Abstract
Endophytic bacteria exert beneficial effects on various crop plants especially the non-legumes, and the effects are carried out in multidimensional mechanisms unlike the biological N2 fixation (BNF) process. They create a conducive environment in the apoplastic area of root tissues as well as in shoot for providing benefits to the host plant. Among the endophytic bacteria, recently, Bacillus spp. are gaining prominence as a biofertilizer and bioenhancer for crop production. A large number of species and strains of this genera have been isolated and identified from the diversified crop plants such as rice, wheat, maize, alfalfa, banana, black pepper, canola, cucumber, clover, oil palm, and apple. Inoculation of plants with these endophytic Bacilli resulted in various beneficial effects on the colonization including better nutrition, improvement of growth, yield, and quality of crop plants. A significant amount of atmospheric N2 is fixed and incorporated into a good number of non-legumes like rice, wheat, maize, banana, oil palm etc. that are confirmed by the 15N isotopic dilution technique. The Bacillus spp. are found in the apoplastic area, produce phytohormone especially auxin, and excrete their fixed N2 as ammonium to the host plant cells. Additionally, these endophytes are also able to enhance the accumulation of P, K, and Ca through the stimulation of cell membrane-ATP-ase activity. The Bacillus spp. are also capable to solubilize complex rock phosphate to a simpler form of phosphate, i.e. dihydrogen orthophosphate and monohydrogen orthophosphate, and help plant phosphorus nutrition. Besides, they produce siderophores, which are very much effective in iron uptake in diversified crop plants. Therefore, the endophytic Bacilli are considered as microbial agents for enhancing uptake and better utilisation of nutrients in different crop plants under normal and harsh environmental conditions. This chapter updates our understanding of nutrient accumulation in non-legumes crop plants by endophytic Bacillus spp.
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16.1 Introduction
Endophytic bacteria thrive and colonize in the internal tissue of the plant showing no external sign of infection or adverse effect on the host plant (Afzal et al. 2019; Holliday 1989; Schulz and Boyle 2006). Generally, they complete their life cycle partially or wholly inside the plant and inhabited in the apoplastic area, i.e. intercellular space or middle lamella of epiblema, cortical tissue of roots, or in the xylem vessel of stem and even in the leaf as well (Xia et al. 2015). They can be regarded either as obligate or facultative endophytes where obligates are not culturable and require a more specific environment for their growth. On the contrary, the facultative endophytes are able to survive in soil, rhizosphere, artificial medium, and inside the plants. The facultative endophytes are widely distributed throughout the plant biota for their advantage of growth potentiality, higher adaptability under adverse conditions. The most common endophytes were isolated from wild or cultivated crops of monocotyledonous and dicotyledonous plants. They may be classified as actinomyces, bacteria, and fungi depending on the microorganism, with bacterial and fungal endophytes being the most studied organisms. The interactions between endophytes and the host plants are complex which involve mutualism and antagonism, and the association might be obligate or facultative. Nearly 300,000 plant species are present on earth, and each individual plant is host to one or more endophytes (Strobel et al. 2004). Only a few of these plants have ever been completely studied in relation to their endophytic biology. Hence, the potentiality to explore this arena is crucial, in order to boost up the biofertilizer development in a sustainable approach. Plant growth-promoting bacterial endophytes (PGPBE) have also been identified which promote plant growth and development in versatile approaches (Mia et al. 2016). Their identification as PGPEBE is attributed to their role in enhancing plant growth using various traits namely production of ammonia, indole-3-acetic acid (IAA), siderophores, N2 fixation, and accumulation of essential nutrient elements viz. P, K, Ca, Mg, and Fe (Mia et al. 2009). Several rhizospheric or endophytic bacteria belonging to the genera Azospirillum, Azotobacter, Burkholderia, Bacillus, Enterobacter, Pseudomonas, Rhizobium, and Agrobacterium have