Plant growth promotion by streptomycetes: ecophysiology, mechanisms and applications
© The Author(s) 2016
Received: 13 January 2016
Accepted: 29 May 2016
Published: 3 August 2016
The genus Streptomyces comprises filamentous Gram-positive bacteria that are widely recognized for their ability to produce bioactive compounds such as antimicrobial, antiparasitic and immune-suppressing compounds via secondary metabolism. These bioactive compounds represent a third of all commercially available antibiotics. Streptomycetes have been found in beneficial associations with plants where they have improved plant growth and protected against pests, which have attracted the attention of researchers worldwide. This review focuses on the potential of streptomycetes as plant growth-promoting bacteria (PGPS) and considers features related to secondary metabolic pathways, interactions with host plants and recent advances in elucidating plant growth-promoting mechanisms. Such advances in basic knowledge have increased the prospects for streptomycetes to be used as bioinoculants for sustainable agriculture.
It has been estimated that the world’s population will reach about nine billion by 2050 , which will require high levels of yield from agricultural systems. Centered on the Green Revolution model established in the last century, a range of research and technology transfer initiatives have been employed to meet the demand for food, fiber, and energy. However, it has become increasingly clear that the conventional systems of food production have many negative impacts on the environment .
To develop food production under environmentally and socially sustainable systems represents one of the twenty-first century’s greatest challenges for agricultural researchers. One of the most promising initiatives for a new model of agriculture is based on converting the natural processes that occur in the soil–plant system into biological input technologies. In this context, microorganisms, their products and their processes are essential resources for a new generation of biotechnologies applicable to plant production and protection, and potentially a paradigm shift in agricultural practice.
Using plant growth-promoting bacteria (PGPB) for the benefit of agriculture has received increasing attention and acceptance [3–5]. Besides the well-studied Gram-negative plant-associated bacteria, Gram-positive bacteria can also have beneficial interactions with plants and promote plant growth [6–8]. Streptomyces is the most widely studied genus of Gram-positive PGPB and is the central subject of this review. This genus comprises a wide diversity of species that have a high G-C (guanine and cytosine) ratio in its DNA, up to 75 % of its genome . This genus produces a wide variety of biologically active compounds; some with plant growth activity. It has been suggested by some authors that the increasingly intensive surveys of soil-borne microbes have resulted in a decreased frequency of newly discovered compounds . However, the metabolic versatility and cosmopolitan behavior of Streptomyces species have enabled them to be isolated from different environments, some of which have not yet been explored, hence, presenting an opportunity to discover new bioactive compounds.
Morphogenetic and physiological aspects of the Streptomyces genus have been reviewed [11, 12]. Other reviews have focused on the biotechnological potential of plant-associated endophytic actinobacteria  and free-living plant growth-promoting actinobacteria . This review presents an overview of the plant growth-promoting ability of various species from the genus Streptomyces; it considers historical aspects of their discovery, their physiological features, their plant growth mechanisms and their application as bioinoculants in agriculture.
Historical and taxonomic aspects
Nearly 200 years after Antony van Leeuwenhoek reported the first observation of bacteria in 1684 using his own handcrafted microscope, other pioneers, such as Ferdinand Cohn and Robert Koch, founded modern concepts about bacteriology as a science domain . It took another 200 years to identify and reach the current understanding of actinobacteria. Further, only 204 years after van Leeuwenhoek studies, the first description of a microorganism that eventually became known as an actinobacterium was described, when Armauer Hansen discovered a microorganism in the tissues of leprosy patients, which was later described as the etiologic agent of this disease in 1874 .
In 1875, Cohn described the first Actinobacteria species, which he named Strepthrotrix foersteri. He isolated this microbe from samples of human tear ducts provided by R. Foerster, a medical friend. Cohn supposed that Strepthrotrix foersteri was not associated with any disease, but that it reached the patient’s eye through airborne soil particles. Later, he observed that Strepthrotrix foersteri had morphological features of fungi and bacteria . However, the proposed nomenclature for the bacterial genus was deemed invalid because Strepthrotrix had already been classified as a true fungus by Corda in 1839 . Then in 1877, Carl Otto Harz described the etiologic agent of “lampy jaw”. Harz observed structures similar to reproductive bodies and hyphae of fungi; therefore, he considered the microorganism to be a fungus and named it Actinomyces bovis . In 1882, Robert Koch discovered another microorganism during his observations using light microscopy that is now recognized as an actinobacterium: the tuberculosis pathogen Mycobacterium tuberculosis . Koch observed that the microbes presented morphological characteristics that were similar to those of microorganisms previously described by Hansen associated with leprosy disease .
Although there was a clear relationship between these microorganisms, it was not until 1916 that R.E. Buchanan suggested a nomenclature and classification for this group. Buchanan proposed the order Actinomycetales, containing the family Actinomycetaceae and the following genera: Actinobacillus, Leptotrichia, Actinomyces, and Nocardia . In 1943, Waksman and Henrici proposed a new classification for the actinomycetes, which was based on their ability to form branching cells. Waksman and Henrici observed that one actinomycete group formed a condensed mat of interlinked branching hyphae that produced reproductive spores. The Streptothrix described by Cohn fell into this group, but due to the invalid genus name, Waksman and Henrici named it Streptomyces, which means “twisted fungus” .
In the fourth decade of the twentieth century, Streptomyces was recognized. Many studies were performed during this time to find chemotherapeutic treatments to control tuberculosis . In 1943, Waksman again received attention, this time due to his greatest discovery: the antibiotic streptomycin isolated from Streptomyces griseus is effective against the tuberculosis pathogen . About 600 validated species of Streptomyces have now been described following their isolation from many environmental sources. They are now the subject of research to discover new bioactive compounds for the pharmaceutical and agricultural industries .
The first proposed nomenclature of actinobacteria was based on sporulation patterns. Although morphological characteristics are typically important for Streptomyces identification, some studies have demonstrated that classification based on cell morphology, colony pigmentation, and physiological features do not always reflect the natural phylogenetic relationship between actinobacteria and related organisms . Introduction of the polyphasic taxonomic approach combined molecular and biochemical analyses which elucidated streptomycetes systematics. In addition, increased availability of 16S rRNA sequence data has enabled accurate studies of taxonomic affiliations and phylogenetic relationships [15, 21, 22].
The Streptomyces genus belongs to the Streptomycetaceae family and the single-order Streptomycetales . This order belongs to both phylum and class Actinobacteria . The actinobacteria from the Streptomyces genus are the most extensively studied mycelial actinobacteria. They are aerobic, Gram-positive bacteria that grow as branching filaments that consist of vegetative mycelia and aerial hyphae [15, 24]. Some morphological and physiological properties, along with the ability to produce a wide range of pigments, have been used not only to classify the Streptomyces genus [25, 26], but also to study its ecological distribution and biotechnological potential [27, 28].
Morphological differentiation and physiology
Streptomycetes have a markedly different cell envelope structure than Gram-negative bacteria, such that Streptomyces genus has been identified using cell wall composition [29, 30]. Similar to other actinobacteria, streptomycetes have no outer membrane and their cell walls have a thick peptidoglycan (or murein) layer . The presence of LL-diaminopimelic (LL-DAP) in the cell wall confers a typical chemotaxonomic characteristic to all members of the Streptomyces genus [32, 33], and its presence together with glycine characterizes the cell wall as Type I [31, 34]. Teichoic acids (anionic glycopolymers) comprise another important cell wall component that confers a negative charge to the cell surface and contributes to physiological functioning and cell co-aggregation [35, 36].
The growth of Streptomyces involves hyphal tip extension and sub-apical branching . Unlike the process in rod-shaped bacteria where cytokinesis is based on building a cross wall by depositing murein into lateral walls, Streptomyces growth occurs by hyphae production at the cell pole . Although it is not clearly elucidated, this cell growth pattern is regulated by the apical protein complex DivIVA. In Bacillus subtilis, DivIVA interacts with the Min system to coordinate division at the middle of the cell. In contrast, in Streptomyces, the Min system is absent, thus DivIVA affects division at the cell tip. Another aspect of streptomycetes growth involves the conservation of two groups of proteins, the tubulin homolog FtsZ and several membrane proteins, which are both associated with cytokinetic Z-ring and septal peptidoglycan .
The last phase of the Streptomyces life cycle consists of the apical cells of the aerial hyphae differentiating into a spore chain . A differentiating apical compartment grows by tip extension and starts synchronous, multiple cell divisions into a developmentally controlled form . Again, there is the participation of FtsZ, which leads to sporulation septa and then these pre-spores assemble thick spore walls by depositing actin . The size of Streptomyces spores can range from 0.7 to 1.2 µm [42, 43]. These last two phases of the Streptomyces life cycle are closely related to antibiotic production . During programmed cell death of the substrate mycelia, antibiotics are simultaneously produced, perhaps to protect the nutrient sources against competitor microorganisms [44, 45].
