. 2015, 2016b; Ahmad et al. 2016; Parewa et al. 2014; Prakash and Verma 2016).
One of the most important factors in obtaining high-yield cereal crops is the application of nitrogen-based fertilizers, which is why farmers apply high amounts of these types of fertilizers that are both very costly and hazardous to the environment, especially when used indiscriminately. In addition, ~50% of applied N-fertilizers are somehow lost through different bio-geological processes, which not only represent an economical loss but also pollute the environment (Ladha et al. 1998). Thus, crop scientists all over the world are facing this alarming situation and searching for cost-effective and biosafe alternatives (Jeyabal and Kupuswamy 2001). With this aim in mind, the scientific community needs to investigate ways to increase crop production and at the same time to avoid the problems associated with the overuse of fertilizers (García-Fraile et al. 2015).
Therefore, it is necessary to enhance crop productivity in a sustainable manner, which does not exacerbate the problem of pollution. Furthermore, farmers need to be open to the idea of using other kinds of fertilizing schemes, such as biofertilizers. The application of plant growth-promoting bacteria, such as those used as biofertilizers, for sustainable agriculture may provide a solution to this problem (Meena et al. 2015a, b, f, 2016b; Priyadharsini and Muthukumar 2016; Kumar et al. 2016a, 2017; Raghavendra et al. 2016; Zahedi 2016; Rawat et al. 2016; Dotaniya et al. 2016; Jaiswal et al. 2016; Jha and Subramanian 2016).
The development of a proper biofertilizer requires: (i) isolation and selection of bacteria, (ii) effective carrier selection, (iii) observation of modes of entry of endophytic bacteria into the host plant, (iv) determining the mechanisms involved in plant growth promotion, (v) verifying the effectiveness of inoculants, and (vi) to check the biosafety of these strains for the environment and health (Berg and Smalla 2009; Chauhan et al. 2015). In addition, it is necessary to understand the nature of the microorganisms before their use as biofertilizers in order to utilize only microorganisms safe for human health; this includes not only the consumer or end user but also those handling the biofertilizers during their production (Meena et al. 2017). Strains belonging to the genera Azospirillum, Gluconacetobacter, Bacillus or Azotobacter, among others, are currently commercialized as biofertilizers for nonlegumes without any adverse effects being reported to date (Bashan 2014). In this chapter, we revise the available data regarding plant growth promotion by bacterial endophytes isolated from different cereals and focus on their possible use in biofertilization. Moreover, we will specifically focus on the culturomics approach, analysing the role of cultivable microorganisms since they are essential for agriculture and very important in the movement and availability of the minerals required for plant growth (Yasin et al. 2016; Meena et al. 2016c, d; Saha et al. 2016a; Yadav and Sidhu 2016; Das and Pradhan 2016; Dominguez-Nunez et al. 2016). Ultimately, these microorganisms are essential for the partial or total reduction of synthetic fertilizers (Malusá and Vassilev 2014).
7.2 Endophytic Bacteria: Definition, Importance and Mechanisms of Action
For many years, scientists from all around the world have developed and published several studies reporting on the great potential that some bacterial strains have in the promotion of plant growth, namely, plant growth-promoting bacteria or PGPB, through several mechanisms (García-Fraile et al. 2015). Many of these bacteria are endophytes, which are defined as bacteria living inside a plant tissue (“endo”, inside; “phyte”, plant). Some of them can influence plant growth and pertain to a subset of the endophytic population called PGPBEs (Gaiero et al. 2013).The potential of PGPBEs to improve plant health has led to a great number of studies examining their applied use as inoculants, primarily in agricultural crops (Kuklinsky-Sobral et al. 2004; García-Fraile et al. 2015). Because of these qualities, PGPBEs are important candidates to be used as inoculants to reduce the need for chemicals, such as pesticides and fertilizers, becoming important in the development of sustainable agricultural practices (Saha et al. 2016b; Verma et al. 2014, 2015a, b; Meena et al. 2014a, 2015e; Sharma et al. 2016; Bahadur et al. 2016b).
In general, endophytes are more likely to show plant growth-promoting effects than bacteria exclusively colonizing the rhizosphere (Conn et al. 1997; Chanway et al. 2000). Also, some endophytes are better colonizers and are capable of outcompeting others present in the surroundings (Verma et al. 2004).Therefore, endophytes (single or forming consortia) found in a particular plant species can be considered as more competent and suitable for their reinoculation in the same plant crop from which they were isolated.
7.2.1 Plant Root Colonization
Colonization and infection processes in cereals by endophytic bacteria differ from leguminous plants. The infection process can take place at cracks, such as those occurring at root emergence sites or those created by deleterious microorganisms, as well as through cells situated at root tips (Reinhold-Hurek and Hurek 2011). To successfully colonize the host plant, endophytic bacteria have specific traits, such as flagella, cell wall degrading enzymes (CWDEs) or twitching motility, among others (Lodewychx et al. 2002). Due to endophytic bacteria being able to penetrate into the root of the host, they are better candidates than the bacteria found in the rhizosphere for use as PGPB in plants (Meena et al. 2013b, 2015c, 2016e; Shrivastava et al. 2016; Velazquez et al. 2016; Bahadur et al. 2016a; Masood and Bano 2016; Teotia et al. 2016).
Active and passive mechanisms have been reported for the translocation processes of endophytic bacteria inside their plant hosts, allowing them to progress from the rhizoplane to the cortex of the root system (Fig. 7.1). Once a bacterium reaches the root cortical zone, a barrier such as the endodermis can block further colonization of the inner tissues; only few bacteria are able to pass through the endodermis (Gregory 2006). It is likely that endophytes able to pass through the endodermis can secrete CWDEs allowing them to continue colonization through the inner roots (James et al. 2002). Alternatively, some bacteria may passively enter as a portion of this endodermal cell layer is often disrupted, such as during the growth of secondary roots, which derive from the pericycle situated just below the endodermis barrier (Gregory 2006). Under natural conditions, some deleterious bacteria can also disrupt the endodermis, allowing endophytic bacteria at the same time to pass into the central cylinder to further reach the root xylem vessels of their hosts (Compant et al. 2010).
For example, Azorhizobium caulinodans are able to enter rice roots at emerging lateral roots (lateral root cracks) by crack entry and move into intercellular space within the cortical cell layer or roots (Goormachtig et al. 2004). Lateral root crack colonization of rice was also observed with similar frequency following inoculation with Azospirillum brasilense, where colonization was stimulated by naringenin and other flavonoids (Jain and Gupta 2003).
In addition, some strains may have the ability to infect rice root tissues via root hairs located at the emerging lateral roots and to spread extensively throughout the rice root (Ladha et al. 1996; Francine et al. 2007). Some naturally occurring rhizobia can invade the emerging lateral roots of rice, wheat, maize and oilseed rape (Cocking 2003; Bashan 2014; Yanni et al. 2016).
7.2.2 How to Localize Endophytic Bacteria Inside Plants
Colonization by these bacterial endophytes can be confirmed through multiple methods. These methods include fluorescent-tagging, immunological detection, fluorescence/confocal microscopy or scanning and transmission electron microscopy. Bacterial entry routes into the host plant have been traced and scored in many cases by using these approaches (Prayitno et al. 1999; Chaintreuil et al. 2000; Verma et al. 2004; Perrine-Walker et al. 2007a). Otherwise, specific primers could be of use to analyse bacteria inside plants (Hartmann et al. 2000).
Other authors like Bulgarelli et al. (2015) combine 16S rRNA gene profiling and shotgun metagenomic analysis to investigate the structure and function of the bacterial root microbiota in wild and domesticated barley (Hordeum vulgare). Moreover, Stets et al. (2013) used matrix-assisted laser desorption ionization time-of-flight mass spectrometry (MALDI-TOF MS) to assess the diversity of wheat-associated bacterial isolates. Also, they validated their results by using 16S rRNA gene sequence analyses, which correlated with the clusterization of the mass spectra profiles. The results obtained demonstrated that this technique had the potential to classify bacteria at different levels.
Several authors have previously demonstrated the potential of in situ visualization of specific gfp-tagged bacteria in plant roots (Chelius and Triplett 2000; Ramos et al. 2002). GFP-tagged B. subtilis CB-R05 strain was studied to monitor its interaction in Oryza sativa under axenic conditions by using confocal laser scanning microscope (CLSM). CB-R05 cells penetrate through the rhizoplane, especially in the elongation and differentiation zones of the rice roots and, also, are able to colonize it intracellularly (Ji et al. 2014).
Moreover, Chi et al. (2005) examined the colonization and infection of rice plant tissues by different species of gfp-tagged rhizobia and their influence on the growth physiology of rice. Other studies aim to evaluate the potential of Rhizobium sp. to colonize the roots of a wide variety of cereals by tagging bacteria with fluorescent proteins (Mitra 2014). Results derived from these studies showed that in the first days of the rhizobia-plant root interaction, bacteria predominantly colonized the elongation zone of the roots, the root surfaces and, interestingly, root hairs. Also, other studies reported the inoculation of rice seedlings with a GFP-tagged strain of Rhizobium, displaying some phenotypes similar to those seen in the infection process that occurs in leguminous plants. Results suggest that some strains may have the ability to infect rice root tissues via root hairs located at the emerging lateral roots and to spread extensively throughout the rice roots (Perrine-Walker et al. 2007b).
Quadt-Hallmann and Kloepper (1996) used antibodies coupled to fluorophores to study the colonization of internal tissues of different plant species by the endophytic bacteria Enterobacter asburiae JM22. Polyclonal and monoclonal antibodies applied in enzyme-linked immunosorbent assay (ELISA), dot blot assay, tissue printing, or immunogold labelling was sensitive and specific enough to detect JM22 in plant tissues.