been noted as plant growth-promoting (PGP ) microorganisms (Vessey 2003). Among them, Bacillus is frequently reported as a potential biofertilizer due to its multifunctional PGP traits namely, phosphate solubilisation, IAA production accumulation of nutrients, siderophore (iron chelator) production, and biopesticidal activity (Bahadir et al. 2018; Bjelić et al. 2018; Mohite 2013; Wahyudi et al. 2011, 2020). In addition, biofertilizers containing Bacillus strains are considered important because of their spore-forming capacity, allowing their adaptation to extreme abiotic conditions, like extreme temperatures, pH, or pesticide exposure. These species have been shown to have positive effects on soybean seed germination by enhancing the root and shoot length or the number of lateral roots of the seedling, which is related to the production of phytohormone and siderophore, and the capability of these bacteria to solubilize P complex. It has also been reported that Bacillus promoted seed germination and growth of tomato, pepper, eggplant, and rice (Mia and Shamsuddin 2013; Beneduzi et al. 2008). Other studies also revealed that Bacillus have improved plant growth under drought stress and produced a variety of compounds that can be used for the management of a wide array of plant pathogens. Bacteria viz. B. megaterium, B. cereus, B. pumilus, B. circulans, B. licheniformis, B. subtilis , B. brevis, and B. firmus have been recognised as N2 fixers based on their nitrogenase activity (Radhakrishnan et al. 2017). It is the most abundant genus in the rhizosphere, and the PGP activity of some of these strains has been known for many years. There are several metabolites that are released by these strains, which strongly affected the environment by increasing nutrient availability in the plants (Barriuso and Solano 2008).
Currently, one of the major challenges of agriculture is to boost up crop productivity under adverse environmental conditions, especially poor fertile soils having less availability of nutrients. It is interesting to note that microbes that are beneficial to plants are used to enhance crop yield and are alternatives to chemical fertilizers. Additionally, several endophytic Bacillus species have emerged as a complementary, efficient, and safe alternative to current crop management practices. It is reported that endophytic Bacillus is not host-specific, can colonize a wide array of crop plants, and this gives it a great potential tool for increasing crop productivity in a sustainable manner. This chapter reviews current knowledge on the roles of endophytic Bacilli in nutrient accumulation in non-legume crop plants.
16.2 Beneficial Effects of Endophytes on Accumulation of Nutrients in Non-legumes
The major contributions of beneficial and biofertilizer endophytes are to supply nutrients like fixed N2, enhanced uptake of other essential nutrients like P, K, Zn, and Fe. However, limited information are available on the direct contribution of endophytes to host plant like legume-Rhizobium symbiosis process (Hardoim et al. 2008). Nevertheless, endophytes mediate plant growth promotion through direct and indirect mechanisms. Since they start their journey as rhizosphere bacteria, it is assumable that they may retain their attributes inside the plant. Their mechanisms of beneficial effects seem related to rhizosphere bacteria because most endophytes can be cultured and can survive outside of the host in the rhizosphere. A list of endophytic Bacilli performs beneficial effects has been presented in Table 16.1.
16.2.1 Mechanism of Beneficial Effects of Bacillus Spp. on Plants
Unlike nutrient accumulation, they can directly benefit plants by providing nitrogen supply via N2 fixing abilities iron chelators and siderophore production (Long et al. 2008), P complex solubilizing compounds and (Knoth 2014). In addition, they influence on plant growth through the production of phytohormones especially auxin which increased root growth through hair formation, increased lateral roots, volume, and surface area. Also, several S oxidizing endophytes are known which can oxidize elemental S into SO42+ to be used by plants (Banerjee and Yesmin 2009). Moreover, endophytes are prolific sources of phytochemicals (Nisa 2015) which impede plant hygiene (Chen 2011; Benhamou et al. 1998). They are also excellent sources of biologically active secondary metabolites and contributing to the production of metabolites (Brader 2014; Schulz and Boyle 2002).