Among the 23,000 bioactive secondary metabolites produced by microorganisms, two-thirds are produced by actinobacteria, and Streptomyces spp. accounts for more than 70 % of these . This production of secondary metabolites is attributed to the development of aerial hyphae as a result of nutrient limitation . The biological activity of these compounds involves inhibitory or microbiocide activity against microorganisms (i.e., antibiotics), toxicity against metazoans, microbial hormone-like activity, and metal transport [48–50]. It has been well demonstrated that the secondary metabolites produced by streptomycetes increases adaptation to biological, physical, and chemical stresses; thus, they are recognized as ‘stress metabolites’ .
Structural genome studies tell us that most genes involved in regulating secondary metabolite pathways are arranged in clusters. These clusters might encode the highly phosphorylated guanosine nucleotide (p)ppGpp and some regulatory proteins involved in producing secondary metabolites . In Streptomyces species under nutritional stress, alarmone ppGpp plays a role as a regulator of antibiotic production [52, 53]. Members of both the SARP and LAL families of regulatory proteins appear to be confined to actinobacteria, mainly genus Streptomyces, and have shown species-specific controls for secondary metabolism pathways [54–56]. Cell-to-cell communication is a determining factor for modulating antibiotic production, and γ-butyrolactones (GBLs) are the main intercellular signaling compounds .
The overall ecophysiological traits of the Streptomyces genus support the concept of cosmopolitan biogeographical behavior. The traits include the ability to form spores under unfavorable abiotic conditions, a competitive ability related to antibiotic production, a broad pH range that is favorable for growth, and a wide pH range that is optimal for growth between different Streptomyces species (such as pH 4.3 for the acidophilic S. yeochonensis , pH 7.0 for the neutrophilic S. roseus , and pH 10 for the alkaliphilic S. alkalithermotolerans ). Streptomycetes are typically chemoorganotrophic with a great versatility for metabolizing a wide range of carbon sources including mono- and disaccharides, polyol, organic acids (glucose, dextrose, fructose, lactose, maltose, mannitol, rhamnose, sucrose, glycerol, and glycolic acid), polysaccharides (including cellulose and starch), and more complex and recalcitrant C-sources (such as humic and fulvic acids) [60–62].
Biotechnological potential and cosmopolitan features of the Streptomyces species
The best genetically known representative of the genus
Mediterranean sponge Axinella polypoides (Porifera)
Producer of streptomycin antibiotic
Decomposed cow dung
Alleviates the stresses caused by Sc. sclerotiorum and salt in chickpea
Pathogen of potato scab
Rhizosphere of Ebenus sibthorpii
Antagonist activity against Rhizoctonia solani
Surface-sterilized stems of rice
Plant tissue of Citrus reticulata
Antagonist activity against Xylella fastidiosa
Inner tissue of Portulaca oleracea L. stems
Phenazine-1-carboxylic acid producer
Surface-sterilized roots of Curcuma phaeocaulis
Vermicompost of sunflower cake
Plant growth-promoting streptomycete. AIA and catalase producer
Vermicompost of sunflower cake
Ecology of Streptomyces–plant host interaction
To acquire a better understanding and to manipulate the interactions between plant growth-promoting streptomyces (PGPS) and their hosts, it is necessary to elucidate those biochemical mechanisms that lead to compatible relationships. As shown above (Table 1), most of these streptomycetes are soil-dwelling bacteria with a free-living life cycle in the soil (i.e., saprophytic competence) and they are able to efficiently colonize the rhizosphere and rhizoplane compartments. Eventually, some PGPS might become endophytic and colonize the inner tissues of the host plant and partly or fully conduct their life cycle within them . Therefore, before discussing plant responses to PGPS, it is necessary to describe the rhizosphere and rhizoplane colonization process.
The rhizosphere is the soil volume under the influence of plant root exudates, secretions, and loose cell deposition . The rhizoplane plays a crucial modulatory role on the microbial community structure and microbial diversity that will ultimately influence plant growth and performance in the soil–plant system . Additionally, microbial activity in the rhizosphere soil is markedly influenced by carbon-containing metabolites released from roots via the rhizodeposition process . Rhizodeposition consists of numerous compounds such as ionic secretions, free oxygen and water, enzymes, proteins, mucilage, amino acids, organic acids, sugars, and phenolics . These compounds act as nutritional resources, chemoattractants, chemorepulsants, and signaling compounds that shape the microbial community structure and activity of different groups of microorganisms and have a significant influence on plant root–microorganism interactions .
The PGPS are widely recognized to be good rhizosphere colonizers and their rhizosphere competence may be partially explained by several chemotaxic features, such as bacterial rate multiplication, quorum sensing-controlled gene expression, amino acids, antibiotics, and siderophore synthesis . Initially, soil-borne or introduced streptomycete cells that respond to released compounds are actively attracted to the rhizosphere by chemotaxis [69, 72]. At this point, the versatile nutritional requirements and increased population rates coupled with bioactive compound production and detoxification mechanisms are determinants for successful rhizosphere establishment. The former properties play a pivotal role in overcoming complex competition and can be partially explained by the ability to produce antibiotics and other bioactive compounds that confer an ecological advantage and allow PGPS to colonize niches. Several biomolecules that are secondary metabolites of Streptomyces contribute to biocontrol and successful colonization; e.g., siderophores from S. coelicolor , the antifungal nigericin and antibiotic geldanamycin from S. violaceusniger YCED-9 , and chitinase from S. violaceusniger YH27A .
Some secreted proteins are important for successful root colonization by Streptomyces . Differential protein expression was exhibited by S. coelicolor when it was cultivated in minimal medium with and without Lemna minor fronds. Bacterial enzymes involved in degrading cellulose, alkenes, and amino acids were induced in the presence of plant extracts, suggesting that the carbon and energy were acquired through degrading compounds present in L. minor exudates .
Isolates of PGPS can be screened for the attribute that only a minority of species are recognized as phytopathogenic agents; namely Streptomyces scabies, S. acidiscabies, S. turgidiscabies, and S. ipomoeae, which are all etiologic agents of common scab diseases . Streptomyces scabies is a model organism for investigating plant host–pathogen interactions in Gram-positive bacteria in which a protein secretion system is essential for its pathogenesis . The effector proteins can be secreted by the secretory (Sec) and twin-arginine translocation (Tat) pathway or, additionally, by the specialized Type VII secretion system (T7SS) . Thaxtomin, a family of nitrated dipeptide phytotoxins, is an important pathogenicity factor secreted by S. scabies and plays a role in cellulose biosynthesis inhibition . Nec1 is a protein that is required for root colonization by S. scabies . Another important intercellular signal attributed to pathogenic streptomycetes and its host is nitric oxide (NO) . Synthase-derived NO is produced by plant-pathogenic Streptomyces in response to cellobiose production, which expands plant tissues and appears to be involved in the nitration of thaxtomin .
In contrast, a wide variety of Streptomyces species establish beneficial plant–microbe interactions [84–86]. The ability of some Streptomyces species to gain access into root tissues and to establish an endophytic lifestyle without causing visible harm or symptoms in the host plant has been reported (Table 1). These species can be found mainly in the apoplastic compartments that comprise the intercellular spaces and lumen of differentiated dead cells (sclerenchyma and xylem cells) of the host plant organs (roots, stems, leaves, flowers, fruits, and seeds); intracellular occurrences seem to be less frequent . Using a Streptomyces sp. strain EN27 tagged with green fluorescent protein, the endophytic colonization of embryos, endosperm, and emerging radicles of wheat seeds has been reported .
Unlike Gram-negative bacteria, Streptomyces and other filamentous actinobacteria possess active penetration structures that grow on the plant surface and infect intact cells . The ability to attach and develop an infection point through the cell wall of sweet potato (Ipomoea batatas [L.] Lam.) has been reported for S. ipomoea. Subsequently, the tip-growth hyphae colonize the interior of parenchyma cells and establish an endophytic interaction . Similarly, using short branches that emerged from the main hyphae, S. scabies was observed to penetrate the cell walls of potato plants . Based on the described cell wall penetration process by these short hyphae within a short and uniform distance from the branching point, the authors suggested a specialized penetration function for this structure. Furthermore, Streptomyces might enter plant tissues by natural openings such as stomatal apertures, lenticels, hydathodes, wounds, broken trichomes, and root hair cracks formed by lateral root emergence zones . A transmission electron microscope analysis demonstrated that S. galbus MBR-5 entered the leaves of Rhododendron sp. seedlings through stomatal openings .