Thomas and Reddy (2013) used the fluorophore Syto9 (S9), which binds nucleic acids in bacteria, in combination with propidium iodide (PI) to localize endophytic bacteria in the inner tissues of Musa acuminate (banana) by epifluorescence and confocal laser scanning microscopy (CLSM). Their results showed an extensive bacterial colonization of banana tissues. Rothballer et al. (2003) examined the endophytic potential of two strains of A. brasilense, Sp245 and Sp7, on roots of different wheat cultivars using fluorescent in situ hybridization (FISH) in combination with confocal laser scanning microscopy. The results obtained revealed which strain was able to grow better in contact with wheat roots.
The location of bacteria inside the plants reveals information about the preferences of colonization of internal tissues by the endophytic bacteria. We can also distinguish if they perform an intra- or extracellular colonization. However, these techniques just give us a qualitative idea of the colonization. To quantify and give an accurate result of bacterial colonization, techniques based on fluorescence should be combined with other techniques, such as bioinformatic tools. In this sense, Liu et al. (2001) developed a computer-aided interactive system called “CMEIAS” (Center for Microbial Ecology Image Analysis System) to analyse the high degree of morphological diversity in growing microbial communities associated or not to a substrate, which might be the plant root surface.
7.2.3 Plant Responses to Endophytic Bacterial Colonization
Once bacteria enter into the plant, different defence reactions have often been described. For example, the strengthening of cell walls, the production of antibiotics, growth-stimulating substances or enzymes and gum formation inside vessels have been observed (James et al. 2002; Compant et al. 2005; Miché et al. 2006). However, in contrast to the plant response to phytopathogens, few defence mechanisms have been described in plant response to PGPBEs. Moreover, certain plants have been shown to change their chemical responses when interacting with PGPBEs compared with non-beneficial bacteria, indicating that the plant does not recognize the PGPBEs as harmful agents (Miché et al. 2006; Rocha et al. 2007). It has also been reported that plants may show defence reactions controlling endophytic colonization, involving the production of salicylic acid (SA), jasmonic acid (JA) or ethylene, among other molecules. For example, dicotyledonous plants are known to use salicylic acid (SA) and ethylene as signalling molecules, which control colonization by some endophytes (Iniguez et al. 2005).
In monocotyledonous plants such as rice, the addition of jasmonic acid (JA), but not ethylene, was shown to interfere with the colonization of the diazotroph Azoarcus sp., suggesting that plant defence responses involving the JA signalling pathway may also control endophytic colonization inside the root system. However, in a compatible endophytic association, JA-associated plant responses were less pronounced and did not restrict endophytic colonization (Miché et al. 2006).
For example, rhizobial inoculation in cereal plants, especially rice, is associated with an increased accumulation of phenolic substances such as gallic, tannic, ferulic and cinnamic acids in plant leaves (Mirza et al. 2001). Such increases in phenolic acids are a pathogenic stress-related phenomenon in plants (Pieterse et al. 2002). Defence reactions triggered in response to rhizobial invasions are termed as rhizobacteria-mediated induced systemic resistance. However, this systemic resistance is not enough to prevent the entry of the Rhizobium inside the plant. Thus, rhizobia successfully colonize and disseminate throughout the inner host plant without evoking an observable defence reaction in the plant (Mia and Shamsuddin 2010).
7.3 Nitrogen-Fixing Bacterial Endophytes
Several studies have shown that endophytic bacteria are able to enter the inner tissues of plants, successfully colonize them and cause benefits. Therefore, it is inevitable that the use of these endophytic bacteriaasan alternatives to chemical fertilizers as a means to aid in the demand for food will receive support. According to FAO, the main cereal crops in terms of global production are maize, rice and wheat. In 2011, their production was more than 833, 723 and 704 Mt., respectively (Perez-Montaño et al. 2014). In order to maintain high production levels, there is a massive use of N-based fertilizers, and ~60% of the total synthetic nitrogen fertilizers produced worldwide is currently used in cereal crops (Dobermann 2007; Westhoff 2009). As nitrogen continues to be a serious problem for agriculture, due to the lack of available forms for plants or due to the excess of N-based fertilizers, the formulation of biofertilizers based in nitrogen-fixing endophytic bacteria presents itself as the more suitable solution to overcome these problems. In this section, we focus on endophytic bacteria that are able to fix nitrogen for these cereal crops with higher yields worldwide (Mia and Shamsuddin 2010; Sindhu et al. 2016; Meena et al. 2013c, 2014b, 2015d; Singh et al. 2016, 2015).
Bacteria responsible for nitrogen fixation are called diazotrophs, which harbour nitrogenase, the enzyme complex that catalyses the conversion of N2 gas to ammonia, a form that can be used by plants (Santi et al. 2013). Some of these diazotrophic bacteria are also PGPBEs. They have been detected inside the plant, causing beneficial effects such as plant growth promoters and nitrogen fixation. These bacteria, found in close association with roots, are usually designated “associative” nitrogen-fixing bacteria. However, the frontier between associative and endophytic plant colonization is not always clear since associative bacteria can also be observed in plant tissues; although, they are less abundant than strains originally classified as endophytes (Elmerich 2007). In contrast to what occurs in endosymbiosis, these bacteria do not induce differentiated structures in the roots, and although endophytic bacteria invade plant tissues, they cannot be regarded as endosymbionts that reside intracellularly in living plant cells. Endophytic diazotrophs may have an advantage over root-surface associative diazotrophs as they colonize the interior of plant roots and can establish themselves in niches that provide more appropriate conditions for effective nitrogen fixation and subsequent transfer of the fixed nitrogen to the host plant (Reinhold-Hurek and Hurek 2011). Some of the main bacteria that can live in association with maize, rice and wheat and contribute to improve plant growth are presented in Table 7.1. Some bacterial genera, such as Azospirillum, Azoarcus, Herbaspirillum and Gluconacetobacter, which promote growth, fix nitrogen and have more efficiency in colonization, were isolated in a plant species and were more competent in the reinoculation in the same plant.
The use of the bacterial genus Azospirillum as inoculants and the discovery of the high acetylene reduction (AR) activity associated with the roots of cereals immediately attracted much interest among agronomists and soil microbiologists. Many studies were performed on the inoculation of these crops with Azospirillum sp., particularly the Azospirillum brasilense type strain Sp7 originally isolated from the rhizosphere soil of Digitaria decumbens (and the closely related strain Cd) (Bashan and Levanony 1990). Boddey and Dobereiner (1995) showed that Azospirillum strains isolated from surface-sterilized roots of a certain cereal showed a greater aptitude to reinfect the same cereal and to promote responses in crop yield and/or N accumulation when these “homologous” strains were inoculated. In this respect, several studies showed that the A. brasilense strain Sp 245, isolated from surface-sterilized wheat roots, repeatedly increased grain yield and N accumulation in wheat in both field and pot experiments, where Sp 7 and/or Cd promoted little or no plant response (Baldani et al. 2002). Similar results have been obtained with maize, wheat and pearl millet by other authors (Couillerot et al. 2013; Masciarelli et al. 2013; Piccinin et al. 2013; Morley 2013; Lakhani et al. 2014).
The genus Azoarcus is a group of gram-negative, endorhizospheric diazotrophic bacteria, originally isolated from roots of the grass Leptochloa fusca (L.), namely, Kallar grass, which are able to invade plant tissues due to their cellulolytic enzymes (Reinhold-Hurek et al. 1993). Reinhold-Hurek et al. (1993) observed that Azoarcus is able to colonize the interior of sorghum plants by means of its cellulolytic enzymes. Therefore, Azoarcus sp. strain BH72 is not specific to its original host plant, Kallar grass, and maybe used as inoculum for other members of the Gramineae family. To evaluate its contribution of biological nitrogen fixation (BNF), the total nitrogen content in the whole system was analysed. After 28 days of cultivation, a sevenfold increase of total N was measured, from which the majority (72.6%) was located in the growth medium.
Gluconacetobacter diazotrophicus, a N2-fixing bacterium has been originally isolated from sugarcane roots and inside stems collected in various sites of Brazil (Cavalcante and Dobereiner 1988) and of Australia (Li and Macrae 1992). This endophytic bacterium is able to fix N2 even in the presence of nitrates and seems to be best adapted to the environment for growing sugarcane (Cavalcante and Dobereiner 1988). This bacterium could have more economic importance compared with other diazotrophs associated with sugarcane (Fuentes-Ramirez et al. 1993).
Moreover, some studies have shown its ability to act as a PGPBE (Fuentes-Ramirez et al. 1993; Saravanan et al. 2008; Mehnaz and Lazarovits 2006; Sahai et al. 2015). Fuentes-Ramirez et al. isolated 18 strains belonging to this species that produce different concentrations of indoleacetic acid (IAA). Thus, considering that G. diazotrophicus was found within the plant tissue, the biosynthesis of IAA suggests that these strains could promote root formation and improve sugarcane growth by direct effects on metabolic processes, in addition to their role in N2 fixation. G. diazotrophicus has been isolated from other plant hosts, such as wetland rice, pineapples, tea, coffee, etc. (Saravanan et al. 2008). Mehnaz and Lazarovits (2006) showed the inoculation effects of G. diazotrophicus in maize provided significant plant growth promotion expressed as increased root and shoot weight when compared to uninoculated plants.
Species from the genus Herbaspirillum, which are classified as plant growth-promoting rhizobacteria (PGPR), can produce biological nitrogen fixation (BNF) for plants, as well as present P-solubilization and siderophore production (Richardson et al. 2009). In a recent study, Alves et al. (2015) showed the plant growth promotion effect of 21 strains of Herbaspirillum species on maize plants. In this trial, the grain yield was evaluated as well as the contribution of biological nitrogen fixation (BNF). This study showed that H. seropedicae ZAE94 was the best strain under controlled conditions, and its application as a field inoculant increased maize yield up to ~34%, depending on the plant genotype.
All these nitrogen-fixing endophytic bacteria also improve root development by the production of different classes of growth regulators that influence primary root growth and increase the number and length of lateral roots and elongating root hairs, which in turn results in an increase in the field productivity of crops (Dobbelaere et al. 1999; Contesto et al. 2008; Combes-Meynet et al. 2011; Walker et al. 2012).
