key: cord-0058030-yxps2dws
authors: Ghosh, Sougata; Bhagwat, Tanay; Webster, Thomas J.
title: Endophytic Microbiomes and Their Plant Growth-Promoting Attributes for Plant Health
date: 2020-11-11
journal: Current Trends in Microbial Biotechnology for Sustainable Agriculture
DOI: 10.1007/978-981-15-6949-4_11
sha: 3696f3a35622d518af07da298fdadd2b391943f8
doc_id: 58030
cord_uid: yxps2dws

Endophytes reside within internal tissues of living plants without causing any harm to the host. The influence of these microbial communities on plant growth, yield, stress, and disease resistance, has been identified as potential research priorities in agriculture. In this chapter, we aim to explore the diverse host–endophyte interactions for plant growth promotion and health. Initially, the colonization of endophytes in specific plant tissues is discussed along with their mechanism of entry, habitat selection, response to stimuli, and evasion of the plant immunity. Endophytic microbes promote plant growth through different types of direct and indirect mechanisms. Plant growth-promoting endophytes (PGPE) play a vital role in phytohormone production, nutrient acquisition, nitrogen fixation, and solubilization of minerals. Further, indirect mechanisms (like suppression of plant pathogens by producing volatile organic compounds, antagonizing agents, and quorum quenchers) are also discussed in detail. Siderophores production and the secretion of different hydrolytic enzymes like chitinases, glucanases, and proteases also help in the induction of systemic resistance and protection of the host plants. Bioactive metabolites derived from endophytes serve as excellent therapeutic agents and have potential applications in agriculture, cosmetics, pharmaceutical, and food industries. Hereby, this chapter highlights the scientific rationale behind using endophytic microbiomes as potential biofertilizers, biopesticides, and biocontrol agents.

Increasing crop yield has attracted wide attention in order to meet global demand considering the increase in the world's population. However, conventional farming practices have certain limitations under increasing challenges like shortage of fertile lands, climate change, pests, and other associated abiotic and biotic stress. Thus, various plant growth-promoting microbes are being explored as biofertilizers in agriculture which seems to be a promising innovation to provide viable and environmentally friendly solutions with the potential to ensure food security (Glick 2014) . However, this can only be achieved through in-depth knowledge about the underlying plant-microbe interactions. Microbes that reside within the plants without causing any negative impacts are called endophytes. Stimulation of plant defense responses is some inherent properties of endophytes (de Matos et al. 2001) .

Plants are significant atmospheric CO 2 fixers on Earth. The solar energy enables plants to utilize CO 2 and reduce it to glucose and further various carbonaceous compounds. Hence, plant-associated heterotrophic microbes derive carbon, nitrogen, and energy from the host plants (Vandenkoornhuyse et al. 2007 ). On the other hand, plants require the microflora for their growth and stress tolerance. Thus, mutualistic relationships and interdependence exist between microbes and their host plants (Thrall et al. 2007; Sharaff et al. 2020; Suman et al. 2016) . Potential uses of plantassociated bacteria as plant growth stimulating agents and management of soil as well as plant health have been portrayed in numerous literatures. Plant growthpromoting bacteria (PGPB) are associated with many, if not all, plant species and are commonly present in many environments (Bashan and Holguin 1998) . PGPB are generally plant growth-promoting rhizobacteria (PGPR) that colonize the root surfaces and the rhizosphere (the closely adhering soil interface). Some of these PGPR can also enter the root interior and establish endophytic populations. Prime sites for bacterial colonization are lateral root emergence sites, outer cell layers, root cortex, phloem, and xylem, which may occur both intracellularly and inside the apoplast (Fig. 11 .1).

Microbes can evade the endodermis barrier, moving from the root cortex to the vascular system, and eventually colonize as endophytes in roots, shoot, leaves, tubers, flowers, and other organs. Internal tissues of root, internodes, and leaves of grapevine are colonized by the PGPB Burkholderia sp. strain PsJN. Similarly, the surface and interior of roots, stems, and needles of lodgepole pine (Pinus contorta Dougl. var. latifolia Engelm.) harbor the diazotrophic bacterial strain Paenibacillus polymyxa P2b-2R (Liu et al. 2017) . A facultative intracellular symbiont of Methylobacterium extorquens strain DSM13060 was isolated from the Scots pine (Pinus sylvestris L.) shoot tips where the bacteria aggregated within the living cells surrounding the nucleus (Koskimäki et al. 2015) . Microbes adapt to particular internal tissue environment by varying its extent of colonization within host plant organs and tissues (Gray and Smith 2005; Rana et al. 2019b ). Consequently, close Liu et al. (2017) associations between endophytes and host plants are formed without causing any adverse effects to the plant. These endophytes do not cause harm to the plant and establish a mutualistic association with the host plant (Rana et al. 2019c ). This chapter covers diverse aspects of plant growth-promoting endophytic bacteria and fungus. Endophyte-associated distribution patterns; nutrient uptake, phytohormone production, and stress tolerance are elaborated with minute details. Further, their role in augmenting the phytoremediation potential of host plants is also discussed.

The term "endophyte" is a microbe that asymptomatically colonizes internal living tissues of plants (host) during a particular period of their life span (Stone et al. 2000) . Endophytes do not harm the host plant and can be isolated from surfacesterilized plant tissue or the inner tissues of the host plant (Hallman et al. 1997) . A few of these microbes are believed to actively infiltrate plant tissues through invading wounds or openings or using hydrolytic enzymes like pectinase and cellulase. Some endophytes emerge from the rhizosphere or phylloplane microflora, by infiltrating and colonizing root tissue as a passage to the xylem. However, on infection with endophytes, plants become healthy and exhibit enhanced tolerance to abiotic and biotic stress compared to their endophyte-free counterparts (Bonnet et al. 2000) . Endophytic microbes can be bacteria, actinomycetes, or fungi 2020a, c) .