Plants exhibit defense responses during infection by PGPS, but they are less aggressive than those expressed during pathogenic interactions . Although the biochemical mechanisms involved in these plant responses are not clearly elucidated, the pivotal role of phytohormones such as salicylic acid (SA), jasmonic acid (JA), and ethylene (ET) has been widely reported in the literature [93–96]. Arabidopsis thaliana inoculated with the endophytic Streptomyces sp. strain EN27 induced low levels of gene expression related to the JA and ET pathways . Furthermore, plant response to PGPS infection involves generating reactive oxygen species, which are cytotoxic . This plant process can be subverted by enzymatic machinery related to antioxidant activity; e.g., catalase and superoxide dismutase by S. coelicolor, and aconitase by S. viridochromogenes strain Tü494. This process plays an important role in alleviating the cytotoxic effects induced by reactive oxygen species and in allowing successful plant tissue colonization [97–99].
Endophytic colonization usually represents an important ecological advantage to the microorganism, because the protected environment is less susceptible to abiotic stress (pH, redox, osmotic, and hydraulic variations) and microbial competition compared with the rhizosphere–soil system. Moreover, the intimate contact between plant host cells and microbial cells might be more effective for the bidirectional exchange of signals, functional metabolites, and nutritional sources for a successful beneficial interaction, which may promote growth of the host plant [88, 100]. The mechanisms involved in plant growth-promoting activity by both endophytic and rhizosphere streptomycetes will be discussed below.
Plant growth promotion by streptomycetes
Most of the fundamental and applied studies of beneficial plant–microbe interactions relate to Gram-negative bacteria [101–103]. Although less often studied, many representative groups of Gram-positive bacteria, particularly those belonging to genus Streptomyces, exhibit a range of traits that may improve plant growth by using different mechanisms . As quoted for other beneficial interactions, the plant growth-promoting effects related to Streptomyces–plant interactions can be divided into biofertilization, biostimulation, and bioprotection .
Due to the mineralogical and electrochemical properties of many soils, some essential mineral nutrients are unavailable to plants because they are present in insoluble forms . Biofertilization consists of a direct mechanism that improves the macro or micronutrient acquisition (uptake and assimilation) by plants. Nutrients sequestered in the crystalline lattice of the mineral fraction of soil can be solubilized and released into solution by organic acids (such as gluconic acid, citric acid, succinic acid, and oxalic acid) that are secreted by different microorganisms . Jog and colleagues  reported the release of free phosphate by acidification resulting from the release of malic acid and gluconic acids by Streptomyces mhcr0816 and Streptomyces mhce0811, respectively. These authors also observed an increase in the number of branches and lateral roots, shoot length, and mineral content of Fe, Mn, and P in wheat plants inoculated with these streptomycetes. Soil treated with a phosphate-solubilizing strain of Streptomyces that was isolated from a wheat field increased N, Fe, P, and Mn content in shoots of wheat . In addition, solubilization of rock phosphate by S. youssoufiensis has been reported [108, 109]. Streptomycetes can further promote mineral supply by synthesizing siderophores and siderophore uptake systems . Streptomyces sp. GMKU 3100, a siderophore-producing endophytic streptomycete, was capable of promoting the growth of rice and mungbean, whereas its siderophore-deficient mutant did not differ from the uninoculated control . Until now, there is no convincing evidence for free-living or endophytic Streptomyces species able to fix nitrogen, since the controversial report related to S. thermoautotrophicus by Ribbe and colleges  was recently refuted .
Plant growth can be directly improved by the microbial production of metabolic compounds with phytohormonal activity at micromolar to nanomolar concentrations . Auxin and auxin-like compounds regulate many aspects of plant growth and development including cell plasticity, tissue elongation, embryogenesis, tip dominance, and emergence of lateral roots . The production of indole-3-acetic acid (IAA) by Streptomyces spp. has been quoted in several reports [107, 113, 114]. For example, S. atrovirens ASU14 utilized tryptophan and produced 22 µg/mL of the IAA . An auxin-like activity due to pteridic acid A was produced by S. hygroscopicus TP-A0451 isolated from Pteridium aquilinum (bracken) stems . This compound stimulated root elongation and induced the formation of adventitious roots in Phaseolus vulgaris (kidney bean) hypocotyls. Another class of phytohormones that have an important function in plant growth is gibberellin. This phytohormone is involved in physiological process that includes seed germination, growth of stems and leaves, floral induction, and growth of flowers and fruits [117, 118]. Streptomyces species isolated from a marine environment exhibited the ability to produce a range of phytohormones, including gibberellic acid, and enhanced the agronomic performance of eggplant (Solanum melongena) by influencing its growth parameters, including root length and fresh or dry root weight .
Plant-associated microbes might have the ability to minimize the challenges imposed by phytopathogens. This biocontrol activity can manifest as antibiosis, nutrient and space competition, parasitism, predation, hypovirulence, and induced systemic resistance [69, 120], which are indirect mechanisms of plant growth promotion. The versatile production of secondary metabolites involved in biocontrol is primarily a competitive strategy to successfully colonize the root zone . The genus Streptomyces is widely recognized as being able to synthesize several bioactive metabolites that act to control phytopathogen and to confer an advantage to rhizosphere or endophytic colonization . It has been reported that antifungal metabolites produced by 213 Streptomyces strains isolated from different habitats exhibited in vitro antagonistic activity against Rhizoctonia solani . An investigation into the nematicidal property of Streptomyces roseoverticillatus CMU-MH021 revealed the production of secondary metabolites that acted against the root-knot nematode Meloidogyne incognita . Streptomyces roseoverticillatus CMU-MH021 produced fervenulin, which decreased the percentage of hatched eggs and increased the percentage mortality of second-stage juveniles; it produced isocoumarin, which also increased the percentage mortality of second-stage juveniles. A recently released draft genome sequence of the mushroom mycoparasite antagonist Streptomyces sp. strain 150FB, with close correspondence to the S. avermitilis MA-4680 genome, revealed possible factors related to disease suppression, namely, a set of genes encoding extracellular enzymes involved in degrading fungal cell wall polysaccharides, disrupting membranes and proteins, and also peroxidases and ribonucleases . In addition, two terpenes and two siderophore biosynthetic gene clusters were detected. Streptomycetes can also stimulate plant defense by the priming phenomenon, resulting in induced systemic resistance . Streptomyces sp. strain AcH505 suppressed oak powdery mildew infection . This streptomycete strain elicited a systemic defense response in oak (Quercus robur), inducing the jasmonic acid/ethylene-dependent pathway and the salicylic acid-dependent pathway.
Secondary metabolites produced by Streptomyces species, main bioactivity property, and their genes and structural organization
abeABCD; α-abeA genes
S. hygroscopicus var. ascomyceticus
Immunosuppressant; neurotrophic; antifungal
FK520 gene cluster
Antitumor; antifungal; insecticidal
aur operon (aurA through aurI)
sven0916-sven0928 gene cluster
merA-D; mere; merP genes
S. viridochromogenes Tu¨494
phsB; orfM; phsC; pmi; ppm; ppd; phsA; pat; dea; prpA
Plant-associated streptomycetes can also benefit the host plant by mitigating abiotic stress such as heat, cold, drought, and nutrient depletion, thus reducing their negative impacts and consequently increasing plant growth . The application of Streptomyces filipinensis no. 15, a 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase and IAA producer, reduced the endogenous levels of ACC, the immediate precursor of ethylene, in both roots and shoots and subsequently enhanced plant fitness to the environment . Plant growth-promoting and stress-alleviating activities have been demonstrated for a halo-tolerant and ACC deaminase-producing Streptomycete sp. strain PGPA39 applied to tomato (Solanum lycopersicum) plants under salinity stress .
Furthermore, a different approach that is based on the indirect mechanisms of plant growth by PGPS has received particular attention. In a study involving a tripartite culture system , streptomycete application seemed to act as a modulator in both mycorrhizal and nitrogen-fixing symbiosis and raised their ability to induce plant growth [131, 132]. An increased number, size, and vigor of root nodules were observed on young pea (Pisum sativum) seedlings cultivated in soil with naturally abundant Rhizobium and that was inoculated with S. lydicus WYEC108 . Streptomyces sp. AcH505 isolated from the hyphosphere of a spruce (Picea abies) promoted mycelial growth and the mycorrhization rate by Amanita muscaria and Suillus bovinus, while it suppressed the mycelial extension of the plant pathogens Armillaria obscura and Heterobasidion annosum [134, 135].
Our group has recently proposed some different methods to enhance the plant growth-promoting ability of the endophytic diazotrophic bacteria Herbaspirillum seropedicae strain HRC54 (unpublished results). One method involved axenic studies combining H. seropedicae with the Streptomyces bellus strain UENF AC06 that was isolated from mature vermicompost. This mixed cultivation increased the population growth and nitrogen fixation rates of Herbaspirillum when measured by acetylene reduction activity. Therefore, S. bellus strain AC06 may be used to improve the plant growth-promotion response by H. seropedicae strain HRC54, and we suggest that this mixed cultivation is a potential bioinoculant for agricultural systems.