16.2.2 Phytohormone Production in Relation to More Root Growth for Higher Nutrient Uptake
Plant growth promotion by endophytic Bacillus spp. , through phytohormone production, is perhaps the well-agreed method which causes morphological and anatomical changes in roots of the plant. The mechanism of phytohormones production by endophytic Bacillus in host plants is similar to plant growth-promoting rhizobacteria. But here, the roots get extra benefits for proper utilisation of synthesized auxin, since the endophytes remain in the apoplastic areas. There are several pathways to produce auxin where endophytes mainly follow the tryptophan precursor–mediated pathways. Whatever the pathways followed for auxin synthesis, the products are released in the apoplastic area of root cortical zone transported to endodermis through apoplastic and symplastic pathways via downhill process. The endodermis releases auxin to the pericycle, located just beneath it; the auxin stimulates the pericycle to convert into meristem consequently form the lateral roots primordia and finally, produced the lateral roots as well as the root hair (Péret et al. 2009; Waidmann et al. 2020). The increased root growth facilitated the plants to absorb more nutrients through root interception, which is one of the mechanisms of nutrient uptake (Marschner 1995).
16.2.3 Atmospheric Nitrogen (N2) Fixation
Nitrogen is one of the most important nutrient elements which limits crop yield under deficient conditions. The main source of N is the atmospheric N2, which is unavailable to crop plants due to strong triple bond (N ≡ N), which must be reduced by the fixation process. Biological N2 fixation is the most significant where a large amount of N2 is fixed by various types of symbiotic associative free-living and endophytic bacteria in association with plants, both of dicotyledon and monocotyledon. The process is mediated by the activity of enzyme nitrogenase using ATP and the overall reaction is shown as follows:
Diazotrophic endophytes can fix a handsome amount of N2, which have been recorded in rice, wheat, maize, sugarcane, oil palm, and bananas, and have been documented by various researchers (Mia et al. 2007, 2010a; Amir et al. 2001; Bashan and Holguin 1997). The mechanism of fixing N2 by nitrogenase enzyme present in the endophytes are very much similar to Rhizobium species symbiosis with legumes, and their genomes possess an nifHDK operon, encoding both nitrogenase components: the nitrogenase protein (MoFe protein, NifDK), which contains a molybdenum–iron cofactor in the prosthetic group (Carvalho et al. 2014). The nitrogenase enzyme is encoded by ~20 genes which are termed as nif genes (N-fixation genes) that are organised in seven operons (nif cluster) spanning over 24 kb. The nifH gene encodes the Fe protein and nif D and nifK genes encode the Mo-Fe protein of the nitrogenase enzyme (Rubio and Ludden 2008; Seefedt et al. 2009). The fixed N2 could be confirmed and measured by several methods like acetylene reduction assay (ARA), 15N isotopic both enrichment and dilution techniques. The ARA technique is a qualitative measure for the activity of enzyme nitrogenase and can be used under certain cases and conditions (Mia and Shamsuddin 2010; Danso 1985). The 15N isotopic technique is used to provide a direct method for detecting BNF (Danso 1995), which comprises enrichment and dilution techniques. The 15N isotope dilution technique was used to quantify the contribution of BNF to clover legume by McAuliffe et al. (1958) which has the capacity to separate out any plant-associated contribution of BNF to plants and is recognised as a more accurate method (Boddey et al. 1996; Roger and Ladha 1992).
The microbial bioassay where isolated endophytes could be cultured specific N-free cultural media and specific conditions and can be quantified by the degree of growth of endophytic bacteria (Das and De 2018). Cell sap analysis is another technique of estimating N2-fixation where analysis of N solute in xylem exudates and plant parts is based on the determination of the composition of N compounds in plant tissues or N flowing through the xylem sap to the shoot, although the method has some limitation as only a small proportion of known N2 fixing plants are ureide exporters (Mia and Shamsuddin 2010). A list of N2-fixing Bacilli spp. has been presented in Table 16.2.