It seems bacteria are most suitable for living inside plants by natural selection. The source of bacterial endophytes is microbial diversity of soil or rhizosphere and their clones. Endophytes are known for >120 years (Hardoim et al. 2009 ). In 1926, endophytic growth was recognized as a particular stage in the life of bacteria, described as an advanced stage of infection, and as having a close relationship with mutualistic symbiosis (Perotti 1926) . Since then, various endophytes are isolated from surface-disinfected plant organs (Henning and Villforth 1940) . Potatoassociated bacterial communities indicated, in a large study conducted, that species richness and diversity were lower for endophytes than the rhizosphere of potato (Berg et al. 2005) . However, the microbiome in the root endosphere is significantly less diverse compared to the microbiomes in the rhizosphere and bulk soil. Hence, roots can work as the most effective habitat filters, restricting community membership resulting in more narrowly defined lineages as the niche from soil to roots. Root endophytic bacterial communities are typically dominated by Proteobacteria ( ̴ 50% in relative abundance), Actinobacteria ( ̴ 10%), Firmicutes ( ̴ 10%), and Bacteroidetes ( ̴ 10%) apart from other bacterial phyla that include Chloroflexi, Cyanobacteria, Armatimonadetes, Verrucomicrobia, Planctomycetes, and Nitrospirae.

The presence of endophytes is thought to be ubiquitous in plants as they can be detected in almost all parts including root, shoot, leaves, internodes, and reproductive tissues as well. The differences between the endosphere microbiomes of the root and shoot determine the source of dominant endophytes in them. Rootassociated endophytes are primarily derived from soil, which then colonizes internal tissues of stems and leaves through the apoplast in xylem vessels. Therefore, it is common to have microbes of the plant leaf/shoot endosphere significantly overlapping with those in roots at both the taxonomic and functional levels. Recent molecular identification provides a strong evidence of diverse genera and species in endophytes. Kobayashi and Palumbo (2000) reported both Gram-positive and Gram-negative bacterial endophytes from different internal tissues of diverse plant species. Significant variations in populations of both indigenous and infiltrated endophytes were reported which might be attributed to the tissue type, source, plant age, time of sampling, and the environment. Interactions of the internal microflora of plants are needed to be investigated that might lead to beneficial effects due to their combined activities.

There is a deep underlying genetic basis for the differential colonization of various plant tissues by endophytes. Degradation of the cell wall facilitates entry of the bacteria within the interior for translocation to the apoplast. The genome of endophytic bacteria harbors numerous genes encoding cell wall-degrading enzymes (Straub et al. 2013) . Genes encoding plant polymer degrading enzymes like cellulases, endoglucanase, xylanases, cellobiohydrolases, and cellulose-binding proteins have been reported in high copy numbers in the metagenome of rice root endophytic bacterial communities (Sessitsch et al. 2012) . Bacteria in the phyllosphere may be Fig. 11 .2 A schematic representation of bacterial colonization patterns in a leaf. The picture shown on the left demonstrates that the presence of bacteria has been detected in the leaf petiole, midrib, and veins. The picture shown on the right is a magnified leaf cross section, which demonstrates that endophytic bacteria may not only colonize the apoplast but are also present intracellularly. Endophytic bacteria are believed to be able to ascend from roots to the leaf via the vascular tissues of the xylem and phloem. Adapted with permission from Liu et al. (2017) derived from soil or may have entered through natural openings (e.g., stomata and hydathodes), wounds, and cracks generated by wind, insects, and pathogen attacks (Vorholt 2012) . Figure 11 .2 shows that specific sites of bacterial colonization in a leaf are mostly upper epidermis cells, palisade mesophyll cells, xylem vessels as well as spaces between spongy mesophyll layer cells (Olivares et al. 1997) . Bacterial endophytes are detected in plant reproductive organs, such as flowers, fruits, and seeds, although in small numbers. Table 11 .1 represents various bacterial endophytes from crop plants. 

Benefits conferred by endophytes are well recognized but it may not always be clear which population of microorganisms (endophytes or rhizospheric bacteria) promotes plant growth. Differential gene expression might facilitate entry, colonization, and also plant growth promotion. Nitrogen fixation (Iniguez et al. 2004) or the production of phytohormones, by enhancing the availability of minerals (Sessitsch et al. 2004; Sturz et al. 2000) , may help to promote plant growth. Further endophytes may lay a critical role in biocontrol of phytopathogens as they colonize the same ecological niche. Various mechanism of biocontrol includes production of antifungal or antibacterial agents, siderophore production, nutrient competition, and induction of systematic-acquired host resistance or immunity (Thakur et al. 2020) . Endophytic microorganisms have the capacity to control pathogens, insects, and nematodes ). In some cases, they also have the capacity to accelerate seedling emergence and promote plant establishment under adverse conditions. Endophytes can confer metal resistance to plants and reduce metal toxicity due to their own metal resistance capability ).

A deficiency in macro and micronutrients in the soil is detrimental to crop yield and the affected plants become more prone to soil-borne pathogens such as Fusarium, Pythium, and Phytophthora. Hence chemical fertilizers, herbicides, fungicides, and pesticides are largely used in order to overcome the problems. However, these harmful and toxic chemicals pose a potential threat to human health and the environment as well (Aktar et al. 2009; . Endophytes enable the plants to overcome habitat-imposed abiotic and biotic stresses which otherwise result in major losses in plant yield. Endophytic bacteria are capable of promoting plant growth and development through a wide variety of not only direct mechanisms which include nutrient (e.g., phosphorous, nitrogen, and iron) acquisition and production of various phytohormones (Santoyo et al. 2016; Yadav et al. 2020 ) but also indirect mechanisms for plant growth promotion such as antagonistic effects toward phytopathogens (Compant et al. 2010; Rastegari et al. 2020a, b) . It also includes the production of defense-related enzymes like chitinase and β-1,3-glucanase, secreting antimicrobial compounds, lowering endogenous stress-related ethylene (ET), induction of systemic resistance (ISR), quenching the quorum sensing (QS) of phytopathogens, and competition for niche and/or resources (Compant et al. 2010; Glick 2014; Santoyo et al. 2016; Singh et al. 2020a ). In the following section, various direct and indirect mechanisms of plant growth promotion by endophytic bacteria are elaborated ).

Endophytes directly promote plant growth using various mechanisms that include phytohormone production, nutrient acquisition, nitrogen fixation, and solubilization of minerals.