Biotechnological application of PGPS in agriculture
Commercially developed plant growth-promotion products from streptomycetes
Streptomycete active ingredients or their metabolites
Plant growth-promotion effects
Streptomyces lydicus WYEC 108
Actinovate® SP/Actinovate® AG (seed application)
Grass, ornamentals, vegetables, and forest species in greenhouses, nurseries, and more
Biocontrol by soil-borne plant pathogens and foliar diseases
Micro108® soluble/Micro108® Seed Inoculant
Food and fiber crops, ornamentals, turf grass, landscape plants, including tree seedlings for transplanting into the forest
Enhances plant vitality and encourages more vigorous root systems
For indoor/outdoor greenhouse, nursery, turf grass, ornamental plant, and field uses
Biocontrol of soil-borne plant pathogen
Seedling production, vegetables, herbs, and ornamentals
Biocontrol by soil and seed-borne pathogens
Shadehouse, greenhouse, field-grown ornamentals, foliage plants, Christmas trees, and other woody ornamentals
Biocontrol of leaf miners, mites, and suppression of aphids, whiteflies, and thrips
VERMITEC® (additional brands AGRI-MEK®)
Cotton, citrus, pome fruit, nuts and vegetables
Biocontrol of mites and insects
PROCLAIM® (additional brands AFFIRM®, DENIM ™)
Vegetables (Brassica, leafy and fruiting vegetables) and cotton
Lepidoptera. Side effects on mites, leaf miners, and thrips
Cotton, corn, and soybean
Biocontrol of nematodes
The first challenge to produce a bioinoculant using PGPS is to find the best strain of streptomycete (single formulation) or its combination with other microbes (mixed formulation). Screening studies involve different experimental assays in the laboratory and greenhouse. Elite strains must be tested under different environmental conditions and for different plant species and different genotypes of a target crop . Following these steps, it is necessary to develop specific bioinoculant formulations, which involve determining the required physical and chemical characteristics of the carrier, and ascertaining which additives and metabolites would increase the viability, activity, and performance of the microorganism when introduced under field conditions . Lastly, research to develop methods of bioinoculant delivery and timing must be carried out in the greenhouse and field to maximize the plant response to the applied bioinoculant. It has been found that applying streptomycetes is different to applying Gram-negative bacteria because better plant responses have generally been obtained when the streptomycete application to the soil or substrate occurred before sowing the seeds, thus allowing the selected strain to colonize and establish [6, 137, 138].
The viability and activity of the population inoculum is often affected by abiotic stress. Since the endophytic compartment represent a more protective niche for plant–bacteria interaction, formulations based on endophytic streptomycete strains had advantages over non-endophytic streptomycetes that would guarantee successful positive plant host response . Representative streptomycetes possess the ability to colonize the rhizosphere or endophytic tissues of plants [6, 87], to produce spores resistant to irradiation, heat, and drought , and to have an impressive range of metabolites with a variety of biological activities . Streptomyces may also convert plant exudates or macromolecules/supramolecules present in the rhizosphere into a form that can be used by other plant growth-promoting microbes. This proposition originated from our research group and represents a technological conversion of the fundamental concept of ecological succession of community members and metabolic cooperation. In this line of research, we combined the non-starch-degrading diazotrophic bacterium H. seropedicae strain HRC54 with S. bellus strain UENF AC 06, and verified that an increased population of the bacteria was probably sustained by C-sources from a starch degradation by-product. It is noteworthy that Herbaspirillum did not grow when S. bellus was absent in the medium and when starch was the sole C-source (unpublished results). It is another example of a simple idea that can be converted into a biotechnological product with a range of applications for sustainable crop production.
Concluding remarks and perspectives
The greatest challenge for agriculture in the current century is to produce food for the increasing world population and to reduce the dependence on non-renewable resources and environmental impact. The use of plant growth-promoting microbes to enhance crop production has emerged as a sustainable and alternative tool to meet this challenge . The most studied and technologically developed plant growth-promoting microbes mainly include rhizobia and other Gram-negative bacteria. However, besides their widely known ability to produce antibiotics, representatives of the Gram-positive genus Streptomyces have been found in beneficial associations with plants, including those of agronomic importance [64, 142–144]. The diversity of bioactive compounds produced by Streptomyces spp. includes substances capable of improving plant growth; hence, they are recognized as PGPS. Increased knowledge of secondary metabolic pathways involving the production of bioactive compounds and mechanisms of plant growth promotion by Streptomyces will be assisted by the rapid development of functional genomics and bioinformatics over the coming years. PGPS can promote plant growth by colonizing the rhizosphere or the endophytic plant environment. However, the interactions between rhizosphere PGPS and indigenous microbiota as well as the infection process performed by endophytic PGPS are still not clearly elucidated. Metagenomic approaches and the use of molecular markers such as fluorescent proteins will certainly contribute to the study of dynamic microbial populations in the plant rhizosphere, PGPS inoculation, and streptomycetes endophytic plant colonization. In addition, the use of PGPS as commercial biofertilizers is developing, but research into the design of bioinoculant formulations (such as additives, carriers, and delivery methods) will increase the plant growth and yields and acceptance by farmers around the world.
JAJS and FLO contributed equally to this review. Both authors read and approved the final manuscript.
The authors declare that they have no competing interests.
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- Godfray HCJ, et al. Food security: the challenge of feeding 9 billion people. Science. 2010;327(5967):812–8.PubMedView ArticleGoogle Scholar
- Tilman D, et al. Global food demand and the sustainable intensification of agriculture. Proc Natl Acad Sci USA. 2011;108(50):20260–4.PubMedPubMed CentralView ArticleGoogle Scholar
- Ahemad M, Kibret M. Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. J King Saud Univ Sci. 2014;26(1):1–20.View ArticleGoogle Scholar
- Bashan Y, et al. Advances in plant growth-promoting bacterial inoculant technology: formulations and practical perspectives (1998–2013). Plant Soil. 2014;378(1–2):1–33.View ArticleGoogle Scholar
- Abbamondi GR, et al. Plant growth-promoting effects of rhizospheric and endophytic bacteria associated with different tomato cultivars and new tomato hybrids. Chem Biol Technol Agric. 2016;3(1):1–10.View ArticleGoogle Scholar
- Bonaldi M, et al. Colonization of lettuce rhizosphere and roots by tagged Streptomyces. Front Microbiol. 2015;6:25.PubMedPubMed CentralView ArticleGoogle Scholar
- Francis I, Holsters M, Vereecke D. The Gram-positive side of plant-microbe interactions. Environ Microbiol. 2010;12(1):1–12.PubMedView ArticleGoogle Scholar
- Nebbioso A, et al. Phytochemical profiling of tomato roots following treatments with different microbial inoculants as revealed by IT-TOF mass spectrometry. Chem Biol Technol Agric. 2016;3(1):1–8.View ArticleGoogle Scholar