A good number of endophytic Bacillus spp. have been identified based on the nitrogenase activity like B. megaterium, B. cereus, B. pumilus, B. circulans, B. licheniformis, B. subtilis , B. brevis, and B. firmus (Xie et al. 1998). One of the plant-associated members, viz. B. sphaericus strain UPMB10, fixes a substantial amount of atmospheric N2 in association with various non-legumes, including, banana, oil palms, and sweet potato (Mia et al. 2007, 2010a; Mia and Shamsuddin 2010; Mia et al. 2013). The strain UPMB10 has been evaluated for their N2-fixing capacities in association with oil palm seedlings, banana, rice, and vegetable soybean through ARA and 15N isotopic dilution technique (Mia et al. 2007). Inoculation with B. spharecus strain UPMB10 could fix 37–39%N2 in banana tissue cultured plantlets enumerated by 15N isotopic dilution technique. The highest % Ndfa (nitrogen derived from atmosphere) was recorded at the lowest fertilizer-N applied plant with strain UPMB10. Generally, % Ndfa declined with an increase in fertilizer N application, making a lower contribution of N2 fixed to the total plant N. The confirmation of N2 fixation was supported by higher ARA values (129 ηmole plant−1 hour−1) in roots of inoculated plants (Mia et al. 2007). In field conditions, rice plants could obtain 20% of their total N requirement and 25–50% of N for oil palm in nursery condition by rhizobacterial inoculation (Shrestha and Ladha 1996; Amir et al. 2001). In a greenhouse study on sugarbeet, three different Bacillus isolates fixed N2 and increased growth (Çakmakçi et al. 2006). Enhanced accumulation of N in sweet sorghum by inoculation of Bacillus spp. were recorded by Ribeiro et al. (2018). In another study, Hafeez et al. (2006) noted that selected Bacillus sp. used as bioinoculants on wheat resulted in increased root length, plant biomass, and higher accumulation of N and P. Generally, they are widely used in crop production system and are important P-solubilizing inocula, resulting in improved growth and yield of crops (Prakash and Arora 2019).
The production of plant growth regulators such as auxin, cytokinin, and gibberellin by these bacteria may also give additional support to the growth and development of host plant species (Joo et al. 2009; Kang et al. 2009). Recent literature indicates that Bacillus sp. have a positive role in plant growth enhancement and biologically active metabolites production (Indiragandhi et al. 2008; Kang et al. 2009). Shen et al. (2019) isolated B. aryabhattai E7, B. aryabhattai MN1, and B. fortis T9 from rice seedling roots and found that these strains have both N2 fixation potential and IAA production abilities. Sequence analyses of endophytic Bacilli in banana cv. ‘Prata Anã’ roots revealed that PCR amplification of the nifH gene was detected in 24 of the 102 bacterial isolates. Seven species of Bacillus were nifH-positive, including: B. amyloliquefaciens, B. cereus, B. flexus, B. licheniformis, B. pumilus, B. subtilis , and B. tequilenses (Suzane et al. 2013). Çakmakçi et al. (2006) observed that three different Bacilli isolates fixed N2 and increased growth in sugar beet in a greenhouse study. A good number of endophytic and associative Bacillus spp. have been commercialized as bioinoculants for the growth of crop plants (Islam and Hossain 2013).
16.2.4 Transfer of Fixed N2 to Host Cell
Whatever the amount of N2 fixed by endophytes, the release and transportation of fixed N2 to the host tissues is of the greatest importance. The release or excretion of NH4+ and subsequent transportation to the host cell is not clearly identified in the case of associative bacteria since very little amount of N2 is fixed, which is most probably being utilized by the bacteria itself. Nevertheless, several strains of endophytic bacteria have a unique N regulation system where the NH4+ is excreted out of the cell through simple diffusion despite accumulation in its own cell (Brewin et al. 1999; Castorph and Kleiner 1984; Day et al. 2001; Kleiner 1982). The excreted NH4+ are transported to cytoplasm via ion channel or plasmodesmata either by downhill or uphill process thereafter being utilized via GS-GOGATT pathway for the synthesis of amino acid and subsequently, other amino acids through transamination process (Mia 2015).