7.4 Bacterial Endophytes from Cereals Used as Plant Probiotics
Many bacterial endophytes able to promote plant growth have been isolated from within the cereals, as shown in Table 7.2. Nevertheless, we can observe that these same isolates are then used to reinoculate the same plant host. It may be due to adaptation that the bacteria have to colonize the plant. This kind of bacteria has a potential to interact with cereals, due to the effects and benefits produced. In this part of the chapter, we focus on the description of various mechanisms used by endophytes to enhance plant growth, improve agronomic characteristics and solve problems of pollution.
Currently, there are a huge number of studies published that report the use of endophytic bacteria as PGPR inoculants (some of them summarized in Table 7.2). Commonly, plant growth promotion occurs due to a combination of different action modes, such as the improvement of the host’s nutrient status, promoting root surface area and increasing the availability of nutrients to the plants (Perez-Montaño et al. 2014 (Fig. 7.2). Every bacterial strain may use one or several mechanisms, depending on the phase of plant’s life cycle (Long et al. 2008).
According to Govindarajan et al. (2008), rice yield production was increased with respect to a control treatment when a bacterial inoculant was applied. Moreover, the effect of the inoculation caused rice seedlings to grow better under N-deficient conditions. Mäder et al. (2011) showed an increase in wheat grain yield (~31%) after the inoculation with Pseudomonas jessenii R62 and Pseudomonas synxantha R81, in comparison to uninoculated control plants.
Recently, the potential of endophytic bacteria to degrade pollutants in order to allow plants to emerge as the natural vegetation at a contaminated site or to decrease contaminant concentration is being analysed (Syranidou et al. 2016). Although many number of studies focus on the degradation of compounds, such as herbicides, pesticides and hazardous organic compounds, in many occasions, these benefits and effects are also related and associated with an improvement of plant development. Sorty et al. (2016) reported that endophytic bacteria could alleviate the harmful effects of salt stress and enhance seed germination in wheat, as well as to promote plant growth and to increase dry biomass and total soluble sugars. Wheat seedlings are able to germinate under different salinity regimes after co-inoculation with Bacillus subtilis SU47 and Arthrobacter sp. SU18 (Upadhyay et al. 2012).
Under stress conditions, plants increase their ethylene levels causing important cell damage (Argueso et al. 2007; Hardoim et al. 2015; Perez-Montaño et al. 2014). Thus, the role of ACC deaminase production by endophytic bacteria and the ability to decrease ethylene levels have been also analysed (Glick 2014; Etesami et al. 2014; Gamalero and Glick 2015; Khan et al. 2016). Ethylene is a plant hormone, which is also the key regulator of plant colonization by endophytic bacteria. According to Etesami et al. (2014), the endophytic strain P. fluorescens REN1, selected for its high ACC deaminase production, significantly colonized rice seedling roots in comparison with other ACC deaminase-producing isolates in controlled conditions. This result supports the idea of the use of ACC deaminase activity as a powerful tool to select effective endophytic bacteria with plant growth-promoting capabilities.
Another key factor to be analysed in the plant-endophytes association is phytohormone production (auxins, gibberellins and cytokinins), which is one of the most well-studied mechanisms in relation to plant growth promotion (Hardoim et al. 2015). Auxins are a class of plant growth regulators, known to stimulate cell elongation in plants, and their production by endophytic strains has been reported (Long et al. 2008; Shi et al. 2009). Merzaeva and Shirokikh (2010) presented an increase in the germination capacity of rye seedlings, which were treated with auxins produced by endophytic bacteria.
Apart from being typical trait of root-associated endophytes, gibberellins production elicits various metabolic functions of plant growth (Macmillan 2001), and the production by endophytes is currently described worldwide (Khan et al. 2014; Shahzad et al. 2016). Cytokinin production by bacterial endophytes is commonly analysed and reported in relation to plant growth promotion. According to the data presented by Kudoyarova et al. (2014), Bacillus subtilis IB-22 increased amino acid rhizodeposition in wheat roots due to its ability to produce cytokinins. Apart from the fact that most of the described endophytes present the mechanisms explained above, some endophytes are also inoculated as biocontrol agents (Díaz-Herrera et al. 2016; Xu et al. 2017). According to Pan et al. (2015) B. megaterium BM1 (entophytic strain isolated from wheat) significantly reduces the incidence and severity of infection by Fusarium graminearum in wheat crops.
7.5 Current Situation of Commercial Products Based on Endophytic Bacteria
In order to satisfy the increase in food demand and environmental concerns, new ways of fertilization and the production of agronomic commercial products are being developed with the principal aim of creating a more sustainable agriculture. According to the new restrictive laws and some programmes and initiatives (e.g. Horizon 2020) concerning the use of chemical fertilizers, the creation and commercialization of new green products is expanding worldwide, and several companies are developing a wide range of products based on different bacterial inoculants. Researchers and companies must consider the introduction and use of endophytes for the formulation of these products, where the full understanding of their behaviour under different conditions is probably the key aspect for developing an application system that assures continuity and efficacy.
Despite the simplicity of production technologies and the low-cost industrial procedures of biofertilizer production, in comparison to the chemical fertilizer industry, there are big differences among the number of companies and the products they produce (Table 7.3), which are currently on sale globally (Naveed et al. 2015).
Europe is one of the areas that have developed more governmental policies for controlling the biofertilizer market (Garcia-Fraile et al. 2015). However, there are no existing specific regulations or a single process to regulate the quality for newly produced biofertilizers, and the already established laws are very different among the European Union member states. Some EU countries, such as the United Kingdom and Ireland, do not have specific regulations regarding the use of microbial inoculants.
Since 1998, the European company “Xurian Environnement” has been analysing and producing a wide range of commercial green products. The team of technical experts provide personalized assistance to increase the biomass of cereal and oilseed crops. One of the bestselling products is Ovalis Rhizofertil®, a microbial inoculant based on the strain P. putida I-4613. Another company, currently in expansion, is Symborg, which commercializes a product called VitaSoil®, a mix of rhizospheric microorganisms specific for the growth promotion of cereal crops and soil regeneration.
According to the Food and Agricultural Organization (FAO), Asia and the Pacific zone are the largest users of fertilizers in the world and import the three major nutrients (nitrogen, phosphate and potassium) in large amounts. However, regional governments promote the development of the biofertilizer market in order to contribute to a more sustainable agriculture in these countries. The most important companies in terms of sales and production are Agri Life and Ajay Bio-tech (India) LTD. Some of the products sold by these companies are suitable for cereal crops, such as Ajay Azo/Rhizo/Azospirillum® (different biofertilizers based on Azotobacter, Rhizobium and Azospirillum species, respectively) and Agri Life Nitrofix® (biological fertilizer based on the strain A. chroococcum MTCC 3853), among others. These biofertilizers are based on single or combined efficient nitrogen-fixing bacteria (NFB) or phosphate-solubilizing bacteria (PSB) that help plant uptake of nutrients when applied to seed or through the soil. Moreover, the company “JSC Industrial Innovations” commercializes Azotobacterin®, which produces up to a ~20% increase in yield of crops such as wheat, barley and maize, among other cereals. This product contains the diazotrophic bacterial strain A. brasilense B-4485. According to Garcia-Fraile et al. (2015), this product is one of the most frequently used in Russia.
In China, the company “China Bio-Fertilizer AG” sells a product called “CBF”, which is formed by a mix of two bacterial species of the genus Bacillus (B. mucilaginosus and B. subtilis) that are able to solubilize phosphorus and potassium, resulting in an increase in crop yields (up to ~30% depending on plant species).
In America, farmers are expected to use an additional 300,000 tonnes of nitrogen fertilizers in 2018, which will be mainly applied to agricultural surface crops (wheat, corn and forage crops). This continent has the biggest worldwide biofertilizer company, Monsanto, which currently belongs to the company Bayer. Monsanto focuses on empowering farmers to produce more from their land while conserving natural resources such as water and energy. Also, they produce “QuickRoots®”, a microbial seed inoculant based on a bacteria-fungi mixture, mainly B. amyloliquefaciens and T. virens, to enhance nutrient uptake in wheat and corn crops, which results in an enhanced yield potential. Monsanto, as well as other companies such as Novozymes and BASF, also operates worldwide.
Also in the USA, the Flozyme Corporation, a company that has been testing new technologies designed to increase crop production and reduce or eliminate the need for fertilizers, produces and commercializes “Inogro”. This product is a mix of more than 30 microbial species selected for their plant growth promotion abilities. Independent tests showed a significant increase in rice yields under greenhouse conditions (www.flozyme.com/agriculture/).
Since 1984, the company “Laboratorios Bioagro S.A. (Argentina)” has focused on the research and development of highly environmental friendly products to help satisfy the farmers’ needs. One of their most famous products is “Liquid PSA”, which contains P. aurantiaca SR1 and is registered by the national service for agricultural health of Argentina, due to its promotion of wheat growth. Moreover, in the same country, the company Semillera Guasch SRL launched a brand named Zaden Agrotecnologias®, which produces a biological inoculant called Zadpirillum® that is based on the plant growth-promoting strain A. brasilense AZ39 and enhances maize yields.
Even Africa will require 4 million tonnes of nitrogen fertilizers in 2018, and the use of biofertilizers varies widely among countries due to the farmers’ reticence to apply microbial biofertilizers. Therefore, the experts recommend a combination between using local technological knowledge and microbial fertilizers (Babalola and Glick 2012) as the only way to satisfy the increasing food demand that will continue to exist over the next decades. As regards there are projects searching for solutions, such as Engineering Nitrogen Symbiosis for Africa project (ENSA) or N2Africa project, led by two of the most important European research centres, John Innes Centre and Wageningen University, respectively, which have received funding from the Bill and Melinda Gates Foundation and aim to help African farmers to enhance their crop yields by engineering nonleguminous plants for fixing nitrogen and to improve inoculants based on microbial strains.
