Abstract
Grain legumes are a cost-effective alternative for the animal protein in improving the diets of the poor in South-East Asia and Africa. Legumes, through symbiotic nitrogen fixation, meet a major part of their own N demand and partially benefit the following crops of the system by enriching soil. In realization of this sustainability advantage and to promote pulse production, United Nations had declared 2016 as the “International Year of pulses”. Grain legumes are frequently subjected to both abiotic and biotic stresses resulting in severe yield losses. Global yields of legumes have been stagnant for the past five decades in spite of adopting various conventional and molecular breeding approaches. Furthermore, the increasing costs and negative effects of pesticides and fertilizers for crop production necessitate the use of biological options of crop production and protection. The use of plant growth-promoting (PGP) bacteria for improving soil and plant health has become one of the attractive strategies for developing sustainable agricultural systems due to their eco-friendliness, low production cost and minimizing consumption of non-renewable resources. This review emphasizes on how the PGP actinobacteria and their metabolites can be used effectively in enhancing the yield and controlling the pests and pathogens of grain legumes.
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Introduction
Grain legumes also called ‘Poor man’s meat’ are an essential entity in food and feed due to its protein, minerals, and other bioactive molecules. Increasing nutritional awareness increased the per-capita consumption of grain legumes across the world (Amarowicz and Pegg 2008). The symbiotic association of leguminous crops with rhizobia contributes 65% of nitrogen (N) needs. Their better adaptation as an inter-crop with cereals or tuber crops helps in increased income generation and livelihood resilience of small holder farmers. However, production level of such leguminous crops has constraints in various forms such as pest and pathogen attacks, infertile soils, and climate changes. Development of improved cultivars through breeding and molecular techniques had been practiced; still, the productivity remains stagnant for the last two decades. All these together attracted the attention at global level, and thus, the general assembly of United Nations has announced this year as ‘International Year of Pulses (2016 IYOP)’ to emphasize the need for focusing on pulses for food and nutritional security and to create awareness and understanding of the challenges faced in pulse farming and trading (FAO 2014).
A cleaner and greener approach towards the improvement of leguminous crop production is the use of a category of microbes called Plant Growth-Promoting Rhizobacteria (PGPR), a group of heterogeneous bacteria found in rhizosphere or plant tissues (Kloepper and Schroth 1978). They induce plant growth by enhancing the availability of soil nutrients, supplying phytohormones, and inducing systemic resistance against phytopathogens. There are voluminous data available on PGPR, but most of it belongs to the phylum Bacteroidetes, Firmicutes, and Proteobacteria, of which the most commonly studied are Azospirillum, Azotobacter, Bacillus, Pseudomonas, Gluconacetobacter, Enterobacter, Serratia, Paenibacillus, and Rhizobium (Bhattacharyya and Jha 2012). However, the reports on the plant growth-promoting (PGP) traits of bacteria belonging to the phylum Actinobacteria are limited, despite its ubiquitous existence in bulk soil, rhizospheric soil, and plant tissues and their usefulness in agriculture (Bhattacharyya and Jha 2012; Jog et al. 2012). Hence, this review emphasizes to document mainly on PGP traits of actinobacteria and how far it was studied in the context of growth-promotion, biocontrol against pests, and pathogens, as mitigators of abiotic stress, as a tool for enhanced phytoremediation and bio-fortification.
Actinobacteria diversity
The bacteria belong to the phylum Actinobacteria are Gram-positive filamentous bacteria, with 6 classes, 25 orders, 52 families, and 232 genera and represent one of the largest taxonomic units among the 18 major lineages currently recognized within the domain Bacteria (Stackebrandt and Schumann 2000). They can thrive in either bulk soil or rhizospheric soil, and due to spore forming characteristics, they can remain dormant in agricultural soil for a longer period. The actinobacteria population increases with the soil depth up to horizon ‘C’. It is estimated that actinobacteria are distributed with average 104–106 spores g−1 soil in various crops fields (Shaharokhi et al. 2005; Ul-Hassan and Wellington 2009). Though they are mesophilic organisms, species of the family such as Thermoactinomycetaceae are commonly found in compost and manures at thermophilic growing temperature (Ul-Hassan and Wellington 2009). They also stay as either epiphyte or endophyte in plant tissues of wide host range including barley, wheat, rice, soybean, cowpea, chickpea, banana, tomato, and medicinal plants. Among them, Streptomyces is the predominant genus followed by Actinomadura, Microbispora, Micromonospora, Nocardia, Nonomurea, Mycobacterium, Frankia, Actinoplanes, Saccharopolyspora, and Verrucosispora (Martinez-Hidalgo et al. 2014; Vijayabharathi et al. 2016).
PGP traits of actinobacteria
As like other PGPR, actinobacteria also employ both direct and in-direct mechanisms to influence the plant growth and protection. The direct mechanisms involve the production of vital factors for crop growth such as growth hormones and the assistive actions on nitrogen fixation, phosphate solubilization, and iron acquisition. PGP actinobacteria indirectly influence the plant growth by controlling and minimizing the deleterious effects of external stresses of either biotic or abiotic sources through the following modes: competition for nutrients, production of low molecular inhibitory substances such as ammonia, cyanogens, alcohols, aldehydes, sulfides, and ketones, cell-wall degrading enzymes, and secondary metabolites with biocidal properties, in which the latter, two are the key phenomenon deployed by the actinobacterial community (El-Tarabily and Sivasithamparam 2006; Glick 2012; Bouizgarne 2013; Dey et al. 2014).