16.2.5 Solubilisation of Soil Insoluble Phosphates
Apart from N2 fixation, several endophytes release organic acids into the soil which solubilize the phosphate complexes and convert them into ortho-phosphate for plant uptake and utilisation. Although phosphorous exist abundantly in soils, most of it remains unavailable as an insoluble form (Miller 2010). Endophytic Bacillus is capable to solubilize the complex unavailable rock phosphate to an available form of P where inoculation of Bacillus spp. could solubilize the P-Fe minerals and enhanced uptake of P and Fe in pearl millet (Ribeiro et al. 2018). A good number of Bacillus spp. have been isolated from bananas and aerobic rice by Matos et al. (2017) and Panhwar et al. (2009), which are very much effective in the solubilisation of rock phosphate. Rhizobacteria B. methylotrophicus CKAM isolated from apple roots showed higher P- solubilisation (Mehta et al. 2014). Similarly, the application of B. megatorium in combination with fish bone produced the highest amount of available P for crop plants (Saeid et al. 2018). One of the most important mechanisms is the production of organic acid and release to the soil to solubilize monocalcium, bicalcium, and tricalcium complex phosphate to simpler phosphate as well as increase the activity of phosphatase. The concentration of organic acid is released through root exudates is decreased with increasing the presence of complex phosphate in the rhizosphere.
16.2.6 Enhancement of K Uptake by Plants
Potassium is an essential macronutrient element that contributes to the growth and development of crop plants by influencing the activities of various enzymes system. This element has non-specific functions not directly involved in any reaction system in the cell and do physiological functions in the various arena through osmoregulatory, enzymetic regulation, charge balance in the cytosole (Mia 2015). The greatest amount of K is found in the plant body which is highly mobile in the plant system. Although higher quantities of K present in the soil plant cannot take this element as those are fixed and unavailable for the plants. Recently, the use of potassium solubilizing bacteria (KSB) viz. Acidothiobacillus ferrooxidans, Paenibacillus spp., B. mucilaginosus, B. edaphicus, and B. circulans have shown to solubilize K- bearing minerals, like biotite, feldspar, illite, muscovite, orthoclase, and mica. This type of bacteria can dissolve silicate minerals and release K through the production of organic and inorganic acids, acidolysis, polysaccharides, and complexolysis, chelation, and exchange reactions. The application of B. sphaericus strain UPMB10 could not increase the K concentration but its total accumulation was greatly increased due to higher (36%) dry matter production in tissue-cultured banana plantlets growth under a hydroponic condition where dry matter production is directly related to K accumulation. The higher accumulation of K might be due to enhanced root proliferation from the inoculation process (Mia et al. 2010a). Anyway, the KSB have a greater impact on the release of K by various mechanisms. Inoculation of KSB Bacillus strain B2084 and B2088 increased the higher accumulation K in a shoot of pearl millet (Ribeiro et al. 2018). The endophytes may also have functions in providing K for a plant by increasing root exudates through supplying different chemicals which can lower the pH by proton efflux, enhancing chelation of the cation bonds to K, and acidolysis of the fixed K area of the soil (Etesami et al. 2017; Meena et al. 2014).
16.2.7 Improvement of Ca Uptake and Absorption by Plants
The endophytic PGPB inoculation greatly increased Ca concentration (nearly 14%) in root especially in plants inoculated along with supplemental 33% fertilizer-N in banana. However, inoculation without fertilizer-N, which could not show any increment, indicated the requirement of starter inorganic N. As Ca is a non-mobile element in the plant system, a higher concentration is found in the root and no influence has been observed in the pesudostem and leaf. Similarly, inoculated plants provided with 33% fertilizer-N also showed lower concentrations when compared to inoculated plants without fertilizer-N. However, in leaf, application of 100% fertilizer-N showed lower Ca concentration (Mia et al. 2009).
The higher Ca uptake by the inoculated plants might not only be due to higher plant growth but also higher uptake capacity, which is induced by bacterial interaction through the acceleration of proton efflux, which results in the acidification of the rhizosphere. It is one of the important mechanisms in cation uptake by the roots, which is the consequence of stimulation of root membrane ATP-ase activity. The endophyte could increase this enzyme activity through bacteria-root interaction as both the strain successfully colonized banana roots. Higher activity of this enzyme resulted in higher Ca concentration in roots (Marschner 1995). Similarly, Bashan et al. (1989) concluded that Azospirillum could increase the proton efflux by stimulating ATP-ase activity in the root of wheat seedlings. Increased accumulation of Ca in the cytosole may be the stimulation of the Ca2+ ion channel consequently greater influx of Ca2+ from the apoplastic area.