Five types of phytohormones, e.g., ethylene, indole-3-acetic acid (IAA), cytokinins, gibberellins, and abscisic acid may play an important role in several stages such as cell elongation, cell division, tissue differentiation, and apical dominance. Both host plants and their endophytes can synthesize these hormones. Hormonal balance of the plant can be altered by plant-associated bacteria as well. Ethylene is an important example to show that the balance is most important for the effect of hormones. An ubiquitous plant hormone, it plays a vital role in plant growth and survival, to abiotic and biotic stresses including root initiation and nodulation, cell elongation, leaf senescence, abscission, and fruit ripening as well as auxin transport ). While normally considered as an inhibitor of plant growth and known as a senescence hormone, at reduced levels it can stimulate plant growth in Arabidopsis thaliana (Pierik et al. 2006) . Stress-mediated ethylene production inhibits root elongation, lateral root growth, and root hair formation. It is interesting to note that the endophytes can reduce the ethylene level. The compound 1-aminocyclopropane-1-carboxylate (ACC) is a precursor of ethylene in plants. ACC-deaminase-producing bacteria can degrade ACC into α-ketobutyrate and ammonia, which can be metabolized by the microbes as nitrogen source. Thus, bacteria-mediated reduction of endogenous ACC levels results in root growth (Glick 2005) . ACC deaminase-producing bacteria have an additional potential to protect plants against biotic and abiotic stress owing to the fact that ethylene is also a stress hormone Saleem et al. 2007 ).

Indole acetic acid (IAA), one of the most physiologically active auxins, is produced by various plant organs like young leaves and germinating seeds by utilizing the amino acid tryptophan. IAA plays a significant role in plant growth by bringing about apical dominance, promoting root development and proliferation, tropisms (phototropism in the case of shoots and gravitropism in the case of roots), and inducing cell division and differentiation (Tiwari et al. 2020 ). IAA is a common product of l-tryptophan metabolism by several endophytes leading to plant morphogenic effects. Evidence suggests that endophytes produce IAA while colonizing the internal plant tissues and thereby promoting plant growth. The Pseudomonas stutzeri P3 strain was found to produce IAA in Echinacea plants and help in the proliferation of these plants even after micropropagation, likewise, a number of bacteria such as Agrobacterium tumefaciens, A. rhizogenes, Pseudomonas savastanoi, Pseudomonas spp., Rhizobium spp., Bradyrhizobium spp., Azospirillum spp., and Acinetobacter spp. associated with the plants are known to produce IAA (Huddedar et al. 2002; Rao 1986; Baldi et al. 1991; Leinhos 1994) .

Nitrogen Improved nutrient acquisition helps to promote plant growth directly. Plantassociated microorganisms can supply macronutrients and micronutrients, most significant example being bacterial nitrogen fixation. Nitrogen-fixing bacteria can use root exudates (carbohydrates) and in return provide nitrogen to the plant that can be used for amino acid synthesis. Azospirillum, Burkholderia, and Stenotrophomonas are free-living nitrogen-fixing bacteria (Dobbelare et al. 2003) . Brazilian sugarcane requires minimum amounts of fertilizer and shows no N 2 deficiencies due to N 2 fixing endophytes within them. However, level of N 2 fixed by endophytes and amount available to the host plant is still needed to be investigated (Giller and Merckx 2003) . Different reports suggest that 30-80 kg N/ha/year are available (Boddey et al. 1995) . Under optimal conditions, some plant genotypes seem to obtain part of their N requirements from nitrogen fixation. Kallar grass grows in nitrogen-deficient soils in Pakistan and a diversity of Azoarcus spp. was recovered (Reinhold-Hurek et al. 1993) . Inside wheat, Klebsiella sp. strain Kp342 fixes N 2 that also increases maize yield in the field (Iniguez et al. 2004; Riggs et al. 2001) .

Similarly, nitrogen-fixing endophytes seem to relieve N 2 deficiencies of sweet potato (Ipomoea batatas) in N 2 -poor soils (Reiter et al. 2003) . Grasses growing in nutrient-poor sand dunes contain members of genera Pseudomonas, Stenotrophomonas as well as Burkholderia. Burkholderia endophytes could contribute nitrogen to the grasses because nitrogenase was detected in roots and cell walls of stems and rhizomes (Dalton et al. 2004) . Similarly, the endophytic genera Burkholderia, Rahnella, Sphingomonas, and Acinetobacter isolated from the stem of Populus trichocarpa and Salix sitchensis enhanced the growth of plants by providing abundant nitrogen owing to their nitrogen-fixing ability (Doty et al. 2009 ). Some endophytic bacteria possess both nitrogen fixation (e.g., nifH) and denitrification genes. The nitrogen-fixing isolates P. polymyxa P2b-2R isolated from lodgepole pine tissue could effectively colonize both rhizosphere and endosphere of maize plants resulting in plant growth promotion (Puri et al. 2016) .

Phosphorous (P) is an essential micronutrient that helps in the proper functioning of metabolic activities, glucose transport, development of roots, and many other physiological processes (Ahemad 2015) . Since more than 75% of applied phosphorus forms complexes and are unavailable for plant uptake, endophytes may either solubilize precipitated phosphates by acidification, chelation (i.e., PO 4 3− ), ion exchange, and release of organic acid or secrete extracellular acid phosphatase to mineralize organic phosphorus resulting in phosphorous availability to plants ( van der Hiejden et al. 2008; Kour et al. 2020a; Singh et al. 2020b) .

Endophytic bacteria possess the capacity to solubilize phosphates. It was suggested that the endophytic bacteria from soybeans may also participate in phosphate assimilation (Kuklinsky-Sobral et al. 2004) . Recently, de Werra et al. (2009) reported that Pseudomonas fluorescens CHA0 could reduce the pH of its surrounding environment that helps in solubilization of mineral phosphate. This acidification was strongly dependent gluconic acid-producing ability of the endophyte that can be strongly correlated with antagonistic activity against plant pathogens. Further, Idriss et al. (2002) demonstrated that plants inoculated with a phytase-secreting Bacillus amyloliquefaciens FZB45 under P-limitation may result in significant growth enhancement in maize seedlings compared to non-inoculated controls. However, there are no reports of naturally occurring endophytic bacteria with phytase-secreting ability .

Iron (Fe) is vital as iron-containing proteins involved in enzymatic reactions are essential for various physiological activities like transpiration (Bothwell 1995) . Iron exists in soil in highly insoluble ferric (Fe 3+ ) forms such as oxides, hydroxides, phosphates, and carbonates not available for plant uptake. Microbially secreted chelating agents (e.g., siderophores) help to solubilize Fe under conditions of iron deficiency. Siderophores, low-molecular weight organic compounds (500-1500 Da) having an affinity for Fe 3+ ions, also bind other bivalent metal ions or Fe 2+ that can be assimilated by the plant (Rajkumar et al. 2009 ). The siderophore is discussed in more detail in the indirect mechanisms section.