In this context, the collaboration between researchers and industries becomes a key aspect for the development of microbial-based biofertilizers. The underlying mechanisms of the interaction of plants with bacterial endophytes is still unknown, and there are also bio safety issues that need to be addressed; for example, strains forming part of biofertilization schemes must be tested in order to avoid damages. The comprehensive research of bacterial endophytic populations will allow more efficient biofertilizers to be made. Moreover, it is very important that the efforts to develop biofertilizers must be approved and accepted by farmers around the world, where they are provided the proper education and simplified procedures for using the products correctly. These measures would be positive steps to encourage the commercialization and production of biofertilizers by companies worldwide.
7.6 Conclusion and Future Perspectives
Enhanced cereal crop production by the application of PGPBE-based biofertilizers is the necessary breakthrough to underpin a more sustainable food production for feeding the global population and to overcome the environmental issues derived from the abuse of chemical fertilizers. In this chapter, we have presented the great diversity of bacterial endophytic strains isolated from several cereal crops and their potential as plant growth promoters when inoculated onto their isolation source or other types of crops. These PGPBEs are able to establish a more intimate relationship with cereals crops, showing a better colonization of the inner tissues of these plants and performing their beneficial actions in a close interaction with their hosts. Hence, the progressive understanding of microbial populations that are applicable as inoculants for different crops is absolutely necessary in order to ensure higher yields in a sustainable way.
The Food and Agriculture Organization (FAO) promotes the use of biofertilizers in both developed and developing countries, and many have employed them to a greater or lesser extent (FAO 1991). Moreover, most countries have developed policies to reduce the use of chemical fertilizers due to the consumer demands for more organic food. Thus, the commercialization and application of bacterial fertilizers on agricultural crops are increasing year by year. In the near future, more efforts will be needed regarding the development of proper inoculants that enhance cereal growth and yields. Based on this premise, the Horizon 2020 Programme strongly supports European research dedicated to the biotechnological processes and products. Also, Latin America is one of the world’s largest fertilizer consumers, particularly Mexico, and a programme to support the introduction of N-fixing biofertilizers based on Azospirillum was carried on ~1.5 M ha (Fuentes-Ramirez and Caballero-Mellado 2005). India has the most complete legal framework in the world related to biofertilizers, and ~350–500 t of biofertilizers are requested form the Indian National Biofertilizer Development Center (NBDC) and the Bio-Tech Consortium of India Ltd. (BCIL) for agricultural purposes in India (Dewasthale and Bondre 2008). In addition, Japan has long since begun to include nitrogen-fixing bacteria in the formulation of biofertilizers, and the Tokachi Federation of Agricultural Cooperatives (TFAC) is the largest producer and marketer of rhizobial biofertilizers since 1953. This company uses PGPR as biofertilizers and as biocontrol agents, among others. The Forum for Nuclear Cooperation in Asia (FNCA) is also located in Japan and actively develops biofertilizers in Asian countries (Naveed et al. 2015). According to Masso et al. 2014, in Africa, regulatory frameworks are required since biofertilizers are of poor quality and consequently cause economic loss. For this reason, Babalola and Glick (2012) suggest the combined use of traditional techniques together with microbial fertilizers.
Therefore, we propose that more work is needed in order to development better biofertilizers and to ensure their proper use. This also includes the establishment of specific legislation that regulates biofertilizers in order to facilitate the processes of production and commercialization. Governments should support the use of biofertilizers and provide proper funding for research and the creation of companies in the field of biofertilizers. To reduce the farmer’s reticence towards these types of products, specific programmes and initiatives are needed to train farmers in the use of biofertilizers. Due to the increasing demand for fertilizers worldwide, more research efforts are needed to elucidate the inner mechanisms affecting the interaction between cereal crops and beneficial bacteria.
References
Ahmad M, Nadeem SM, Naveed M, Zahir ZA (2016) Potassium-solubilizing bacteria and their application in agriculture. In: Meena VS, Maurya BR, Verma JP, Meena RS (eds) Potassium solubilizing microorganisms for sustainable agriculture. Springer, New Delhi, pp 293–313. https://doi.org/10.1007/978-81-322-2776-2_21
Alves GC, Videira SS, Urquiaga S, Reis VM (2015) Differential plant growth promotion and nitrogen fixation in two genotypes of maize by several Herbaspirillum inoculants. Plant Soil 387(1–2):307–321
Argueso CT, Hansen M, Kieber J (2007) Regulation of ethylene biosynthesis. J Plant Growth Regul 26(2):92–105
Babalola OO, Glick BR (2012) Indigenous African agriculture and plant associated microbes: current practice and future transgenic prospects. Sci Res Essays 7(28):2431–2439
Bahadur I, Meena VS, Kumar S (2014) Importance and application of potassic biofertilizer in Indian agriculture. Int Res J Biol Sci 3:80–85
Bahadur I, Maurya BR, Kumar A, Meena VS, Raghuwanshi R (2016a) Towards the soil sustainability and potassium-solubilizing microorganisms. In: Meena VS, Maurya BR, Verma JP, Meena RS (eds) Potassium solubilizing microorganisms for sustainable agriculture. Springer, New Delhi, pp 225–266. https://doi.org/10.1007/978-81-322-2776-2_18
Bahadur I, Maurya BR, Meena VS, Saha M, Kumar A, Aeron A (2016b) Mineral release dynamics of tricalcium phosphate and waste muscovite by mineral-solubilizing rhizobacteria isolated from indo-gangetic plain of India. Geomicrobiology Journal. https://doi.org/10.1080/01490451.2016.1219431
Baldani VLD, Baldani JI, Döbereiner J (2000) Inoculation of rice plants with the endophytic diazotrophs Herbaspirillum seropedicae and Burkholderia spp. Biol Fertil Soils 30:485–491
Baldani JI, Reis VM, Baldani VL, Döbereiner J (2002) Review: a brief story of nitrogen fixation in sugarcane-reasons for success in Brazil. Funct Plant Biol 29(4):417–423
Bashan Y, Levanony H (1990) Current status of Azospirillum inoculation technology: Azospirillum as a challenge for agriculture. Can J Microbiol 36:591–608
Bashan Y, De-Bashan LE, Prabhu SR, Hernandez JP (2014) Advances in plant growth-promoting bacterial inoculant technology: formulations and practical perspectives (1998–2013). Plant Soil 378(1–2):1–33
Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microb Ecol 68:1–13
Biswas JC, Ladha, JK, Dazzo FB (2000) Rhizobia inoculation improves nutrient uptake and growth of lowland rice. Pak J Bot l64:1644–1650
Boddey RM, Dobereiner J (1995) Nitrogen fixation associated with grasses and cereals: recent progress and perspectives for the future. Fert Res 42(1–3):241–250
Bulgarelli D, Garrido-Oter R, Münch PC, Weiman A, Dröge J, Pan Y, McHardy AC, Schulze-Lefert P (2015) Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host Microbe 17(3):392–403
Cavalcante VA, Dobereiner J (1988) A new acid-tolerant nitrogen-fixing bacterium associated with sugarcane. Plant Soil 108:23–31
Chaintreuil C, Giraud E, Prin Y, Lorquin J, Ba A, Gillis M, de Lajudie P, Dreyfus B (2000) Photosynthetic Bradyrhizobia are natural endophytes of the African wild rice Oryza breviligulata. Appl Environ Microbiol 66:5437–5447
Chanway CP, Shishido M, Nairn J, Jungwirth S, Markham J, Xiao G, Holl FB (2000) Endophytic colonization and field responses of hybrid spruce seedlings after inoculation with plant growth-promoting rhizobacteria. Forest Ecol Manag 133(1):81–88
Chauhan H, Bagyaraj DJ, Selvakumar G, Sundaram SP (2015) Novel plant growth promoting rhizobacteria-prospects and potential. Appl Soil Ecol 95:38–53
Chelius MK, Triplett EW (2000) Dyadobacter fermentans gen. Nov., sp. nov., a novel gram-negative bacterium isolated from surface-sterilized Zea mays stems. Int J Syst Evol Microbiol 50(2):751–758
Chi F, Shen SH, Cheng HP, Jing YX, Yanni YG, Dazzo FB (2005) Ascending migration of endophytic rhizobia, from roots to leaves, inside rice plants and assessment of benefits to rice growth physiology. Appl Environ Microbiol 71(11):7271–7278
Cocking EC (2003) Endophytic colonization of plant roots by nitrogen-fixing bacteria. Plant Soil 252(1):169–175