- Lightfield J, Fram NR, Ely B. Across bacterial phyla, distantly-related genomes with similar genomic GC content have similar patterns of amino acid usage. PLoS One. 2011;6(3):e17677.PubMedPubMed CentralView ArticleGoogle Scholar
- Qin S, et al. Biodiversity, bioactive natural products and biotechnological potential of plant-associated endophytic actinobacteria. Appl Microbiol Biotechnol. 2011;89(3):457–73.PubMedView ArticleGoogle Scholar
- Flärdh K. Growth polarity and cell division in Streptomyces. Curr Opin Microbiol. 2003;6(6):564–71.PubMedView ArticleGoogle Scholar
- Flardh K, Buttner MJ. Streptomyces morphogenetics: dissecting differentiation in a filamentous bacterium. Nat Rev Microbiol. 2009;7(1):36–49.PubMedView ArticleGoogle Scholar
- Porter JR. Antony van Leeuwenhoek: tercentenary of his discovery of bacteria. Bacteriol Rev. 1976;40(2):260–9.PubMedPubMed CentralGoogle Scholar
- Hopwood DA. Streptomyces in nature and medicine: the antibiotic makers. Oxford: Oxford University Press; 2007.Google Scholar
- Dworkin M, Falkow S. The prokaryotes: vol. 4: bacteria: firmicutes, cyanobacteria, vol. 4. Berlin: Springer Science & Business Media; 2006.Google Scholar
- Cambau E, Drancourt M. Steps towards the discovery of Mycobacterium tuberculosis by Robert Koch, 1882. Clin Microbiol Infect. 2014;20(3):196–201.PubMedView ArticleGoogle Scholar
- Daniel TM. The history of tuberculosis. Respir Med. 2006;100(11):1862–70.PubMedView ArticleGoogle Scholar
- Buchanan RE. Studies in the nomenclature and classification of the bacteria: VIII. The subgroups and genera of the Actinomycetales. J Bacteriol. 1918;3(4):403–6.PubMedPubMed CentralGoogle Scholar
- Waksman SA. Streptomycin: background, isolation, properties, and utilization. Science. 1953;118(3062):259–66.PubMedView ArticleGoogle Scholar
- Kämpfer P, et al. The family Streptomycetaceae, in the prokaryotes. Berlin: Springer; 2014. p. 889–1010.Google Scholar
- Chandra G, Chater KF. Developmental biology of Streptomyces from the perspective of 100 actinobacterial genome sequences. FEMS Microbiol Rev. 2014;38(3):345–79.PubMedView ArticleGoogle Scholar
- Ochi K. A taxonomic study of the genus Streptomyces by analysis of ribosomal-protein at-L30. Int J Syst Bacteriol. 1995;45(3):507–14.PubMedView ArticleGoogle Scholar
- Ludwig W, et al. Road map of the phylum Actinobacteria, in Bergey’s manual® of systematic bacteriology. Berlin: Springer; 2012. p. 1–28.View ArticleGoogle Scholar
- Petrus MLC, Claessen D. Pivotal roles for Streptomyces cell surface polymers in morphological differentiation, attachment and mycelial architecture. Antonie Van Leeuwenhoek Int J Gen Mol Microbiol. 2014;106(1):127–39.View ArticleGoogle Scholar
- Pridham TG, Hesseltine CW, Benedict RG. A guide for the classification of Streptomycetes according to selected groups—placement of strains in morphological sections. Appl Microbiol. 1958;6(1):52–79.PubMedPubMed CentralGoogle Scholar
- Tresner HD, Davies MC, Backus EJ. Electron microscopy of Streptomyces spore morphology and its role in species differentiation. J Bacteriol. 1961;81:70–80.PubMedPubMed CentralGoogle Scholar
- Atalan E, et al. Biosystematic studies on novel streptomycetes from soil. Antonie Van Leeuwenhoek Int J Gen Mol Microbiol. 2000;77(4):337–53.View ArticleGoogle Scholar
- Laidi RF, et al. Taxonomy, identification and biological activities of a novel isolate of Streptomyces tendae. Arab J Biotechnol. 2006;9:427–36.Google Scholar
- Schleifer KH, Kandler O. Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev. 1972;36(4):407–77.PubMedPubMed CentralGoogle Scholar
- Yamaguchi T. Comparison of the cell-wall composition of morphologically distinct actinomycetes. J Bacteriol. 1965;89:444–53.PubMedPubMed CentralGoogle Scholar
- Shashkov AS, et al. A polymer with a backbone of 3-deoxy-d-glycero-d-galacto-non-2-ulopyranosonic acid, a teichuronic acid, and a beta-glucosylated ribitol teichoic acid in the cell wall of plant pathogenic Streptomyces sp. VKM Ac-2124. Eur J Biochem. 2002;269(24):6020–5.PubMedView ArticleGoogle Scholar
- Tatar D, et al. Streptomyces iconiensis sp. nov. and Streptomyces smyrnaeus sp. nov., two halotolerant actinomycetes isolated from a salt lake and saltern. Int J Syst Evol Microbiol. 2014;64(Pt 9):3126–33.PubMedView ArticleGoogle Scholar
- Weidenmaier C, Peschel A. Teichoic acids and related cell-wall glycopolymers in gram-positive physiology and host interactions. Nat Rev Microbiol. 2008;6(4):276–87.PubMedView ArticleGoogle Scholar
- Acharyabhatta A, Kandula SK, Terli R. Taxonomy and polyphasic characterization of alkaline amylase producing marine actinomycete Streptomyces rochei BTSS 1001. Int J Microbiol. 2013;2013:276921.PubMedPubMed CentralView ArticleGoogle Scholar
- Hamid M. The use of morphological and cell wall chemical markers in the identification of Streptomyces species associated with Actinomycetoma. Afr J Clin Exp Microbiol. 2013;14(2):45–50.Google Scholar
- Lechevalier MP, Lechevalier H. Chemical composition as a criterion in the classification of aerobic actinomycetes. Int J Syst Bacteriol. 1970;20(4):435–43.View ArticleGoogle Scholar
- Dyson P. Streptomyces, in encyclopedia of microbiology. 3rd ed. In: Schaechter M, editor. Oxford: Academic Press; 2009. p. 318–332.Google Scholar
- Hasani A, Kariminik A, Issazadeh K. Streptomycetes: characteristics and their antimicrobial activities. Int J Adv Biol Biomed Res. 2014;2(1):63–75.Google Scholar
- Mistry BV, et al. FtsW is a dispensable cell division protein required for Z-ring stabilization during sporulation septation in Streptomyces coelicolor. J Bacteriol. 2008;190(16):5555–66.PubMedPubMed CentralView ArticleGoogle Scholar
- Willemse J, et al. Positive control of cell division: FtsZ is recruited by SsgB during sporulation of Streptomyces. Genes Dev. 2011;25(1):89–99.PubMedPubMed CentralView ArticleGoogle Scholar
- Flardh K, et al. Generation of a non-sporulating strain of Streptomyces coelicolor A3(2) by the manipulation of a developmentally controlled ftsZ promoter. Mol Microbiol. 2000;38(4):737–49.PubMedView ArticleGoogle Scholar
- Pimentel-Elardo SM, et al. Streptomyces axinellae sp. nov., isolated from the mediterranean sponge Axinella polypoides (Porifera). Int J Syst Evol Microbiol. 2009;59(Pt 6):1433–7.PubMedView ArticleGoogle Scholar
- Reponen TA, et al. Characteristics of airborne actinomycete spores. Appl Environ Microbiol. 1998;64(10):3807–12.PubMedPubMed CentralGoogle Scholar
- Claessen D, et al. Bacterial solutions to multicellularity: a tale of biofilms, filaments and fruiting bodies. Nat Rev Microbiol. 2014;12(2):115–24.PubMedView ArticleGoogle Scholar
- van Wezel GP, McDowall KJ. The regulation of the secondary metabolism of Streptomyces: new links and experimental advances. Nat Prod Rep. 2011;28(7):1311–33.PubMedView ArticleGoogle Scholar
- Olano C, et al. Improving production of bioactive secondary metabolites in actinomycetes by metabolic engineering. Metab Eng. 2008;10(5):281–92.PubMedView ArticleGoogle Scholar
- Bibb MJ. Regulation of secondary metabolism in streptomycetes. Curr Opin Microbiol. 2005;8(2):208–15.PubMedView ArticleGoogle Scholar
- Biarnes-Carrera M, Breitling R, Takano E. Butyrolactone signalling circuits for synthetic biology. Curr Opin Chem Biol. 2015;28:91–8.PubMedView ArticleGoogle Scholar
- Morgenstern A, et al. Divalent transition-metal-ion stress induces prodigiosin biosynthesis in Streptomyces coelicolor M145: formation of coeligiosins. Chemistry. 2015;21(16):6027–32.PubMedView ArticleGoogle Scholar
- Yekkour A, et al. A novel hydroxamic acid-containing antibiotic produced by a Saharan soil-living Streptomyces strain. Lett Appl Microbiol. 2015;60(6):589–96.PubMedView ArticleGoogle Scholar