Indirect mechanisms mainly include the suppression of the growth or survival of plant pathogens (phytopathogens) and, thus, bring about the promotion of plant growth by microbial antagonism. Endophytes may produce substances like volatile organic compounds, antagonizing agents, and quorum quenchers that may effectively resist phytopathogen-associated disease. Further, siderophore production and secretion of diverse hydrolytic enzymes (such as chitinases, proteases, and glucanases) and induction of systemic resistance also protect the host plants (Sheoran et al. 2015; Mondal et al. 2020) .

The root surface and internal tissues of plants are significant carbon sinks (Rovira et al. 1965 ) and nutrient-rich niches that attract diverse groups of microbes including phytopathogens. PGPB protects plants by competing with the phytopathogens over these nutrients and niches (Duffy 2001) . Brock et al. (2013) reported that a potent endophyte, Enterobacter radicincitans DSM 16656, induced priming in Arabidopsis via SA-and JA/ET-dependent pathways. Likewise, endofungal bacterium R. radiobacter F4 exhibited nonspecific plant root colonization and enhanced plant resistance against the bacterial leaf pathogens Xanthomonas translucens pv. translucens and Pseudomonas syringae pv. tomato DC3000 (Liu et al. 2017) . However, it is yet to be investigated whether endophytes contribute to priming and ISR.

Endophytic bacteria produce volatile organic compounds (VOCs) that can render resistance to the host plants against the phytopathogens (Chung et al. 2016 ). On inoculation with endophytic Enterobacter aerogenes that produce VOC 2,3-butanediol (2,3-BD), maize plants exhibited increased resistance against Setosphaeria turcica associated northern corn leaf blight disease (D'Alessandro et al. 2014 ). The endophytic Pseudomonas poae strain RE*1-1-14 isolated from sugar beet roots suppressed the fungal pathogen Rhizoctonia solani (Zachow et al. 2015) . Further, P. poae produced a novel lipopeptide poaeamide that suppressed R. solani-associated pathogenesis in sugar beetroots. Similarly, endophytic B. amyloliquefaciens was reported to produce a series of isoforms of iturins that can confer protection to its host against pathogens (Han et al. 2015) . VOCs produced by P. fluorescens and Serratia plymuthica inhibited tumorigenic strains of A. tumefaciens and A. vitis induced crown gall disease in tomatoes. Solid-phase microextraction-gas chromatography-mass spectrometry analysis revealed dimethyl disulfide (DMDS) and 1-Undecene as the major VOCs produced by S. plymuthica IC1270 and P. fluorescens strains, respectively (Dandurishvili et al. 2011) .

Quorum sensing is an important phenomenon exhibited by numerous pathogenic microbes in order to survive in a specific ecological niche, communicate between cells, undergo multiplication, control biofilm formation, and induce competence and also adaptation (Miller and Bassler 2001) . Certain endophytic bacteria employ QS quenching as an antivirulence strategy to control phytopathogen. Endophytic bacterial strains, Bacillus sp. strain B3, Bacillus megaterium strain B4, Brevibacillus borstelensis strain B8, and Bacillus sp. strain B11 from Cannabis sativa L. efficiently disrupt cell-to-cell communication in Chromobacterium violaceum via quenching its QS signals (Kusari et al. 2014) . It is important to note that a diffusible signal factor (DSF) is essential in several Xanthomonas species and Xylella fastidiosa-associated phytopathogenesis (Newman et al. 2008) . Bacillus and Pseudomonas were reported to complement carAB, a gene responsible for fast DSF degradation in the Pseudomonas spp. strain G. This mechanism can be exploited as a powerful strategy in the biocontrol of DSF producing pathogens and, thus, can be deployed in agriculture (Liu et al. 2017) .

Iron is a vital metal for growth in all living organisms. There is a great competition for bioavailable iron in soil habitats as well as on plant surfaces. Under iron-limiting conditions, endophytes produce low-molecular-weight compounds called siderophores to competitively acquire ferric ion (Whipps 2001) . Although various bacterial siderophores differ in their abilities to sequester iron, in general, they deprive pathogenic fungi of this essential element since the fungal siderophores have lower affinity (Loper and Henkels 1999; O'Sullivan and O'Gara 1992) . Some plant growth-promoting endophytes go one step further and draw iron from heterologous siderophores produced by cohabiting microorganisms (Wang et al. 2003; Whipps 2001) . Primarily, siderophores help to acquire iron either from iron adsorbed to solid surfaces or from insoluble hydroxides. Siderophores can also extract iron from soluble and insoluble iron compounds, such as ferric-citrate, Fe-transferrin, ferric phosphate, ferritin, or iron bound to sugars, plant flavone pigments, and glycosides or even from artificial chelators like EDTA and nitritriacetate by Fe(III)/ligandexchange reactions. Hence, although siderophores don't play a direct role in iron solubilization, they can act as carrier for exchange between extracellular iron stores and membrane-located siderophore-transport systems (Winkelmann 2002) . Siderophores play a significant role in microbial metabolism because of the following facts:

1. Siderophores mainly consist of hydroxamate, catecholate, or ahydroxycarboxylate ligands that form hexadentate Fe(III) complexes, satisfying the six coordination sites on ferric ions which make them most significant ironbinding ligands. 2. Siderophore biosynthesis is a highly regulated process which is triggered by iron limitation resulting in building up of high local concentrations of siderophores in the vicinity of microbial cells. 3. Siderophores exhibit structural and conformational specificities to fit into membrane receptors and/or transporters besides their ability to solubilize iron and to function as external iron carriers (Stintzi et al. 2000; Huschka et al. 1986; Ecker et al. 1988 ).

Endophytic isolates of Phialocephala fortinii from P. sylvestris root, Carex curvula, Abies alba, Picea abies, and P. sylvestris showed that siderophore production is a function of pH values and iron(III) concentrations; 4.0-4.5 was the range of pH at which maximum siderophore production was found with the optimal ferric iron concentration of 20-40 μg iron (III) L −1 (0.36-0.72 μM, respectively). The most predominant siderophores produced by P. fortinii is ferricrocin (a hydroxamate siderophore) followed by ferrirubin and ferrichrome C (Bartholdy et al. 2001 ). An endophytic Streptomyces sp. GMKU 3100 isolated from the roots of a Thai jasmine rice plant (Oryza sativa L. cv. KDML105) exhibited remarkably high level of siderophore production. Inactivation of desD-like gene that codes a key enzyme responsible for the final step in siderophore biosynthesis resulted in impairment of siderophore production. Rice and mungbean plants inoculated with the wild-type strain-enhanced plant growth and significantly increased root and shoot biomass and lengths unlike siderophore-deficient mutant treatments (Figs. 11.3 and 11.4) . Endophytic actinomycetes, therefore, can be applied as a potentially safe and environmentally friendly biofertilizer in agriculture (Rungin et al. 2012) .