Combes-Meynet E, Pothier JF, Moenne-Loccoz Y, Prigent-Combaret C (2011) The pseudomonas secondary metabolite 2, 4-diacetylphloroglucinol is a signal inducing rhizoplane expression of Azospirillum genes involved in plant-growth promotion. Mol Plant-Microbe Interact 24:271–284
Compant S, Duffy B, Nowak J, Clément C, Barka EA (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl Environ Microbiol 71:4951–4959
Compant S, Clément C, Sessitsch A (2010) Plant growth-promoting bacteria in the rhizo-and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42(5):669–678
Conn KL, Nowak J, Lazarovitz G (1997) A gnotobiotic bioassay for studying interactions between potato and plant growth-promoting rhizobacteria. Can J Microbiol 43:801–808
Contesto C, Desbrosses G, Lefoulon C, Béna G, Borel F, Galland M, Gamet L, Varoquaux F, Touraine B (2008) Effects of rhizobacterial ACC deaminase activity on Arabidopsis indicate that ethylene mediates local root responses to plant growth-promoting rhizobacteria. Plant Sci 175:178–189
Couillerot O, Ramírez-Trujillo A, Walker V, Felten A, Jansa J, Maurhofer M, Défago G, Prigent-Combaret C, Comte G, Caballero-Mellado J, Moënne-Loccoz Y (2013) Comparison of prominent Azospirillum strains in Azospirillum–Pseudomonas–Glomus consortia for promotion of maize growth. Appl Microbiol Biotechnol 97(10):4639–4649
Das I, Pradhan M (2016) Potassium-solubilizing microorganisms and their role in enhancing soil fertility and health. In: Meena VS, Maurya BR, Verma JP, Meena RS (eds) Potassium solubilizing microorganisms for sustainable agriculture. Springer, New Delhi, pp 281–291. https://doi.org/10.1007/978-81-322-2776-2_20
de Salamone IEG, Dobereiner J, Urquiaga S, Boddey RM (1996) Biological nitrogen fixation in Azospirillum strain-maize genotype associations as evaluated by the 15N isotope dilution technique. Biol Fertil Soils 23:249–256
Dewasthale G, Bondre (2008) Marketing of biofertilizers. Conference on rural marketing. Indian Institute of Management, Kozhikode
Díaz-Herrera S, Grossi C, Zawoznik M, Groppa MD (2016) Wheat seeds harbour bacterial endophytes with potential as plant growth promoters and biocontrol agents of Fusarium graminearum. Microbiol Res 186–187:37–43
Dobbelaere S, Croonenborghs A, Thys A, Broek AV, Vanderleyden J (1999) Phytostimulatory effect of Azospirillum brasilense wild type and mutant strains altered in IAA production on wheat. Plant Soil 212:155–164
Dobbelaere S, Croonenborghs A, Thys A, Ptacek D, Vanderleyden J, Dutto P, Labandera-Gonzalez C, Caballero-Mellado J, Aguirre JF, Kapulnik Y, Brener S, Burdman S, Kadouri D, Sarig S, Okon Y (2001) Responses of agronomically important crops to inoculation with Azospirillum. Aust J Plant Physiol 28:871–879
Dobermann A (2007) Nutrient use efficiency-measurement and management in a time of new challenges. In: Proceedings of the IFA International Workshop on Fertilizer Best Management Practices. Fertilizer Best Management Practices, 7–9 March 2007, Brussels, Belgium. International Fertilizer Industry Association, pp 1–28
Dominguez-Nunez JA, Benito B, Berrocal-Lobo M, Albanesi A (2016) Mycorrhizal fungi: role in the solubilization of potassium. In: Meena VS, Maurya BR, Verma JP, Meena RS (eds) Potassium solubilizing microorganisms for sustainable agriculture. Springer, New Delhi, pp 77–98. https://doi.org/10.1007/978-81-322-2776-2_6
Dotaniya ML, Meena VD, Basak BB, Meena RS (2016) Potassium uptake by crops as well as microorganisms. In: Meena VS, Maurya BR, Verma JP, Meena RS (eds) Potassium solubilizing microorganisms for sustainable agriculture. Springer, New Delhi, pp 267–280. https://doi.org/10.1007/978-81-322-2776-2_19
Elbeltagy AK, Sato NT, Suzuki H, Ye B, Hamada T, Isawa T, Mitsui H, Minamisawa K (2001) Endophytic colonization and in plant nitrogen fixation by a Herbaspirillum sp. isolated from wild rice species. Appl Environ Microbiol 67:5285–5293
Elmerich, C (2007) Historical perspective: from bacterization to endophytes. In: Associative and endophytic nitrogen-fixing bacteria and cyanobacterial associations. Springer, Dordrecht, pp 1–20
Engelhard M, Hurek T, Reinhold-Hurek B (2000) Preferential occurrence of diazotrophic endophytes, Azoarcus spp., in wild rice species and land races of Oryza sativa in comparison with modern races. Environ Microbiol 2:131–141
Estrada P, Mavingui P, Cournoyer B, Fontaine F, Balandreau J, Caballero-Mellado J (2005) A N-fixing endophytic Burkholderia sp. associated with maize plants cultivated in Mexico. Int J Syst Evol Microbiol 55:1233–1237
Etesami H, Hosseini HM, Alikhani HA (2014) Bacterial biosynthesis of 1-aminocyclopropane-1-caboxylate (ACC) deaminase, a useful trait to elongation and endophytic colonization of the roots of rice under constant flooded conditions. Physiol Mol Biol Plants 20(4):425–434
FAO (1991) Organic recycling in Asia and the Pacific. Regional office for Asia and Pacific (RAPA)/FAO, Bangkok, Thailand
Flozyme Corporation Inc; Agriculture, Inogro. Flozyme Corporation Web. http://www.flozyme.com/agriculture/ (2016). Accessed 21 Nov 2016
Fox AR, Soto G, Valverde C, Russo D, Lagares A, Zorreguieta A, Alleva K, Pascuan C, Frare R, Mercado-Blanco J, Dixon R, Ayub ND (2016) Major cereal crops benefit from biological nitrogen fixation when inoculated with the nitrogen-fixing bacterium Pseudomonas protegens Pf-5 X940. Environ Microbiol 18(10):3522–3534
Francine M, Walker P, Prayiton J, Rolfe BG, Weinman JJ, Hocart CH (2007) Infection process and the interaction of rice roots with rhizobia. J Exp Bot 58(12):3343–3350
Fuentes-Ramirez LE, Caballero-Mellado J (2005) Bacterial biofertilizers. In: PGPR: biocontrol and biofertilization. Springer, Dordrecht, pp 143–172
Fuentes-Ramirez LE, Jiminez-Salgado T, Abarca-Ocampo IR, Caballero-Mellado J (1993) Acetobacter diazotrophicus, an indolacetic acid-producing bacterium isolated from sugarcane cultivars in Mexico. Plant Soil 154:145–150
Gaiero JR, McCall CA, Thompson KA, Day NJ, Best AS, Dunfield KE (2013) Inside the root microbiome: bacterial root endophytes and plant growth promotion. Am J Bot 100(9):1738–1175
Gamalero E, Glick BR (2015) Bacterial modulation of plant ethylene levels. Plant Physiol 169:13–22
García-Fraile P, Menéndez E, Rivas R (2015) Role of bacterial biofertilizers in agriculture and forestry. AIMS Bioeng 2:183–205. https://doi.org/10.3934/bioeng.2015.3.183
Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 169:30–39
Goormachtig S, Capoen W, James E, Holsters M (2004) Switch from intracellular to intercellular invasion during water stress-tolerant legume nodulation. Proc Natl Acad Sci USA 101:6303–6308
Govindarajan M, Balandreau J, Muthukumarasamy R, Revathi G, Lakshminarasimhan C (2006) Improved yield of micropropagated sugarcane following inoculation by endophytic Burkholderia vietnamiensis. Plant Soil 280(1–2):239–252
Govindarajan M, Kwon SW, Weon HY (2007) Isolation, molecular characterization and growth-promoting activities of endophytic sugarcane diazotroph Klebsiella sp. GR9. World J Microbiol Biotechnol 23(7):997–1006
Govindarajan M, Balandreau J, Kwon SW, Weon HY, Lakshminarasimhan C (2008) Effects of the inoculation of Burkholderia vietnamensis and related endophytic diazotrophic bacteria on grain yield of rice. Microb Ecol 55(1):21–37
Gregory PJ (2006) Plant roots: growth, activity and interaction with soils. Blackwell Publishing, Oxford, 318 pp
Gutierrez-Zamora ML, Martınez-Romero E (2001) Natural endophytic association between Rhizobium etli and maize (Zea mays L.) J Biotechnol 91(2):117–126
Gyaneshwar P, James EK, Mathan N, Reinhold-Hurek B, Ladha JK (2001) Endophytic colonization of rice by a diazotrophic strain of Serratia marcescens. J Biotechnol 183:2634–2645
Gyaneshwar P, James EK, Reddy PM et al (2002) Herbaspirillum colonization increases growth and nitrogen accumulation in aluminium-tolerant rice varieties. New Phytol 154(1):131–145
Hardoim PR, Van Overbeek LS, Berg G, Ladha JK (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 79:3
Hartmann A, Stoffels M, Eckert B, Kirchhof G, Schloter M, Triplett EW (2000) Analysis of the presence and diversity of diazotrophic endophytes. Prokaryotic nitrogen fixation: a model system for the analysis of a biological process, pp 727–736
Hilali A, Prévost D, Broughton WJ, Antoun H (2001) Effets de l’inoculation avec des souches de Rhizobium leguminosarum biovar trifolii sur la croissance du blé dans deux sols du Maroc. Can J Microbiol 47(6):590–593
Iniguez L, Dong Y, Carter HD, Ahmer BM, Stone JM, Triplett EW (2005) Regulation of enteric endophytic bacterial colonization by plant defences. MPMI 18(2):169–178
Jain V, Gupta K (2003) The flavonoid naringenin enhances intercellular colonization of rice roots by Azorhizobium caulinodans. Biol Fertil Soils 38:119–123
Jaiswal DK, Verma JP, Prakash S, Meena VS, Meena RS (2016) Potassium as an important plant nutrient in sustainable agriculture: a state of the art. In: Meena VS, Maurya BR, Verma JP, Meena RS (eds) Potassium solubilizing microorganisms for sustainable agriculture. Springer, New Delhi, pp 21–29. https://doi.org/10.1007/978-81-322-2776-2_2