16.2.8 Influence of Endophytic Bacilli on Uptake and Absorption of Mg by Plants
Magnesium is an essential macronutrient element which is mobile in the plant system. It plays an important role in the synthesis of chlorophyll molecule as it is the central atom of chlorophyll. Application of endophytic bacteria B. sphericus strain UPMB10 could not increase the concentration of Mg rather enhanced the total accumulation which is due to increased root growth not to general uptake rate as in Ca.
16.2.9 Influence of Bacillus Spp. on Siderophores Production and Iron Uptake
Iron is an important micronutrient element that performs many metabolic activities in the plant through the activation of many enzymes taking part as a prosthetic group. However, it is a problematic element in case of uptake and absorption by the plants because the ferric form (Fe3+) readily becomes insoluble in the soil. Therefore, crop plants suffer deficiency despite having sufficiency in the soil. Recently, the microbial siderophore technique in the uptake of iron is gaining prominence for boosting up crop productivity. It is a smaller molecule organic compound synthesize by microorganisms and is capable of absorbing ferric even under Fe-limited soil conditions thereby solving iron nutrition problems in crop plants. The Fe3+ siderophore complex can easily enter into cytosole and release the Fe3+ where it reduces as Fe2+for further utilisation (Saha et al. 2016). Similarly, endophytes also synthesize siderophore which can absorb and utilize Fe3+as like as rhizosphere bacteria. Endophytes produce small molecular compounds called siderophores, which are iron-chelating compounds that can make available iron to plants and deprive pathogens of iron (Compant et al. 2005). Out of the range of siderophore produced by endophytes, one with biocontrol properties are catecholate, hydroxymate, and/or phenolate types (Rajkumar 2010). Also, siderophores specifically help iron-deficient plants in fixing N2, since diazotrophs require Fe2+ and Mo factors for nitrogenase synthesis and functioning (Kraepiel 2009). The interaction between plants and beneficial bacteria can have a profound effect on plant health, growth, development, production, and soil quality.
Ribeiro et al. (2018) reported the capacity of four endophytic Bacillus strains to solubilize iron phosphate (Fe-P), produce siderophores and indole-acetic acid (IAA) in vitro, and evaluate their plant growth promotion ability in greenhouse conditions by inoculation into pearl millet cultivated in a P-deficient soil. All strains solubilized Fe-P, and three of them produced carboxylate-type siderophores and high levels of IAA in the presence of tryptophan.
16.3 Conclusion and Future Perspectives
Endophytic Bacillus spp. promote better nutrition and increase the yield of crop plants. These biologicals are highly potential tools for boosting crop productivity in a sustainable agricultural system. They exert beneficial effects on plants through multifaceted mechanisms. Recently, Bacillus spp. gaining prominence as potential candidates for endophytic biofertilisation. This chapter reviews the effect of these bacteria on the nutrient accumulation of non-legumes and discusses their mode of action. Our knowledge of molecular crosstalks between endophytic Bacillus spp. and host plants are limited (Alvin et al. 2014). Recent progress in genomics and post-genomics analytical methods enhances our understanding about the underlying molecular mechanisms of the beneficial effects of endophytic Bacilli on plants. Exploration of elite strains of endophytic Bacilli and their genes involved in exerting beneficial effects on plants would help us to apply them in sustainable and climate-smart agricultural systems. Furthermore, the application of the recently developed genome editing by the CRISPR-Cas toolkit would be helpful to design industrially powerful biofertilizers and growth promoters from the genus of plant endophytic Bacillus.
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Hossain, G.M.A., Ghazali, A.H., Islam, T., Mia, M.A.B. (2022). Enhanced Nutrient Accumulation in Non-leguminous Crop Plants by the Application of Endophytic Bacteria Bacillus Species. In: Islam, M.T., Rahman, M., Pandey, P. (eds) Bacilli in Agrobiotechnology. Bacilli in Climate Resilient Agriculture and Bioprospecting. Springer, Cham. https://doi.org/10.1007/978-3-030-85465-2_16
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