Various extracellular enzymes from microbes perform their function outside the cell which is significant to host-endophyte interdependence. Bacteria and fungi produce various extracellular enzymes that include hydrolases, lyases, oxidoreductases, and transferases (Traving et al. 2015; Kour et al. 2019b ). The substrates are mostly macromolecules such as carbohydrates, proteins, lignin, sugar-based polymers, and organic phosphate which are broken down into simpler forms that can be easily transported, absorbed, and assimilated. Enzymes secreted by endophytes help to initiate the association with the host and symbiosis process. Extracellular hydrolyases counteract plant pathogenic infection (Leo et al. 2016) . In fact, certain categories of enzymes namely, cellulases, xylanases, phytases, hemicellulases, asparaginase, proteases, gelatinase, pectinases, tyrosinase, chitinase, amylases, etc., are some of the key enzymes produced by endophytic bacteria and fungi.

Endophytic bacterial strains have been isolated from various plants such as pea (P. sativum), tomato (Lycopersicum esculentum), corn (Zea mays), wheat (Triticum aesitivum), oat (Avena sativa), canola (Brassica napus), barley (Hordeum vulgare), radish (Raphanus sativus) soybean (Glycine max), potato (Solanum tuberosum), lettuce (Lactuca serriola), and cucumber (Cucumis sativa) were identified and characterized that belong to the genus Arthrobacter, Actinobacter, Aeromonas, Agrobacterium, Alcaligenes, Bacillus, Azospirillium, Enterobacter, Flavobacterium Pseudomonas, Acinetobacter, Azotobacter, Beijerinckia, Burkholderia, Enterobacter, Erwinia, Flavobacterium, Rhizobium, and Serratia (Khan et al. 2017; Gray and Smith 2005) . Vijayalakshmi et al. (2016) isolated endophytic bacteria from medicinally important plants, producing α-amylase, protease, and cellulase. Similarly, Leo et al. (2016) reported endophytic bacteria, Alcaligenes faecalis, Burkholderia Rungin et al. (2012) cepacia, and Enterobacter hormaechei from perennial grasses that showed the hyper-enzymatic activity of α-amylase, protease, and cellulose (Table 11 .2).

A variety of microorganisms also exhibited hyperparasitic activity, attacking pathogens by excreting cell wall hydrolases. Chitinase produced by S. plymuthica C48 inhibited spore germination and germ-tube elongation in Botrytis cinerea (Frankowski et al. 2001) . The ability to produce extracellular chitinases is considered crucial for Serratia marcescens to antagonize Sclerotium rolfsii (Ordentlich et al. 1988 ). Using similar mechanisms, Paenibacillus sp. and Streptomyces sp. suppress Fusarium oxysporum while Pseudomonas sp. suppresses Fusarium solani, the commonly known plant pathogen (Lim et al. 1991) . Many endophytic fungi like Alternaria alternate, Hymenoscyphus ericae, and Aspergillus terreus also produce extracellular enzyme xylanase producers including those found in Table 11 .3. Similarly, the endophyte Periconia sp. produced β-glucosidase, while Acremonium species produced cellulases and hemicellulases.

Induced systemic resistance (ISR) is the immunity response mechanism inherent in crop plants that can be triggered by beneficial microbial endophytes during biotic and abiotic stress conditions which may include temperature, salinity, drought, 

Enzyme produced Detection method Amanita muscaria, A. muscaria, A. spissa, Boletus luridus, Cenococcum geophilum, Cortinarius glaucopus, C. purpurascens, Hydnum rufescens, Hymenoscyphus ericae, Laccaria cf., Lactarius acerrimus, L. auriolla, L.chrysorrheus, L. controversus, L. deliciosus, L. deterrimus, L. evosmus, L. pubescens, L. quieticolor, L. quietus, L. rufus, L. semisanguifluus, L. subdulcis, L. subumbonatus, L. zonarius heavy metal, and phytopathogenic infections. A diverse group of metabolites produced by the endophytes can impart the host plant to overcome the stress (Khan et al. 2017) . Immunized through ISR plays a vital role in the protection from pathogenic invasions, exhibition of varied resistance methods, efficient utilization of energy, and exploitation of genetic ability to induce resistance in the plants which are vulnerable for diseases (Latha et al. 2019) . Plants are also protected from the parasitic nematodes due to ISR. Bacterial endophytes like B. amyloliquefaciens, Bacillus pumilus, Bacillus subtilis, P. fluorescens, P. syringae, and S. marcescens can induce ISR (Latha et al. 2019 ). The following section gives an elaborate account of the endophyte-associated ISR in plants.

Detoxification of pathogen virulence factors is another mechanism of biological control. For example, certain biocontrol agents are able to detoxify albicidin toxin produced by Xanthomonas albilineans (Basnayake and Birch 1995; Zhang and Birch 1997) . Endophytic bacterial strains of B. cepacia and Ralstonia solanacearum were reported to suppress the activity of fusaric acid, a toxin secreted by Fusarium species, a major wilt-causing pathogen (Toyoda and Utsumi 1991) . The autoinducer-mediated quorum-sensing of endophytes can impair the virulence of pathogens to inflict diseases, which is of paramount importance (Latha et al. 2019) .

Endophytes also play a critical role in insect and pest-induced biotic stress in plants. Entomopathogenic microorganisms inhibit/antagonize other pathogenic microbes that not only help to protect plants but also reduce use of chemical pesticides. Since being established due to their capacity to protect their hosts against insects-pests, pathogens and even herbivores endophytic microorganisms have received considerable attention in the last 20 years. Webber (1981) first reported that endophytic fungus Phomopsis oblonga protected elm trees from the beetle Physocnemum brevilineum. P. oblonga controlled the beetle P. brevilineum which is the vector for Ceratocystis ulmi, responsible for the elm Dutch disease. Another endophytic fungi belonging to the Xylariacea family synthesized secondary metabolites in hosts of the genus Fagus that affected the beetle larvae. Owing to toxin production, Khan et al. (2017) endophytic fungus repels insects, induces weight loss, inhibits growth and development, and even increases pest mortality. Another mode of action might be rendering the plant unpalatable to several types of pests like aphids, grasshoppers, beetles, etc. due to metabolites secreted by the endophytes. Endophytic isolates of Neotyphodium sp. produced N-formilonine and a paxiline in the host Echinopogum ovatus that exhibited insecticidal activity against L. bonariensis and other insects .