James EK, Gyaneshwar P, Mathan N, Barraquio WL, Reddy PM, Iannetta PPM, Olivares FL, Ladha JK (2002) Infection and colonization of rice seedlings by the plant growth-promoting bacterium Herbaspirillum seropedicae Z67. Mol Plant-Microbe Interact 15:894–906
Jat LK, Singh YV, Meena SK, Meena SK, Parihar M, Jatav HS, Meena RK, Meena VS (2015) Does integrated nutrient management enhance agricultural productivity? J Pure Appl Microbiol 9(2):1211–1221
Jeyabal A, Kupuswamy G (2001) Recycling of organic wastes for the production of vermicompost and its response in rice-legume cropping system and soil fertility. Eur J Agron 15:153–170
Jha Y, Subramanian RB (2016) Regulation of plant physiology and antioxidant enzymes for alleviating salinity stress by potassium-mobilizing bacteria. In: Meena VS, Maurya BR, Verma JP, Meena RS (eds) Potassium solubilizing microorganisms for sustainable agriculture. Springer, New Delhi, pp 149–162. https://doi.org/10.1007/978-81-322-2776-2_11
Ji SH, Gururani MA, Chun SC (2014) Expression analysis of rice pathogenesis-related proteins involved in stress response and endophytic colonization properties of gfp-tagged Bacillus subtilis CB-R05. Appl Biochem Biotechnol 174(1):231–241
Khan Z, Roman D, Kintz T, Delas Alas M, Yap R, Doty S (2014) Degradation, phytoprotection and phytoremediation of phenanthrene by endophyte Pseudomonas putida, PD1. Environ Sci Technol 48(20):12221–12228
Khan AL, Halo BA, Elyassi A, Ali S, Al-Hosni K, Hussai J, Al-Harrasi A, Lee I (2016) Indole acetic acid and ACC deaminase fromendophytic bacteria improves the growth of Solanum lycopersicum. Electron J Biotechnol 21:58–64
Kudoyarova GR, Melentiev AL, Martynenko EV, Timergalina LN, Arkhipova TN, Shendel GV, Kuz'mina LY, Dodd IC, Veselov SY (2014) Cytokinin producing bacteria stimulate amino acid deposition by wheat roots. Plant Physiol Biochem 83:285–291
Kuklinsky-Sobral J, Araújo WL, Mendes R, Geraldi IO, Pizzirani-Kleiner AA, Azevedo JL (2004) Isolation and characterization of soybean-associated bacteria and their potential for plant growth promotion. Environ Microbiol 6(12):1244–1251
Kumar A, Bahadur I, Maurya BR, Raghuwanshi R, Meena VS, Singh DK, Dixit J (2015) Does a plant growth-promoting rhizobacteria enhance agricultural sustainability? J Pure ApplMicrobiol 9:715–724
Kumar A, Meena R, Meena VS, Bisht JK, Pattanayak A (2016a) Towards the stress management and environmental sustainability. J Clean Prod 137:821–822
Kumar A, Patel JS, Bahadur I, Meena VS (2016b) The molecular mechanisms of KSMs for enhancement of crop production under organic farming. In: Meena VS, Maurya BR, Verma JP, Meena RS (eds) Potassium solubilizing microorganisms for sustainable agriculture. Springer, New Delhi, pp 61–75. https://doi.org/10.1007/978-81-322-2776-2_5
Kumar A, Maurya BR, Raghuwanshi R, Meena VS, Islam MT (2017) Co-inoculation with Enterobacter and Rhizobacteria on yield and nutrient uptake by wheat (Triticum aestivum L.) in the alluvial soil under indo-gangetic plain of India. J Plant Growth Regul. https://doi.org/10.1007/s00344-016-9663-5
Ladha JK, Kundu DK, Coppenolle MGA, Carangal VR, Peoples MB, Dart PJ (1996) Legume productivity and soil nitrogen dynamics in lowland rice-based cropping systems. Soil Sci Soc Amer J 60:183–192
Ladha JK, Padre AT, Punzalan GC, Castillo E, Singh U, Reddy CK (1998) Nondestructive estimation of shoot nitrogen in different rice genotypes. Agron J 90:33–40
Lakhani SH, Gediya KM, Patel AP (2014) Response of pearl millet (Pennisetum glaucum L.) to sowing methods and bio-fertilizers during summer season under middle Gujarat conditions. Trends Biosc 7(21):3423–3427
Lalande R, Bissonnette N, Coutlée D, Antoun H (1989) Identification of rhizobacteria from maize and determination of their plant-growth promoting potential. Plant Soil 115(1):7–11
Li R, MacRae IC (1992) Specific identification and enumeration of Acetobacter diazotrophicus in sugarcane. Soil Biol Biochem 24:413–419
Liu JFBD, Dazzo FB, Glagoleva O, Yu B, Jain AK (2001) CMEIAS: a computer-aided system for the image analysis of bacterial morphotypes in microbial communities. Microb Ecol 41(3):173–194
Lodewychx C, Vangronsveld J, Porteous F, Moore ER, Taghavi S, Mezgeay M, der Lelie DV (2002) Endophytic bacteria and their potential applications. Cr Rev Plant Sci 21:583–606
Long HH, Schmidt DD, Baldwin IT (2008) Native bacterial endophytes promote host growth in a species-specific manner; phytohormone manipulations do not result in common growth responses. PLoS One 3:e2702
MacMillan J (2001) Occurrence of gibberellins in vascular plants, fungi and bacteria. J Plant Growth Regul 20(4):387–442
Mäder P, Kaiser F, Adholeya A, Singh R, Uppalb HS, Sharmac AK, Srivastavac R, Sahaid V, Aragnoe M, Wiemkenf A, Johrig BN, Friedh PM (2011) Inoculation of root microorganisms for sustainable wheat-rice and wheat-black gram rotations in India. Soil Biol Biochem 43:609–619
Malusá E, Vassilev N (2014) A contribution to set a legal framework for biofertilisers. Appl Microbiol Biotechnol 98(15):6599–6607
Masciarelli O, Urbani L, Reinoso H, Luna V (2013) Alternative mechanism for the evaluation of indole-3-acetic acid (IAA) production by Azospirillum brasilense strains and its effects on the germination and growth of maize seedlings. J Microbiol 51(5):590–597
Masood S, Bano A (2016) Mechanism of potassium solubilization in the agricultural soils by the help of soil microorganisms. In: Meena VS, Maurya BR, Verma JP, Meena RS (eds) Potassium solubilizing microorganisms for sustainable agriculture. Springer, New Delhi, pp 137–147. https://doi.org/10.1007/978-81-322-2776-2_10
Masso C, Jefwa JM, Jemo M, Thuita M, Tarus D, Vanlauwe B (2014) Chapter twenty-two impact of inadequate regulatory frameworks on the adoption of bio-fertilizer (eg PGPR) Technologies. Recent advances in biofertilizers and biofungicides (PGPR) for sustainable agriculture, p 258
Maurya BR, Meena VS, Meena OP (2014) Influence of Inceptisol and Alfisol’s potassium solubilizing bacteria (KSB) isolates on release of K from waste mica. Vegetos 27:181–187
Meena OP, Maurya BR, Meena VS (2013a) Influence of K-solubilizing bacteria on release of potassium from waste mica. Agric Sust Dev 1:53–56
Meena VS, Maurya BR, Bohra JS, Verma R, Meena MD (2013b) Effect of concentrate manure and nutrient levels on enzymatic activities and microbial population under submerged rice in alluvium soil of Varanasi. Crop Res 45(1,2 & 3):6–12
Meena VS, Maurya BR, Verma R, Meena RS, Jatav GK, Meena SK, Meena SK (2013c) Soil microbial population and selected enzyme activities as influenced by concentrate manure and inorganic fertilizer in alluvium soil of Varanasi. Bioscan 8(3):931–935
Meena VS, Maurya BR, Bahadur I (2014a) Potassium solubilization by bacterial strain in waste mica. Bang J Bot 43:235–237
Meena VS, Maurya BR, Verma JP (2014b) Does a rhizospheric microorganism enhance K+ availability in agricultural soils? Microbiol Res 169:337–347
Meena RS, Meena VS, Meena SK, Verma JP (2015a) The needs of healthy soils for a healthy world. J Clean Prod 102:560–561
Meena RS, Meena VS, Meena SK, Verma JP (2015b) Towards the plant stress mitigate the agricultural productivity: a book review. J Clean Prod 102:552–553
Meena VS, Maurya BR, Meena RS (2015c) Residual impact of wellgrow formulation and NPK on growth and yield of wheat (Triticum aestivum L.) Bangladesh J Bot 44(1):143–146
Meena VS, Maurya BR, Verma JP, Aeron A, Kumar A, Kim K, Bajpai VK (2015d) Potassium solubilizing rhizobacteria (KSR): isolation, identification, and K-release dynamics from waste mica. Ecol Eng 81:340–347
Meena VS, Meena SK, Verma JP, Meena RS, Ghosh BN (2015e) The needs of nutrient use efficiency for sustainable agriculture. J Clean Prod 102:562–563. https://doi.org/10.1016/j.jclepro.2015.04.044
Meena VS, Verma JP, Meena SK (2015f) Towards the current scenario of nutrient use efficiency in crop species. J Clean Prod 102:556–557. https://doi.org/10.1016/j.jclepro.2015.04.030
Meena RK, Singh RK, Singh NP, Meena SK, Meena VS (2016a) Isolation of low temperature surviving plant growth-promoting rhizobacteria (PGPR) from pea (Pisum sativum L.) and documentation of their plant growth promoting traits. Biocatalysis Agricult Biotechnol 4:806–811
Meena RS, Bohra JS, Singh SP, Meena VS, Verma JP, Verma SK, Sihag SK (2016b) Towards the prime response of manure to enhance nutrient use efficiency and soil sustainability a current need: a book review. J Clean Prod 112(1):1258–1260
Meena SK, Rakshit A, Meena VS (2016c) Effect of seed bio-priming and N doses under varied soil type on nitrogen use efficiency (NUE) of wheat (Triticum aestivum L.) under greenhouse conditions. Biocatal Agric Biotechnol 6:68–75
Meena VS, Bahadur I, Maurya BR, Kumar A, Meena RK, Meena SK, Verma JP (2016d) Potassium-solubilizing microorganism in evergreen agriculture: an overview. In: Meena VS, Maurya BR, Verma JP, Meena RS (eds) Potassium solubilizing microorganisms for sustainable agriculture. Springer, New Delhi, pp 1–20. https://doi.org/10.1007/978-81-322-2776-2_1