- Rutledge PJ, Challis GL. Discovery of microbial natural products by activation of silent biosynthetic gene clusters. Nat Rev Microbiol. 2015;13(8):509–23.PubMedView ArticleGoogle Scholar
- Chakraburtty R, Bibb M. The ppGpp synthetase gene (relA) of Streptomyces coelicolor A3(2) play’s a conditional role in antibiotic production and morphological differentiation. J Bacteriol. 1997;179(18):5854–61.PubMedPubMed CentralGoogle Scholar
- Gomez-Escribano JP, et al. Streptomyces clavuligerus reIA-null mutants overproduce clavulanic acid and cephamycin C: negative regulation of secondary metabolism by (p)ppGpp. Microbiology-Sgm. 2008;154:744–55.View ArticleGoogle Scholar
- Chen C, et al. Effect of overexpression of endogenous and exogenous Streptomyces antibiotic regulatory proteins on c (FK506) production in Streptomyces sp KCCM11116P. Rsc Adv. 2015;5(21):15756–62.View ArticleGoogle Scholar
- Kurniawan YN, et al. Differential contributions of two SARP family regulatory genes to indigoidine biosynthesis in Streptomyces lavendulae FRI-5. Appl Microbiol Biotechnol. 2014;98(23):9713–21.PubMedView ArticleGoogle Scholar
- Xie C, Deng JJ, Wang HX. Identification of AstG1, A LAL family regulator that positively controls ansatrienins production in Streptomyces sp. XZQH13. Curr Microbiol. 2015;70(6):859–64.PubMedView ArticleGoogle Scholar
- Kim SB, et al. Taxonomic study of neutrotolerant acidophilic actinomycetes isolated from soil and description of Streptomyces yeochonensis sp. nov. Int J Syst Evol Microbiol. 2004;54(Pt 1):211–4.PubMedView ArticleGoogle Scholar
- Zakalyukina YV, Zenova G, Zvyagintsev D. Peculiarities of growth and morphological differentiation of acidophilic and neutrophilic soil streptomycetes. Microbiology. 2004;73(1):74–8.View ArticleGoogle Scholar
- Sultanpuram VR, Mothe T, Mohammed F. Streptomyces alkalithermotolerans sp. nov., a novel alkaliphilic and thermotolerant actinomycete isolated from a soda lake. Antonie Van Leeuwenhoek. 2015;107(2):337–44.PubMedView ArticleGoogle Scholar
- Antony-Babu S, Stach JE, Goodfellow M. Genetic and phenotypic evidence for Streptomyces griseus ecovars isolated from a beach and dune sand system. Antonie Van Leeuwenhoek. 2008;94(1):63–74.PubMedView ArticleGoogle Scholar
- Noda S, et al. 4-Vinylphenol biosynthesis from cellulose as the sole carbon source using phenolic acid decarboxylase- and tyrosine ammonia lyase-expressing Streptomyces lividans. Bioresour Technol. 2015;180:59–65.PubMedView ArticleGoogle Scholar
- Xu J, et al. Streptomyces xiamenensis sp. nov., isolated from mangrove sediment. Int J Syst Evol Microbiol. 2009;59(Pt 3):472–6.PubMedView ArticleGoogle Scholar
- Hamedi J, Mohammadipanah F. Biotechnological application and taxonomical distribution of plant growth promoting actinobacteria. J Ind Microbiol Biotechnol. 2015;42(2):157–71.PubMedView ArticleGoogle Scholar
- Jog R, et al. Mechanism of phosphate solubilization and antifungal activity of Streptomyces spp. isolated from wheat roots and rhizosphere and their application in improving plant growth. Microbiology. 2014;160(Pt 4):778–88.PubMedView ArticleGoogle Scholar
- Duncan KR, et al. Exploring the diversity and metabolic potential of actinomycetes from temperate marine sediments from Newfoundland, Canada. J Ind Microbiol Biotechnol. 2015;42(1):57–72.PubMedView ArticleGoogle Scholar
- Hartmann A, Rothballer M, Schmid M. Lorenz Hiltner, a pioneer in rhizosphere microbial ecology and soil bacteriology research. Plant Soil. 2008;312(1–2):7–14.View ArticleGoogle Scholar
- Oh YM, et al. Distinctive bacterial communities in the rhizoplane of four tropical tree species. Microb Ecol. 2012;64(4):1018–27.PubMedView ArticleGoogle Scholar
- Doornbos RF, van Loon LC, Bakker PA. Impact of root exudates and plant defense signaling on bacterial communities in the rhizosphere. A review. Agron Sustain Dev. 2012;32(1):227–43.View ArticleGoogle Scholar
- Bais HP, et al. The role of root exudates in rhizosphere iterations with plants and other organisms. Annu Rev Plant Biol. 2006;57:233–66.PubMedView ArticleGoogle Scholar
- Bever JD, Platt TG, Morton ER. Microbial population and community dynamics on plant roots and their feedbacks on plant communities. Annu Rev Microbiol. 2012;66:265–83.PubMedPubMed CentralView ArticleGoogle Scholar
- Compant S, Clement C, Sessitsch A. Plant growth-promoting bacteria in the rhizo- and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem. 2010;42(5):669–78.View ArticleGoogle Scholar
- Berg G. Plant-microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl Microbiol Biotechnol. 2009;84(1):11–8.PubMedView ArticleGoogle Scholar
- Challis GL, Ravel J. Coelichelin, a new peptide siderophore encoded by the Streptomyces coelicolor genome: structure prediction from the sequence of its non-ribosomal peptide synthetase. FEMS Microbiol Lett. 2000;187(2):111–4.PubMedView ArticleGoogle Scholar
- Trejo-Estrada S, Paszczynski A, Crawford D. Antibiotics and enzymes produced by the biocontrol agent Streptomyces violaceusniger YCED-9. J Ind Microbiol Biotechnol. 1998;21(1–2):81–90.View ArticleGoogle Scholar
- Gherbawy Y, et al. Molecular screening of Streptomyces isolates for antifungal activity and family 19 chitinase enzymes. J Microbiol. 2012;50(3):459–68.PubMedView ArticleGoogle Scholar
- Fyans JK, et al. The ESX/type VII secretion system modulates development, but not virulence, of the plant pathogen Streptomyces scabies. Mol Plant Pathol. 2013;14(2):119–30.PubMedView ArticleGoogle Scholar
- Langlois P, et al. Identification of Streptomyces coelicolor proteins that are differentially expressed in the presence of plant material. Appl Environ Microbiol. 2003;69(4):1884–9.PubMedPubMed CentralView ArticleGoogle Scholar
- Lin L, et al. Thaxtomin A-deficient endophytic Streptomyces sp. enhances plant disease resistance to pathogenic Streptomyces scabies. Planta. 2012;236(6):1849–61.PubMedView ArticleGoogle Scholar
- Anne J, et al. Protein secretion biotechnology in gram-positive bacteria with special emphasis on Streptomyces lividans. Biochim Biophys Acta. 2014;1843(8):1750–61.PubMedView ArticleGoogle Scholar
- Bischoff V, et al. Thaxtomin A affects CESA-complex density, expression of cell wall genes, cell wall composition, and causes ectopic lignification in Arabidopsis thaliana seedlings. J Exp Bot. 2009;60(3):955–65.PubMedPubMed CentralView ArticleGoogle Scholar
- Joshi M, et al. Streptomyces turgidiscabies secretes a novel virulence protein, Nec1, which facilitates infection. Mol Plant Microbe Interact. 2007;20(6):599–608.PubMedView ArticleGoogle Scholar
- Loria R, et al. Thaxtomin biosynthesis: the path to plant pathogenicity in the genus Streptomyces. Antonie Van Leeuwenhoek. 2008;94(1):3–10.PubMedView ArticleGoogle Scholar
- Johnson EG, et al. Plant-pathogenic Streptomyces species produce nitric oxide synthase-derived nitric oxide in response to host signals. Chem Biol. 2008;15(1):43–50.PubMedView ArticleGoogle Scholar
- Meschke H, Schrempf H. Streptomyces lividans inhibits the proliferation of the fungus Verticillium dahliae on seeds and roots of Arabidopsis thaliana. Microb Biotechnol. 2010;3(4):428–43.PubMedPubMed CentralView ArticleGoogle Scholar
- Palaniyandi SA, et al. Genetic and functional characterization of culturable plant-beneficial actinobacteria associated with yam rhizosphere. J Basic Microbiol. 2013;53(12):985–95.View ArticleGoogle Scholar
- Rungin S, et al. Plant growth enhancing effects by a siderophore-producing endophytic streptomycete isolated from a Thai jasmine rice plant (Oryza sativa L. cv. KDML105). Antonie Van Leeuwenhoek. 2012;102(3):463–72.PubMedView ArticleGoogle Scholar
- Coombs JT, Franco CM. Visualization of an endophytic Streptomyces species in wheat seed. Appl Environ Microbiol. 2003;69(7):4260–2.PubMedPubMed CentralView ArticleGoogle Scholar