White spruce Picea glauca, death rate in the Homoptera Adelges abietis increased when galls were infected with the endophytic fungus Cladosporium sphaerosperum while weight gain and survival of the insect-pest, Spodoptera frugiperda, were severely compromised when their hosts were colonized by endophytic fungi like Balansia cyperi. It is important to note that larvae from the bluegrass webworm Parapediasia teterrella preferred endophyte-free plants of L. perenne and F. arundinacea, to a point that the larvae would starve to death if only plants infected with Acremonium were available. Field studies revealed that endophyte-free species were severely attacked by insects, whereas those infected with Acremonium stayed almost free of insect larvae .

Endophytic microbes render the plant its ability to tolerate abiotic stress during severe temperatures and water scarcity. Tomato plants inoculated with psychrotolerant endophytic bacteria Pseudomonas vancouverensis OB155 and P. frederiksbergensis OS261 were able to overcome cold stress (10-12 °C). Lesser membrane damage with increased antioxidant activity was observed in endophyte-colonized plants compared to endophyte-free control plants. Further, cold acclimation genes (LeCBF1 and LeCBF3) were induced in bacteria-inoculated plants (Subramanian et al. 2015) . Similarly, the bacterial endophyte Burkholderia phytofirmans strain PsJN resulted in enhancement of Arabidopsis growth and strengthened its cell wall, and thereby increased cold stress resistance (Su et al. 2015) . Increased plant tolerance to drought was also seen due to endophytic bacteria. B. phytofirmans PsJN modulated transcriptional regulation, cellular homeostasis, and ROS detoxification in a drought stress-affected potato (Sheibani-Tezerji et al. 2015) . These facts strongly rationalize that endophytes can be potential protective agents in crops under extreme climatic environments as they can influence plant physiological responses to stresses (Liu et al. 2017) .

Endophytes can mitigate metal toxicity in plants through their own metal resistance system and encourage plant growth under metal stress. Endophytes improve plant growth in metal-polluted soils either directly or indirectly by metal detoxification, accumulation, or translocation in plants. They can even alter metal accumulation capacity in plants by excreting metal immobilizing extracellular polymeric substances as well as metal mobilizing organic acids and biosurfactants. The metal stress can be circumvented by various mechanisms, which include efflux of metal ions exterior to the cell, transformation of metal ions to less toxic forms, sequestration of metals on the cell surface or in intracellular polymers, and precipitation, adsorption/desorption, or biomethylation (Rajkumar et al. 2013 ). Inoculation of seeds or seedlings of hyperaccumulator plants with metal resistant endophytes results in accelerated phytoremediation in naturally and/or artificially metalcontaminated soil and improved plant growth.

The endophytic bacterial strain Bacillus sp. MN3-4 exhibited metal-resistance owing to active export via a P-type ATPase efflux pump that can transport metal ions across biological membranes against the concentration gradient using energy released by ATP hydrolysis (Shin et al. 2012) . Further, endophytic bacteria can modulate the activity of plant antioxidant enzymes (such as POS, CAT, SOD, glutathione peroxidase, and ascorbate peroxidase) as well as lipid peroxidation (malondialdehyde formation) that collectively enable the host plant to overcome heavy metal-induced oxidative stress. Methylation is another significant way to gain metal resistance or detoxification. Endophytic bacteria with mercury-resistant (Mer) operons express MerB gene-encoding organomercurial lyase, which cleaves organomercurials into mercuric ion (Hg 2+ ) (Brown et al. 2003) . MerA gene encodes mercuric reductase that converts highly toxic ionic Hg 2+ into less toxic volatile Hg 0 (Cursino et al. 2000) , thus alleviating metal toxicity and improving the efficiency of phytovolatilization. Lead-resistant endophytic bacteria Bacillus sp. MN3-4 isolated from the roots of the metal hyperaccumulator plant Alnus firma enhanced reduced metal phytotoxicity by extracellular sequestration and intracellular accumulation (Shin et al. 2012) .

Similarly, cadmium-resistant endophytic bacterium Serratia sp. LRE07 reduced metal stress by absorbing over 65% of Cd and 35% of Zn in bacterial cells from a single metal solution. Endophytes can also alter phytoavailability of heavy metals through the release of metal chelating agents (e.g., siderophores, biosurfactants, and organic acid), acidification of soils, redox activity, and phosphate solubilization. Extracellular polymeric substances (EPS) secreted by endophytes are composed of polysaccharides, proteins, nucleic acids, and lipids that are significantly responsible in metal complexation thereby reducing their bioaccessibility and bioavailability .

Nickel (Ni)-resistant endophytic bacterium Pseudomonas sp. A3R3 increased plant biomass (nonhost Brassica juncea) and Ni accumulation in plants (host A. serpyllifolium) grown in artificially Ni-contaminated soil (Ma et al. 2011) . These effects can be attributed to the ability of endophytes to produce plant growthpromoting substances (ACC deaminase, siderophores, IAA, and P solubilization) and plant polymer-hydrolyzing enzymes like cellulase and pectinase (Table 11 .4). Gouda et al. (2016) have summarized the discovery of a number of bioactive metabolites from endophytes that serve as an excellent source of drugs for the treatment against various diseases and with potential applications in agriculture, medicine, food, and the cosmetic industries (Table 11 .5). Ezra et al. (2004) reported that coronamycin, a complex of novel peptide antibiotics with activity against pythiaceous fungi and the human fungal pathogen Cryptococcus neoformans, was produced by a verticillate Streptomyces sp. isolated as an endophyte from an epiphytic vine Monstera sp. It was also active against the malarial parasite, Plasmodium falciparum. Undoubtedly, one of the most revolutionary findings of endophyte studies was the isolation of taxol-producing endophyte Taxomyces andreanae (Stierle et al. 1993 ). The diterpenoid taxol was approved by the FDA as one of the most potent anticancer drugs, but the supply of this drug was limited for the destructive collection of yew tree, the main source of taxol. Later taxol (paclitaxol) was also reported to be produced by the endophyte Metarhizium anisopliae found in the bark of a Taxus tree and is one of the most promising anticancer agents (Gouda et al. 2016 ). 