Meena VS, Meena SK, Bisht JK, Pattanayak A (2016e) Conservation agricultural practices in sustainable food production. J Clean Prod 137:690–691
Meena VS, Maurya BR, Meena SK, Meena RK, Kumar A, Verma JP, Singh NP (2017) Can Bacillus species enhance nutrient availability in agricultural soils?. In: Islam MT, Rahman M, Pandey P, Jha CK, Aeron A (eds) Bacilli and agrobiotechnology. Springer, Cham, pp 367–395. https://doi.org/10.1007/978-3-319-44409-3_16
Mehnaz S, Lazarovits G (2006) Inoculation effects of Pseudomonas putida, Gluconacetobacter azotocaptans, and Azospirillum lipoferum on corn plant growth under greenhouse conditions. Microb Ecol 51(3):326–335
Merzaeva OV, Shirokikh IG (2010) The production of auxins by the endophytic bacteria of winter rye. Appl Biochem Microbiol 44:44–50
Mia MB, Shamsuddin ZH (2010) Rhizobium as a crop enhancer and biofertilizer for increased cereal production. Afr J Biotechnol 9(37):6001–6009
Miché L, Battistoni F, Gemmer S, Belghazi M, Reinhold-Hurek B (2006) Upregulation of jasmonate-inducible defense proteins and differential colonization of roots of Oryza sativa cultivars with the endophyte Azoarcus sp. Mol Plant-Microbe Interact 19:502–511
Mirza MS, Ahmad W, Latif F, Haurat J, Bally R, Normand P, Malik KA (2001) Isolation, partial characterization, and effect of plant growth promoting bacteria (PGPB) on micropropagated sugarcane in vitro. Plant Soil 237:47–54
Mitra S (2014) Interaction of Rhizobium sp. Strain IRBG74 with a Legume (Sesbania Cannabina) and a Cereal (Oryza Sativa)
Molla AH, Shamsuddin ZH, Halimi MS, Morziah M, Puteh AB (2001) Potential for enhancement of root growth and nodulation of soybean co-inoculated with Azospirillum and Bradyrhizobium in laboratory systems. Soil Biol Biochem 33(4):457–463
Morley R (2013) Impact of free-living diazotrophs, Azospirillum lipoferum and Gluconacetobacter azotocaptans, on growth and nitrogen utilization by wheat (Triticum aestivum cv. Lillian)
Muñoz-Rojas J, Caballero-Mellado J (2003) Population dynamics of Gluconacetobacter diazotrophicus in sugarcane cultivars and its effect on plant growth. Microb Ecol 46(4):454–464
Muthukumarasamy R, Cleenwerck I, Revathi G, Vadivelu M, Janssens D, Hoste B, Kang Ui Gum KU, Park K, Son CY, Sa T, Caballero-Mellado J (2005) Natural association of Gluconacetobacter diazotrophicus and diazotrophic Acetobacter peroxydans with wetland rice. Syst Appl Microbiol 28(3):277–286
Naveed M, Mehboob I, Shaker MA, Hussain MB, Farooq M (2015) Biofertilizers in Pakistan: initiatives and limitations. Int J Agril Biol 17:411–420
Oliveira AD, Urquiaga S, Döbereiner J, Baldani JI (2002) The effect of inoculating endophytic N2-fixing bacteria on micropropagated sugarcane plants. Plant Soil 242(2):205–215
Pan D, Mionetto A, Tiscornia S, Bettucci (2015) Endophytic bacteria from wheat grain as biocontrol agents of Fusarium graminearum and deoxynivalenol production in wheat. Mycotoxin Res 31:137
Parewa HP, Yadav J, Rakshit A, Meena VS, Karthikeyan N (2014) Plant growth promoting rhizobacteria enhance growth and nutrient uptake of crops. Agricult Sustain Dev 2(2):101–116
Perez-Montaño F, Alías-Villegas C, Bellogín RA, Del Cerro P, Espuny MR, Jiménez-Guerrero I, López-Baena FJ, Ollero FJ, Cubo T (2014) Plant growth promotion in cereal and leguminous agricultural important plants: from microorganism capacities to crop production. Microbiol Rev 169:325–336
Perrine-Walker FM, Gartner E, Hocart CH, Becker A, Rolfe BG (2007a) Rhizobium-initiated rice growth inhibition caused by nitric oxide accumulation. Mol Plant-Microbe Interact 20:283–292
Perrine-Walker FM, Prayitno J, Rolfe BG, Weinman JJ, Hocart CH (2007b) Infection process and the interaction of rice roots with rhizobia. J Exp Bot 58(12):3343–3350
Piccinin GG, Braccini AL, Dan LG, Scapim CA, Ricci TT, Bazo GL (2013) Efficiency of seed inoculation with Azospirillum brasilense on agronomic characteristics and yield of wheat. Ind Crop Prod 43:393–397
Pieterse CMJ, Van Wees SCM, Ton J, Van Pelt JA, Van Loon LC (2002) Signaling in rhizobacteria-induced systemic resistance in Arabidopsis thaliana. Plant Biol (Stuttgrat) 4:535–544
Prakash S, Verma JP (2016) Global perspective of potash for fertilizer production. In: Meena VS, Maurya BR, Verma JP, Meena RS (eds) Potassium solubilizing microorganisms for sustainable agriculture. Springer, New Delhi, pp 327–331. https://doi.org/10.1007/978-81-322-2776-2_23
Prayitno J, Stefaniak J, Mclever J, Weinman JJ, Dazzo FB, Ladha JK, Barraquio W, Yanni G, Rolfe BG (1999) Interactions of rice seedlings with bacteria isolated from rice roots. Aust J Plant Physiol 26:521–535
Priyadharsini P, Muthukumar T (2016) Interactions between arbuscular mycorrhizal fungi and potassium-solubilizing microorganisms on agricultural productivity. In: Meena VS, Maurya BR, Verma JP, Meena RS (eds) Potassium solubilizing microorganisms for sustainable agriculture. Springer, New Delhi, pp 111–125. https://doi.org/10.1007/978-81-322-2776-2_8
Quadt-Hallmann A, Kloepper JW (1996) Immunological detection and localization of the cotton endophyte Enterobacter asburiae JM22 in different plant species. Can J Microbiol 42(11):1144–1154
Raghavendra MP, Nayaka NC, Nuthan BR (2016) Role of rhizosphere microflora in potassium solubilization. In: Meena VS, Maurya BR, Verma JP, Meena RS (eds) Potassium solubilizing microorganisms for sustainable agriculture. Springer, New Delhi, pp 43–59. https://doi.org/10.1007/978-81-322-2776-2_4
Ramos HJ, Roncato-Maccari LD, Souza EM, Soares-Ramos JR, Hungria M, Pedrosa FO (2002) Monitoring Azospirillum-wheat interactions using the gfp and gusA genes constitutively expressed from a new broad-host range vector. Aust J Biotechnol l97(3):243–252
Rawat J, Sanwal P, Saxena J (2016) Potassium and its role in sustainable agriculture. In: Meena VS, Maurya BR, Verma JP, Meena RS (eds) Potassium solubilizing microorganisms for sustainable agriculture. Springer, New Delhi, pp 235–253. https://doi.org/10.1007/978-81-322-2776-2_17
Reinhold-Hurek B, Hurek T (1997) Azoarcus spp. and their interactions with grass roots. Plant Soil 194:57–64
Reinhold-Hurek B, Hurek T (2011) Living inside plants: bacterial endophytes. Curr Opin Plant Biol 14:435–443
Reinhold-Hurek B, Hurek T, Claeyssens M, Van Montagu M (1993) Cloning, expression in Escherichia coli, and characterization of cellulolytic enzymes of Azoarcus sp., a root-invading diazotroph. J Bacteriol 175:7056–7065
Richardson AE, Barea JM, McNeill AM, Prigent-Combaret C (2009) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321:305–339
Riggs PJ, Chelius MK, Iniguez AL, Kaeppler SM, Triplett EW (2001) Enhanced maize productivity by inoculation with diazotrophic bacteria. Aust J Plant Physiol 28:829–836
Rocha FR, Papini-Terzi FS, Nishiyama MY, Vêncio RZN, Vicentini R, RDC D, De Rosa VE Jr, Vinagre F, Barsalobres C, Medeiros AH, Rodrigues FA, Ulian EC, Zingaretti SM, Galbiatti JA, Almeida RS, AVO F, Hemerly AS, Silva-Filho MC, Menossi M, Souza GM (2007) Signal transduction-related responses to phytohormones and environmental challenges in sugarcane. BMC Genomics 8(1):1
Rothballer M, Schmid M, Hartmann A (2003) In situ localization and PGPR-effect of Azospirillum brasilense strains colonizing roots of different wheat varieties. Symbiosis 34(3):261–279
Saha M, Maurya BR, Bahadur I, Kumar A, Meena VS (2016a) Can potassium-solubilising bacteria mitigate the potassium problems in India? In: Meena VS, Maurya BR, Verma JP, Meena RS (eds) Potassium solubilizing microorganisms for sustainable agriculture. Springer, New Delhi, pp 127–136. https://doi.org/10.1007/978-81-322-2776-2_9
Saha M, Maurya BR, Meena VS, Bahadur I, Kumar A (2016b) Identification and characterization of potassium solubilizing bacteria (KSB) from indo-Gangetic Plains of India. Biocatal Agric Biotechnol 7:202–209
Sahai R, Saxena AK, Tilak KV (2015) Effect of Gluconacetobacter diazotrophicus on sweet sorghum (Sorghum bicolor) in tropical semi-arid soil. Agribiol Res 4(4):347–353
Santi C, Bogusz D, Franche C (2013) Biological nitrogen fixation in non-legume plants. Ann Bot 111(5):743–767
Saravanan VS, Madhaiyan M, Osborne J, Thangaraju M, Sa TM (2008) Ecological occurrence of Gluconacetobacter diazotrophicus and nitrogen-fixing Acetobacteraceae members: their possible role in plant growth promotion. Microb Ecol 55(1):130–140
Sarig S, Okon Y, Blum A (1992) Effect of Azospirillum brasilense inoculation on growth dynamics and hydraulic conductivity of Sorghum bicolor roots. J Plant Nutr 15(6–7):805–819
Shaharoona B, Arshad M, Zahir ZA (2006) Effect of plant growth promoting rhizobacteria containing ACC-deaminase on maize (Zea mays L.) growth under axenic conditions and on nodulation in mung bean (Vigna radiata L.) Lett Appl Microbiol 42:155–159