- Shimizu M. Endophytic actinomycetes: biocontrol agents and growth promoters, in bacteria in agrobiology: plant growth responses. Berlin: Springer; 2011. p. 201–20.View ArticleGoogle Scholar
- Clark C, Matthews SW. Histopathology of sweet potato root infection by Streptomyces ipomoea. Phytopathology. 1987;77(10):1418–23.View ArticleGoogle Scholar
- Loria R, et al. A paucity of bacterial root diseases: Streptomyces succeeds where others fail. Physiol Mol Plant Pathol. 2003;62(2):65–72.View ArticleGoogle Scholar
- Suzuki T, et al. Visualization of infection of an endophytic actinomycete Streptomyces galbus in leaves of tissue-cultured rhododendron. 日本放線菌学会誌. 2005;19(1):7–12.Google Scholar
- Compant S, et al. Endophytic colonization of Vitis vinifera L. by plant growth-promoting bacterium Burkholderia sp. strain PsJN. Appl Environ Microbiol. 2005;71(4):1685–93.PubMedPubMed CentralView ArticleGoogle Scholar
- Conn VM, Walker AR, Franco CM. Endophytic actinobacteria induce defense pathways in Arabidopsis thaliana. Mol Plant Microbe Interact. 2008;21(2):208–18.PubMedView ArticleGoogle Scholar
- Miche L, et al. Upregulation of jasmonate-inducible defense proteins and differential colonization of roots of Oryza sativa cultivars with the endophyte Azoarcus sp. Mol Plant Microbe Interact. 2006;19(5):502–11.PubMedView ArticleGoogle Scholar
- Shah J. Plants under attack: systemic signals in defence. Curr Opin Plant Biol. 2009;12(4):459–64.PubMedView ArticleGoogle Scholar
- Yasuda M, et al. Effects of colonization of a bacterial endophyte, Azospirillum sp. B510, on disease resistance in rice. Biosci Biotechnol Biochem. 2009;73(12):2595–9.PubMedView ArticleGoogle Scholar
- Cho YH, Lee EJ, Roe JH. A developmentally regulated catalase required for proper differentiation and osmoprotection of Streptomyces coelicolor. Mol Microbiol. 2000;35(1):150–60.PubMedView ArticleGoogle Scholar
- Kim FJ, et al. Differential expression of superoxide dismutases containing Ni and Fe/Zn in Streptomyces coelicolor. Eur J Biochem. 1996;241(1):178–85.PubMedView ArticleGoogle Scholar
- Michta E, et al. Proteomic approach to reveal the regulatory function of aconitase AcnA in oxidative stress response in the antibiotic producer Streptomyces viridochromogenes Tu494. PLoS One. 2014;9(2):e87905.PubMedPubMed CentralView ArticleGoogle Scholar
- Johnston-Monje D, Raizada MN. Plant and endophyte relationships: nutrient management. Compr Biotechnol. 2011;2:713–27.View ArticleGoogle Scholar
- Balsanelli E, et al. Molecular adaptations of Herbaspirillum seropedicae during colonization of the maize rhizosphere. Environ Microbiol. 2015. doi:10.1111/1462-2920.12887.PubMedGoogle Scholar
- James EK, et al. Infection and colonization of rice seedlings by the plant growth-promoting bacterium Herbaspirillum seropedicae Z67. Mol Plant Microbe Interact. 2002;15(9):894–906.PubMedView ArticleGoogle Scholar
- Reinhold-Hurek B, et al. An endoglucanase is involved in infection of rice roots by the not-cellulose-metabolizing endophyte Azoarcus sp. strain BH72. Mol Plant Microbe Interact. 2006;19(2):181–8.PubMedView ArticleGoogle Scholar
- Saharan B, Nehra V. Plant growth promoting rhizobacteria: a critical review. Life Sci Med Res. 2011;21:1–30.Google Scholar
- Devau N, et al. Soil pH controls the environmental availability of phosphorus: experimental and mechanistic modelling approaches. Appl Geochem. 2009;24(11):2163–74.View ArticleGoogle Scholar
- Rajput MS, Kumar G, Rajkumar S. Repression of oxalic acid-mediated mineral phosphate solubilization in rhizospheric isolates of Klebsiella pneumoniae by succinate. Arch Microbiol. 2013;195(2):81–8.PubMedView ArticleGoogle Scholar
- Sadeghi A, et al. Plant growth promoting activity of an auxin and siderophore producing isolate of Streptomyces under saline soil conditions. World J Microbiol Biotechnol. 2012;28(4):1503–9.PubMedView ArticleGoogle Scholar
- Hamdali H, et al. Screening for rock phosphate solubilizing Actinomycetes from Moroccan phosphate mines. Appl Soil Ecol. 2008;38(1):12–9.View ArticleGoogle Scholar
- Hamdali H, et al. Streptomyces youssoufiensis sp nov., isolated from a Moroccan phosphate mine. Int J Syst Evol Microbiol. 2011;61:1104–8.PubMedView ArticleGoogle Scholar
- Ribbe M, Gadkari D, Meyer O. N2 fixation by Streptomyces thermoautotrophicus involves a molybdenum-dinitrogenase and a manganese-superoxide oxidoreductase that couple N2 reduction to the oxidation of superoxide produced from O2 by a molybdenum-CO dehydrogenase. J Biol Chem. 1997;272(42):26627–33.PubMedView ArticleGoogle Scholar
- MacKellar D, et al. Streptomyces thermoautotrophicus does not fix nitrogen. Sci Rep. 2016;6:20086.PubMedPubMed CentralView ArticleGoogle Scholar
- Teale WD, Paponov IA, Palme K. Auxin in action: signalling, transport and the control of plant growth and development. Nat Rev Mol Cell Biol. 2006;7(11):847–59.PubMedView ArticleGoogle Scholar
- Abd-Alla MH, El-Sayed E-SA, Rasmey A-HM. Indole-3-acetic acid (IAA) production by Streptomyces atrovirens isolated from rhizospheric soil in Egypt. J Biol Earth Sci. 2013;3(2):B182–93.Google Scholar
- Manulis S, et al. Biosynthesis of indole-3-acetic acid via the indole-3-acetamide pathway in Streptomyces spp. Microbiology. 1994;140(Pt 5):1045–50.PubMedView ArticleGoogle Scholar
- Lin L, Xu XD. Indole-3-acetic acid production by endophytic Streptomyces sp. En-1 isolated from medicinal plants. Curr Microbiol. 2013;67(2):209–17.PubMedView ArticleGoogle Scholar
- Igarashi Y. Screening of novel bioactive compounds from plant-associated actinomycetes. Actinomycetologica. 2004;18(2):63–6.View ArticleGoogle Scholar
- King RW, Evans LT. Gibberellins and flowering of grasses and cereals: prizing open the lid of the “florigen” black box. Annu Rev Plant Biol. 2003;54:307–28.PubMedView ArticleGoogle Scholar
- Pharis RP, King RW. Gibberellins and reproductive development in seed plants. Ann Rev Plant Physiol Plant Mol Biol. 1985;36:517–68.View ArticleGoogle Scholar
- Rashad FM, et al. Isolation and characterization of multifunctional Streptomyces species with antimicrobial, nematicidal and phytohormone activities from marine environments in Egypt. Microbiol Res. 2015;175:34–47.PubMedView ArticleGoogle Scholar
- Qiao J-Q, et al. Stimulation of plant growth and biocontrol by Bacillus amyloliquefaciens subsp. plantarum FZB42 engineered for improved action. Chem Biol Technol Agric. 2014;1(1):1–14.View ArticleGoogle Scholar
- Golinska P, Dahm H. Antagonistic properties of Streptomyces isolated from forest soils against fungal pathogens of pine seedlings. Dendrobiology. 2013;69.Google Scholar
- Kanini GS, et al. Greek indigenous streptomycetes as biocontrol agents against the soil-borne fungal plant pathogen Rhizoctonia solani. J Appl Microbiol. 2013;114(5):1468–79.PubMedView ArticleGoogle Scholar
- Ruanpanun P, et al. Nematicidal activity of fervenulin isolated from a nematicidal actinomycete, Streptomyces sp. CMU-MH021, on Meloidogyne incognita. World J Microbiol Biotechnol. 2011;27(6):1373–80.PubMedView ArticleGoogle Scholar
- Tarkka MT, et al. Draft genome sequence of Streptomyces sp. strain 150FB, a mushroom mycoparasite antagonist. Genome Announc. 2015;3(2):e01441.PubMedPubMed CentralGoogle Scholar
- Berg G, Smalla K. Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol. 2009;68(1):1–13.PubMedView ArticleGoogle Scholar
- Kurth F, et al. Streptomyces-induced resistance against oak powdery mildew involves host plant responses in defense, photosynthesis, and secondary metabolism pathways. Mol Plant Microbe Interact. 2014;27(9):891–900.PubMedView ArticleGoogle Scholar
- Atkinson NJ, Urwin PE. The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot. 2012;63(10):3523–43.PubMedView ArticleGoogle Scholar
- El-Tarabily KA. Promotion of tomato (Lycopersicon esculentum Mill.) plant growth by rhizosphere competent 1-aminocyclopropane-1-carboxylic acid deaminase-producing Streptomycete actinomycetes. Plant Soil. 2008;308(1–2):161–74.View ArticleGoogle Scholar