Swine meat and meat products, milk, and dairy products Sources: Adapted with permission from Gouda et al. (2016) As a selectively cytotoxic quinone dimmer, torreyanic acid is another important anticancer agent. Lee et al. (1996) reported the isolation of an endophyte strain P. microspore from T. taxifolia (Florida torreya) and the extraction of torreyanic acid from cultures of this endophyte. Camptothecin and its derivatives show strong antineoplastic activity. The fungus, which belongs to the family Phycomycetes, isolated from the inner bark of the plant Nothapodytes foetida, produced the anticancer drug lead compound camptothecin (Puri et al. 2005) .

Endophytes are a potential source of novel secondary metabolites with antiarthritic, antimicrobial, anticancer, antidiabetic, anti-insect, and immunosuppressant activities (Devi et al. 2020; Kour et al. 2019a; Yadav et al. 2019) . Bioactive compounds, such as camptothecin, diosgenin, hypericin, paclitaxel, podophyllotoxin, and vinblastine, are commercially produced by different endophytes colonizing respective plants which are agriculturally and pharmaceutically significant (Gouda et al. 2016; Godstime et al. 2014; Joseph and Priya 2011) .

Promising plant growth-promoting activity and an ability to induce stress tolerance to host plants have drawn wide attention for developing not only culture dependent but also independent characterization of endophytic diversity. However, reports on successful application of endophytes in plants under field conditions are extremely scarce. Future studies should aim to explore the interrelationship between plant immunity and function of the microbial population of endosphere. Similarly, breeding of endophyte-colonized crops, genetic engineering of endophytes, maintenance, and adaptation to benefit plants at various growth stages of plants should be investigated. Further, endophytes impart resistance to hosts against pests, insects, nematodes, and plant pathogenic fungi and bacteria.

Similarly, host plants obtain tolerance to abiotic stress induced by drought, salinity, and toxic metals. Diverse bioactive compounds have been synthesized by microbial endophytes that may include antimicrobials (vanillin, essential oils), antifungals, antivirals (alkaloids), antioxidants (eugenol), anti-inflammatories (cineole), etc. Therefore, commercial processes can be developed to exploit the rich source of endophytic biodiversity to produce natural products for use in pharmaceutics, food, and cosmetics. Activity-based rapid screening technologies should be developed that may help in the selective isolation of beneficial endophytes. Establishing a target endophytic library for plant breeding may help to protect endangered medicinal plants from overexploitation. Endophytes can be envisioned to be the future of biofertilizers and biocontrol agents that can be promising alternatives to environmentally hazardous chemical fertilizers and pesticides resulting in a paradigm shift in agricultural best practices.

Phosphate-solubilizing bacteria-assisted phytoremediation of metalliferous soils: a review

Impact of pesticides use in agriculture: their benefits and hazards

Endophytic microorganisms: a review on insect control and recent advances on tropical plants

Stable isotope labeling, in vivo, of d-and l-tryptophan pools in lemna gibba and the low incorporation of label into indole-3-acetic acid

Hydroxamate siderophore synthesis by Phialocephala fortinii, a typical dark septate fungal root endophyte

Proposal for the division of plant growth promoting rhizobacteria into two classifications: biocontrol-PGPB (plant growth-promoting bacteria) and PGPB

A gene from Alcaligenes denitrificans that confers albicidin resistance by reversible antibiotic binding

Endophytic and ectophytic potato-associated bacterial communities differ in structure and antagonistic function against plant pathogenic fungi

Biological nitrogen fixation associated with sugar cane and rice: contributions and prospects for improvement

Effects of zinc and influence of Acremonium lolii on growth parameters, chlorophyll a fluorescence and antioxidant enzyme activities of ryegrass (Lolium perenne L. cv Apollo)

Overview and mechanisms of iron regulation

Impact of the PGPB Enterobacter radicincitans DSM 16656 on growth, glucosinolate profile, and immune responses of Arabidopsis thaliana

The MerR family of transcriptional regulators

Sweet scents from good bacteria: case studies on bacterial volatile compounds for plant growth and immunity

Plant growth-promoting bacteria in the rhizo-and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization

Capacity of mercury volatilization by mer (from Escherichia coli) and glutathione S-transferase (from Schistosoma mansoni) genes cloned in Escherichia coli

Volatiles produced by soil-borne endophytic bacteria increase plant pathogen resistance and affect tritrophic interactions

Endophytic nitrogen fixation in dune grasses (Ammophila arenaria and Elymus mollis) from Oregon

Broad-range antagonistic rhizobacteria Pseudomonas fluorescens and Serratia plymuthica suppress Agrobacterium crown-gall tumors on tomato plants

Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: perspectives for human health

Plant-growth promoting effects of diazotrophs in the rhizosphere

Diazotrophic endophytes of native black cottonwood and willow

Competition

Substituted complexes of enterobactin and synthetic analogues as probes the ferric-enterobactin receptor in Escheichia coli

New endophytic isolates of Muscodor albus, a volatileantibiotic-producing fungus

Purification and properties of two chitinolytic enzymes of Serratia plymuthica HRO-C48

Exploring the boundaries of N2-fixation in cereals and grasses: an hypothetical and experimental framework

Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase

Bacteria with ACC deaminase can promote plant growth and help to feed the world

Mechanisms of antimicrobial actions of phytochemicals against enteric pathogens-a review

Endophytes: a treasure house of bioactive compounds of medicinal importance

Intracellular and extracellular PGPR: commonalities and distinctions in the plant-bacterium signaling processes

Bacterial endophytes in agricultural crops

The bacterial lipopeptide iturins induce Verticillium dahliae cell death by affecting fungal signalling pathways and mediate plant defence responses involved in pathogen associated molecular pattern-triggered immunity

Properties of bacterial endophytes and their proposed role in plant growth

Experimentelle untersuchungen zur frage der bacteriesymbiose in ho¨heren pflanzen und ihre beeinflussung durch 'Leitemente'

The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems

Isolation, characterization and plasmid pUPI126-mediated indole-3-acetic acid production in Acinetobacter strains from rhizosphere of wheat

Molecular recognition of siderophores in fungi: role of iron-surrounding N-acyl residues and the peptide backbone during membrane transport in Neurospora crassa

Extracellular phytase activity of Bacillus amyloliquefaciens FZB45 contributes to its plantgrowth-promoting effect

Nitrogen fixation in wheat provided by Klebsiella pneumoniae 342

Bioactive compounds from endophytes and their potential in pharmaceutical effect: a review

Endophytic microbes: a resource for producing extracellular enzymes

Bacterial endophytes and their effects on plants and uses in agriculture

The intracellular scots pine shoot symbiont Methylobacterium extorquens DSM13060 aggregates around the host nucleus and encodes eukaryote-like proteins