Shahzad R, Waqas M, Al K, Asaf S, Khan MA, Kang S, Yun B, Lee I (2016) Seed-borne endophytic Bacillus amyloliquefaciens RWL-1 produces gibberellins and regulates endogenous phytohormones of Oryza sativa. Plant Physiol Biochem 106:236–243
Sharma A, Shankhdhar D, Shankhdhar SC (2016) Potassium-solubilizing microorganisms: mechanism and their role in potassium solubilization and uptake. In: Meena VS, Maurya BR, Verma JP, Meena RS (eds) Potassium solubilizing microorganisms for sustainable agriculture. Springer, New Delhi, pp 203–219. https://doi.org/10.1007/978-81-322-2776-2_15
Shi Y, Lou K, Li C (2009) Promotion of plant growth by phytohormone producing endophytic microbe of sugar beet. Biol Fertil Soils 45:645–653
Shrivastava M, Srivastava PC, D’Souza SF (2016) KSM soil diversity and mineral solubilization, in relation to crop production and molecular mechanism. In: Meena VS, Maurya BR, Verma JP, Meena RS (eds) Potassium solubilizing microorganisms for sustainable agriculture. Springer, New Delhi, pp 221–234. https://doi.org/10.1007/978-81-322-2776-2_16
Sindhu SS, Parmar P, Phour M, Sehrawat A (2016) Potassium-solubilizing microorganisms (KSMs) and its effect on plant growth improvement. In: Meena VS, Maurya BR, Verma JP, Meena RS (eds) Potassium solubilizing microorganisms for sustainable agriculture. Springer, New Delhi, pp 171–185. https://doi.org/10.1007/978-81-322-2776-2_13
Singh NP, Singh RK, Meena VS, Meena RK (2015) Can we use maize (Zea Mays) rhizobacteria as plant growth promoter? Vegetos 28(1):86–99. https://doi.org/10.5958/2229-4473.2015.00012.9
Singh M, Dotaniya ML, Mishra A, Dotaniya CK, Regar KL, Lata M (2016) Role of biofertilizers in conservation agriculture. In: Bisht JK, Meena VS, Mishra PK, Pattanayak A (eds) Conservation agriculture: an approach to combat climate change in Indian Himalaya. Springer, Singapore, pp 113–134. https://doi.org/10.1007/978-981-10-2558-7_4
Sorty Am, Meena KK, Choudhary K, Bitla UM, Minhas PS, Krishnani KK (2016) Effect of plant growth promoting bacteria associated with halophytic weed (Psoralea corylifolia L) on germination and seedling growth of wheat under saline conditions. Appl Biochem Biotechnol 180(5):872–882
Stets MI, Pinto AS, Huergo LF, Souza EM, Guimarães VF, Alves AC, Steffens MBR, Monteiro RA, Pedrosa FO, Cruz LM (2013) Rapid identification of bacterial isolates from wheat roots by high resolution whole cell MALDI-TOF MS analysis. J Biotechnol 165(3):167–174
Suman A, Gaur A, Shrivastava AK, Yadav RL (2005) Improving sugarcane growth and nutrient uptake by inoculating Gluconacetobacter diazotrophicus. Plant Growth Regul 47(2–3):155–162
Syranidou E, Christofilopoulos S, Gkavrou G, Thijs S, Weyens N, Vangronsveld J, Kalogerakis N (2016) Exploitation of endophytic bacteria to enhance the phytoremediation potential of the wetland helophyte Juncus acutus. Front Microbiol 7:1016
Teotia P, Kumar V, Kumar M, Shrivastava N, Varma A (2016) Rhizosphere microbes: potassium solubilization and crop productivity-present and future aspects. In: Meena VS, Maurya BR, Verma JP, Meena RS (eds) Potassium solubilizing microorganisms for sustainable agriculture. Springer, New Delhi, pp 315–325. https://doi.org/10.1007/978-81-322-2776-2_22
Thomas P, Reddy KM (2013) Microscopic elucidation of abundant endophytic bacteria colonizing the cell wall–plasma membrane peri-space in the shoot-tip tissue of banana. AoB plants, 5, plt011
Tien TM, Gaskins MH, Hubbell DH (1979) Plant growth substances produced by Azospirillum brasilense and their effect on the growth of pearl millet (Pennisetum americanum L.) Appl Environ Microbiol 37(5):1016–1024
Upadhyay SK, Singh JS, Saxena AK, Singh DP (2012) Impact of PGPR inoculation on growth and antioxidant status of wheat under saline conditions. Plant Biol 14(4):605–611
Van VT, Berge O, Ke S, Balandreau J, Heulin T (2000) Repeated beneficial effects of rice inoculation with a strain of Burkholderia vietnamiensison early and late yield components in low fertility sulphate acid soils of Vietnam. Plant Soil 218(1–2):273–284
Velazquez E, Silva LR, Ramírez-Bahena MH, Peix A (2016) Diversity of potassium-solubilizing microorganisms and their interactions with plants. In: Meena VS, Maurya BR, Verma JP, Meena RS (eds) Potassium solubilizing microorganisms for sustainable agriculture. Springer, New Delhi, pp 99–110. https://doi.org/10.1007/978-81-322-2776-2_7
Verma SC, Ladha JK, Tripathi AK (2001) Evaluation of plant growth promoting and colonization ability of endophytic diazotrophs from deep water rice. J Biotechnol 91(2):127–141
Verma SC, Singh A, Chowdhury S, Tripathi AK (2004) Endophytic colonization ability of two deepwater rice endophytes, Pantoea sp and Ochrobacterium sp using green florescent protein reporter. Biotechnol Lett 26:425–429
Verma R, Maurya BR, Meena VS (2014) Integrated effect of bio-organics with chemical fertilizer on growth, yield and quality of cabbage (Brassica oleracea var capitata). Indian Journal of Agricultural Sciences 84(8):914–919
Verma JP, Jaiswa DK, Meena VS, Meena RS (2015a) Current need of organic farming for enhancing sustainable agriculture. J Clean Prod 102:545–547
Verma JP, Jaiswal DK, Meena VS, Kumar A, Meena RS (2015b) Issues and challenges about sustainable agriculture production for management of natural resources to sustain soil fertility and health. J Clean Prod 107:793–794
Walker V, Couillerot O, Von Felten A, Bellvert F, Jansa J, Maurhofer M, Bally R, Moënne-Loccoz Y, Comte G (2012) Variation of secondary metabolite levels in maize seedling roots induced by inoculation with Azospirillum, Pseudomonas and Glomus consortium under field conditions. Plant Soil 356:151–163
Westhoff P (2009) The economics of biological nitrogen fixation in the global economy. In: Emerich DW, Krishnan HB (Eds) Nitrogen fixation in crop production. Agronomy monograph no. 52. Madison, WI: J Am Soc Agronl309–328
Xu T, Zeng X, Yang X Shanshan Yuan S, Hu X, Zeng J, Wang Z, Liu O, Liu Y, Liao H, Tong C, Liu X, Zhu Y (2017) Isolation and evaluation of endophytic Streptomyces endus OsiSh-2 potential application for biocontrol of rice blast disease. J Sci Food Agric 97(4):1149–1157
Yadav BK, Sidhu AS (2016) Dynamics of potassium and their bioavailability for plant nutrition. In: Meena VS, Maurya BR, Verma JP, Meena RS (eds) Potassium solubilizing microorganisms for sustainable agriculture. Springer, New Delhi, pp 187–201. https://doi.org/10.1007/978-81-322-2776-2_14
Yanni YG, Rizk RY, Corich V, Squartini A, Ninke K, Philip-Hollingsworth S, Orgambide G, Bruijn F, Stoltzfus J, Buckley D, Schmidt TM, Mateos PF, Ladha JK, Dazzo FB (1997) Natural endophytic association between Rhizobium leguminosarum bv. trifolii and rice roots and assessment of its potential to promote rice growth. Plant Soil 194(1–2):99–114
Yanni YG, Rizk RY, El-Fattah FKA, Squartini A, Corich V, Giacomini A, Bruijn F, Rademaker J, Maya-Flores J, Ostrom P, Vega-Hernandez M, Hollingsworth RI, Martinez-Molina E, Mateos PF, Velazquez E, Wopereis J, Triplett E, Umali-Garcia M, Anarna JA, Rolfe BG, Ladha JK, Hill J, Mujoo R, Dazzo NPKFB (2001) The beneficial plant growth-promoting association of Rhizobium leguminosarum bv. trifolii with rice roots. Funct Plant Biol 28(9):845–870
Yanni YG, Dazzo FB, Squartini A, Zanardo M, Zidan MI, Elsadany AEY (2016) Assessment of the natural endophytic association between Rhizobium and wheat and its ability to increase wheat production in the Nile delta. Plant Soil:1–17
Yasin M, Munir I, Faisal M (2016) Can bacillus spp. enhance K+ uptake in crop species. In: Meena VS, Maurya BR, Verma JP, Meena RS (eds) Potassium solubilizing microorganisms for sustainable agriculture. Springer, New Delhi, pp 163–170. https://doi.org/10.1007/978-81-322-2776-2_12
Zahedi H (2016) Growth-promoting effect of potassium-solubilizing microorganisms on some crop species. In: Meena VS, Maurya BR, Verma JP, Meena RS (eds) Potassium solubilizing microorganisms for sustainable agriculture. Springer, New Delhi, pp 31–42. https://doi.org/10.1007/978-81-322-2776-2_3
Acknowledgements
The authors acknowledge financial support provided by the Spanish Government (Ministerio de Economía y Competitividad; MINECO) through the projects AGL2011-29227 and AGL2015-70510-R, by the Junta de Castilla y León (regional government) through the project JCyL SA169U14 and by the Diputación de Salamanca (local government) through the project V113/463AC06. AJG is thankful to a PhD grant from the Spanish Government (Ministerio de Educación, Cultura y Deporte). The authors are grateful to Emma Jane Keck for correcting English style.
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Celador-Lera, L., Jiménez-Gómez, A., Menéndez, E., Rivas, R. (2018). Biofertilizers Based on Bacterial Endophytes Isolated from Cereals: Potential Solution to Enhance These Crops. In: Meena, V. (eds) Role of Rhizospheric Microbes in Soil. Springer, Singapore. https://doi.org/10.1007/978-981-10-8402-7_7
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