- Palaniyandi SA, et al. Streptomyces sp. strain PGPA39 alleviates salt stress and promotes growth of ‘Micro Tom’ tomato plants. J Appl Microbiol. 2014;117(3):766–73.PubMedView ArticleGoogle Scholar
- Schrey SD, et al. Production of fungal and bacterial growth modulating secondary metabolites is widespread among mycorrhiza-associated streptomycetes. BMC Microbiol. 2012;12:164.PubMedPubMed CentralView ArticleGoogle Scholar
- Bonfante P, Anca IA. Plants, mycorrhizal fungi, and bacteria: a network of interactions. Annu Rev Microbiol. 2009;63:363–83.PubMedView ArticleGoogle Scholar
- Schrey SD, Tarkka MT. Friends and foes: streptomycetes as modulators of plant disease and symbiosis. Antonie Van Leeuwenhoek Int J Gen Mol Microbiol. 2008;94(1):11–9.View ArticleGoogle Scholar
- Tokala RK, et al. Novel plant-microbe rhizosphere interaction involving Streptomyces lydicus WYEC108 and the pea plant (Pisum sativum). Appl Environ Microbiol. 2002;68(5):2161–71.PubMedPubMed CentralView ArticleGoogle Scholar
- Maier A, et al. Actinomycetales bacteria from a spruce stand: characterization and effects on growth of root symbiotic and plant parasitic soil fungi in dual culture. Mycol Prog. 2004;3(2):129–36.View ArticleGoogle Scholar
- Schrey SD, et al. Mycorrhiza helper bacterium Streptomyces AcH 505 induces differential gene expression in the ectomycorrhizal fungus Amanita muscaria. New Phytol. 2005;168(1):205–16.PubMedView ArticleGoogle Scholar
- Figueiredo MDVB, et al. Plant growth promoting rhizobacteria: fundamentals and applications, in plant growth and health promoting bacteria. Berlin: Springer; 2011. p. 21–43.Google Scholar
- Gopalakrishnan S, et al. Plant growth-promoting traits of Streptomyces with biocontrol potential isolated from herbal vermicompost. Biocontrol Sci Tech. 2012;22(10):1199–210.View ArticleGoogle Scholar
- Gopalakrishnan S, et al. Evaluation of Streptomyces strains isolated from herbal vermicompost for their plant growth-promotion traits in rice. Microbiol Res. 2014;169(1):40–8.PubMedView ArticleGoogle Scholar
- Kinkel LL, et al. Streptomyces competition and co-evolution in relation to plant disease suppression. Res Microbiol. 2012;163(8):490–9.PubMedView ArticleGoogle Scholar
- Chater KF. Streptomyces inside-out: a new perspective on the bacteria that provide us with antibiotics. Philos Trans R Soc Lond B Biol Sci. 2006;361(1469):761–8.PubMedPubMed CentralView ArticleGoogle Scholar
- Canellas LP, Olivares FL. Physiological responses to humic substances as plant growth promoter. Chem Biol Technol Agric. 2014;1(1):1–11.View ArticleGoogle Scholar
- Araújo JMD, Silva ACD, Azevedo JL. Isolation of endophytic actinomycetes from roots and leaves of maize (Zea mays L.). Braz Arch Biol Technol. 2000;43(4):0–0.View ArticleGoogle Scholar
- Hu D, et al. Genome sequence of Streptomyces sp. strain TOR3209, a rhizosphere microecology regulator isolated from tomato rhizosphere. J Bacteriol. 2012;194(6):1627.PubMedPubMed CentralView ArticleGoogle Scholar
- Kuramata M, et al. Arsenic biotransformation by Streptomyces sp. isolated from rice rhizosphere. Environ Microbiol. 2015;17(6):1897–909.PubMedView ArticleGoogle Scholar
- Bentley SD, et al. Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature. 2002;417(6885):141–7.PubMedView ArticleGoogle Scholar
- Phongsopitanun W, et al. Streptomyces chumphonensis sp. nov., isolated from marine sediments. Int J Syst Evol Microbiol. 2014;64(Pt 8):2605–10.PubMedView ArticleGoogle Scholar
- Srivastava S, et al. Streptomyces rochei SM3 induces stress tolerance in Chickpea against Sclerotinia sclerotiorum and NaCl. J Phytopathol. 2014;163(7–8):583–92.Google Scholar
- Li J, et al. Streptomyces fildesensis sp. nov., a novel streptomycete isolated from Antarctic soil. Antonie Van Leeuwenhoek. 2011;100(4):537–43.PubMedView ArticleGoogle Scholar
- Lambert D, Loria R. Streptomyces scabies sp. nov., nom. rev. Int J Syst Bacteriol. 1989;39(4):387–92.View ArticleGoogle Scholar
- Mingma R, et al. Streptomyces oryzae sp. nov., an endophytic actinomycete isolated from stems of rice plant. J Antibiot (Tokyo). 2015;68(6):368–72.View ArticleGoogle Scholar
- Oliveira LG, et al. Genome sequence of Streptomyces wadayamensis strain A23, an endophytic actinobacterium from Citrus reticulata. Genome Announc. 2014;2(4):e00625.PubMedPubMed CentralView ArticleGoogle Scholar
- Sarmin NI, et al. Streptomyces kebangsaanensis sp. nov., an endophytic actinomycete isolated from an ethnomedicinal plant, which produces phenazine-1-carboxylic acid. Int J Syst Evol Microbiol. 2013;63(Pt 10):3733–8.PubMedView ArticleGoogle Scholar
- Bian GK, et al. Streptomyces phytohabitans sp. nov., a novel endophytic actinomycete isolated from medicinal plant Curcuma phaeocaulis. Antonie Van Leeuwenhoek. 2012;102(2):289–96.PubMedView ArticleGoogle Scholar
- Aguiar KP. Prospecção de bactérias promotoras do crescimento vegetalassociadas a vermicompostos., in CCTA. Campos dos Goytacazes: Universidade Estadual do Norte Fluminense Darcy Ribeiro; 2012. p. 101.Google Scholar
- Jesus JA. Potencial Biotecnológico de actinobactérias e bactérias diazotróficas para o crescimento de plantas, in CCTA. Campos dos Goytacazes: Universidade Estadual do Norte Fluminense Darcy Ribeiro; 2013. p. 107.Google Scholar
- Shao L, et al. Identification of the Herboxidiene biosynthetic gene cluster in Streptomyces chromofuscus ATCC 49982. Appl Environ Microbiol. 2012;78(6):2034–8.PubMedPubMed CentralView ArticleGoogle Scholar
- Hindra, Pak P, Elliot MA. Regulation of a novel gene cluster involved in secondary metabolite production in Streptomyces coelicolor. J Bacteriol. 2010;192(19):4973–82.PubMedPubMed CentralView ArticleGoogle Scholar
- Mansouri K, Piepersberg W. Genetics of Streptomycin production in Streptomyces-griseus—nucleotide-sequence of 5 genes, Strfghik, including a phosphatase gene. Mol Gen Genet. 1991;228(3):459–69.PubMedView ArticleGoogle Scholar
- Rascher A, et al. Insights into the biosynthesis of the benzoquinone ansamycins geldanamycin and herbimycin, obtained by gene sequencing and disruption. Appl Environ Microbiol. 2005;71(8):4862–71.PubMedPubMed CentralView ArticleGoogle Scholar
- Wu K, et al. The FK520 gene cluster of Streptomyces hygroscopicus var. ascomyceticus (ATCC 14891) contains genes for biosynthesis of unusual polyketide extender units. Gene. 2000;251(1):81–90.PubMedView ArticleGoogle Scholar
- He J, Hertweck C. Iteration as programmed event during polyketide assembly; molecular analysis of the aureothin biosynthesis gene cluster. Chem Biol. 2003;10(12):1225–32.PubMedView ArticleGoogle Scholar
- Fernandez-Martinez LT, et al. New insights into chloramphenicol biosynthesis in Streptomyces venezuelae ATCC 10712. Antimicrob Agents Chemother. 2014;58(12):7441–50.PubMedPubMed CentralView ArticleGoogle Scholar
- He M, et al. Isolation and characterization of meridamycin biosynthetic gene cluster from Streptomyces sp. NRRL 30748. Gene. 2006;377:109–18.PubMedView ArticleGoogle Scholar
- Schwartz D, et al. Biosynthetic gene cluster of the herbicide phosphinothricin tripeptide from Streptomyces viridochromogenes Tu494. Appl Environ Microbiol. 2004;70(12):7093–102.PubMedPubMed CentralView ArticleGoogle Scholar
- Patzer SI, Braun V. Gene cluster involved in the biosynthesis of griseobactin, a catechol-peptide siderophore of Streptomyces sp. ATCC 700974. J Bacteriol. 2010;192(2):426–35.PubMedView ArticleGoogle Scholar
- Legault GS, et al. Tryptophan regulates thaxtomin A and indole-3-acetic acid production in Streptomyces scabiei and modifies its interactions with radish seedlings. Phytopathology. 2011;101(9):1045–51.PubMedView ArticleGoogle Scholar
- Kieser T, et al. Practical Streptomyces genetics. Norwich: The John Innes Foundation; 2000.Google Scholar