Extremophiles for hydrolytic enzymes productions: biodiversity and potential biotechnological applications

Agriculturally and industrially important fungi: current developments and potential biotechnological applications

Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: diversity and functional perspectives

Microbial biofertilizers: bioresources and eco-friendly technologies for agricultural and environmental sustainability

Isolation and characterization of soybean-associated bacteria and their potential for plant growth promotion

Quorum quenching is an antivirulence strategy employed by endophytic bacteria

Endophytic bacteria: prospects and applications for the plant disease management

Torreyanic acid: a selectively cytotoxic quinone dimer from the endophytic fungus Pestalotiopsis microspora

Effects of pH and glucose on auxin production by phosphate-solubilizing rhizobacteria in vitro

A novel triculture system (CC3) for simultaneous enzyme production and hydrolysis of common grasses through submerged fermentation

Pseudomonas stutzeri YPL-1 genetic transformation and antifungal mechanism against Fusarium solani, an agent of plant root rot

Inner plant values: diversity, colonization and benefits from endophytic bacteria

Utilization of heterologous siderophores enhances levels of iron available to Pseudomonas putida in the rhizosphere

Inoculation of endophytic bacteria on host and nonhost plants e effects on plant growth and Ni uptake

Beneficial role of bacterial endophytes in heavy metal phytoremediation

Expression of sugarcane genes induced by inoculation with Gluconacetobacter diazotrophicus and Herbaspirillum rubrisubalbicans

Quorum sensing in bacteria

Microbial consortium with multifunctional plant growth promoting attributes: future perspective in agriculture

Virulence of plant pathogenic bacteria attenuated by degradation of fatty acid cell-to-cell signaling factors

Traits of fluorescent Pseudomonas spp. involved in suppression of plant root pathogens

Infection of mottled stripe disease-susceptible and resistant sugar cane varieties by the endophytic diazotroph Herbaspirillum

The role of chitinase of Serratia marcescens in biocontrol of Sclerotium rolfsii

On the limits of biological inquiry on soil science

The Janus factor of ethylene: growth inhibition and stimulation

An endophytic fungus from Nothapodytes foetida that produces camptothecin

Seedling growth promotion and nitrogen fixation by a bacterial endophyte Paenibacillus polymyxa P2b-2R and its GFP derivative in corn in a long-term trial

Endophytic bacteria and their potential to enhance heavy metal phytoextraction

Climate change driven plant-metalmicrobe interactions

Endophytic fungi: biodiversity, ecological significance and potential industrial applications

Biodiversity of endophytic fungi from diverse niches and their biotechnological applications

Endophytic microbiomes: biodiversity, ecological significance and biotechnological applications

Endophytic fungi from medicinal plants: biodiversity and biotechnological applications

Endophytic microbes from diverse wheat genotypes and their potential biotechnological applications in plant growth promotion and nutrient uptake

Endophytic microbes in nanotechnology: current development, and potential biotechnology applications

The rhizosphere. Oxford and IBH

New and future developments in microbial biotechnology and bioengineering: Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: diversity and functional perspectives

Azoarcus gen. Nov., nitrogen-fixing proteobacteria associated with roots of Kallar grass (Leptochloa fusca (L.) Kunth), and description of two species, Azoarcus indigens sp. nov. and Azoarcus communis sp. nov

Endophytic nifH gene diversity in African sweet potato

Enhanced maize productivity by inoculation with diazotrophic bacteria

Plant growth enhancing effects by a siderophore-producing endophytic streptomycete isolated from a Thai jasmine rice plant (Oryza sativa L. cv. KDML105)

Perspective of plant growth promoting rhizobacteria (PGPR) containing ACC deaminase in stress agriculture

Plant growthpromoting bacterial endophytes

Endophytic bacterial communities of field grown potato plants and their plant-growth-promoting and antagonistic abilities

Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenomic analysis

Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: diversity and functional perspectives

Transcriptome profiling of the endophyte Burkholderia phytofirmans PsJN indicates sensing of the plant environment and drought stress

Genetic analysis of plant endophytic Pseudomonas putida BP25 and chemo-profiling of its antimicrobial volatile organic compounds

Characterization of lead resistant endophytic Bacillus sp. MN3-4 and its potential for promoting lead accumulation in metal hyperaccumulator Alnus firma

Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: diversity and functional perspectives

Contribution of microbial phytases to the improvement of plant growth and nutrition: a review

Taxol and taxane production by Taxomyces andreanae, an endophytic fungus of Pacific yew

Microbial iron transport via a siderophore shuttle: a membrane ion transport paradigm

An overview of endophytic microbes: Endophytism defined

The genome of the endophytic bacterium H. frisingense GSF30(T) identifies diverse strategies in the Herbaspirillum genus to interact with plants

Bacterial endophytes: potential role in developing sustainable systems of crop production

Burkholderia phytofirmans PsJN reduces impact of freezing temperatures on photosynthesis in Arabidopsis thaliana

Psychrotolerant endophytic Pseudomonas sp. strains OB155 and OS261 induced chilling resistance in tomato plants (Solanum lycopersicum mill.) by activation of their antioxidant capacity

Endophytic microbes in crops: diversity and beneficial impact for sustainable agriculture

Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: diversity and functional perspectives

Coevolution of symbiotic mutualists and parasites in a community context

Phytohormones producing fungal communities: metabolic engineering for abiotic stress tolerance in crops

Method for the prevention of Fusarium diseases and microorganisms used for the same

A model of extracellular enzymes in free-living microbes: which strategy pays off?

Active root-inhabiting microbes identified by rapid incorporation of plantderived carbon into RNA

Enzyme production and antimicrobial activity of endophytic bacteria isolated from medicinal plants

Microbial life in the phyllosphere

Abiotic resistance and chaperones: possible physiological role of SP1, a stable and stabilizing protein from Populus

A natural control of Dutch elm disease

Role of gluconic acid production in the regulation of biocontrol traits of Pseudomonas fluorescens CHA0

Microbial interactions and biocontrol in the rhizosphere

Microbial siderophore-mediated transport

Metabolic engineering to synthetic biology of secondary metabolites production

Plant microbiomes for sustainable agriculture

The novel lipopeptide poaeamide of the endophyte Pseudomonas poae RE*1-1-14 is involved in pathogen suppression and root colonization

The gene for albicidin detoxification from Pantoea dispersa encodes an esterase and attenuates pathogenicity of Xanthomonas albilineans to sugarcane