Nitrogen fixation
Nitrogen is the major essential crop nutrient available through the process called symbiotic N fixation. This was aided by the relationship between the members of the family Rhizobiaceae, Bradirhizobiaceae, and Phyllobacteriaceae with the leguminous plants through the formation of N-fixing specialized structure called nodules (Schultze and Kondorosi 1998). Frankia, a versatile N fixing actinobacteria, fixes N in non-legumes under both symbiotic and free-living conditions. It infects the root cells of actinorhizal plants through either intracellular root-hair infection or intercellular root invasion (Benson and Silvester 1993). Besides this, several other endophytic actinobacteria exhibited N-fixing ability which includes Arthrobacter, Agromyces, Corynebacterium, Mycobacterium, Micromonospora, Propionibacteria, and Streptomyces (Sellstedt and Richau 2013). This was demonstrated long back by Fedorov and Kalininskaya (1961) by their ability to grow on N-free medium and acetylene reduction activity. Recent studies using 15N isotope dilution analysis and identification of nif genes further support this phenomenon (Valdes et al. 2005; Ghodhbane-Gtari et al. 2010). Molecular studies have established the fact that many actinobacteria can occur as endophytes in various leguminous and non-leguminous plants without forming nodule. This is supported by the existence of nif sequence homology in both Rhizobium and Frankia, the absence of nod genes in the latter (Ceremonie et al. 1999). Even under field conditions, enhanced nodulation of chickpea and soil N content observed upon the application of Streptomyces inoculants indicates their promotional effect and influence of rhizobia-legume symbiosis in a non-specific manner (Gopalakrishnan et al. 2015a, b). However, a detailed understanding of the mechanisms on this symbiotic mode needs to be established.
Phosphate solubilization
Influence of PGPR in enabling the availability of phosphate to plants through various mechanisms is highlighted by various researchers across a range of soil conditions. In the context of actinobacteria, Arthrobacter, Rhodococcus, Gordonia, Streptomyces, and Micromonospora have been reported for P solubilization in vitro and glass house conditions (Chen et al. 2006; Hamdali et al. 2008; Jog et al. 2014). Initial report on P solubilizing capacity of a non-streptomycete Micromonospora endolithica and its subsequent effect on the growth of bean plants have been reported by El-Tarabily et al. (2008). Similar effect has also been demonstrated on wheat by Micromonospora aurantiaca, Streptomyces griseus, and Streptomyces sp., under P-deficient soil (Hamdali et al. 2008; Jog et al. 2014). In these actinobacterial strains, production of various organic acid including citric acid, gluconic acid, lactic acid, malic acid, oxalic acid, propionic acid, and succinic acid which aids for P solubilization has been demonstrated (Chen et al. 2006; Hamdali et al. 2010; Jog et al. 2014).
Iron acquisition
Iron in soil is known for its un-availability to both plants and microbes due to its normal presence as insoluble hydroxides and oxyhydroxides. This is made available by the synthesis of siderophores, the low molecular weight compounds which have high affinity towards iron. Iron chelation by microbial siderophores from soil depends on its pH, concentration, redox potential, stability constant, and receptor availability to exchange with phytosiderophores (Crowley 2006). Microbes produce variety of siderophores and a major class includes catechols and hydroxamate. Numerous strains of actinobacteria have been reported as siderophore producers (Wang et al. 2014). The genus Streptomyces is well known for its siderophores, including its own characteristic types such as hydroxamate siderophores: desferrioxamines and coelichelin (Imbert et al. 1995; Challis and Ravel 2000); siderophore of other actinobacteria members: heterobactin, a siderophore of Rhodococcus and Nocardia (Lee et al. 2012); and also siderophores of other bacterial members: enterobactin, siderophore of the family Enterobacteriaceae (Fiedler et al. 2001). Besides the context of plant nutrition, siderophore also offers for plant protection through the control of phytopathogens. They acquire iron thereby create a competitive environment for other pathogenic microbes in the root vicinity (Glick 2012). This is an effective phenomenon in controlling fungal pathogens as they produce low-affinity siderophores, which can be eliminated by high affinity siderophores of actinobacteria (Wang et al. 2014). Such siderophore producing Streptomyces was also found to show control against Fusarium oxysporum f. sp. ciceri under wilt sick field conditions on chickpea (Gopalakrishnan et al. 2011).
Phytohormones
Phytohormone producing capacity of several rhizospheric and endophytic actinobacteria was demonstrated by various researchers for indole acetic acid (IAA), cytokinins, and gibberellins (El-Tarabily and Sivasithamparam 2006; Vijayabharathi et al. 2016). In recent years, endophytic actinobacteria are getting greater interest. Nocardiopsis, an endophytic actinobacterium associated with mandarin recorded highest IAA production (222.75 ppm) (Shutsrirung et al. 2013). IAA producing endophytic Streptomyces atrovirens, Streptomyces olivaceoviridis, Streptomyces rimosus, Streptomyces rochei, and Streptomyces viridis showed improved seed germination and root elongation and growth (El-Tarabily 2008; Khamna et al. 2010; Abd-Alla et al. 2013). IAA also triggers cell differentiation, hyphal elongation, and sporulation in Streptomyces atroolivaceus (Matsukawa et al. 2007). Metabolites such as pteridic acids A and B produced by endophytic Streptomyces hygroscopicus TP_A045 were found to show auxin-like activity and induce root elongation in common bean (Igarashi et al. 2002). Hence, the phytohormone producing potential and metabolites with phytohormone mimicking activity of actinobacteria can be exploited for enhancing crop productivity of not only legumes and also other crops.
Cell wall degrading enzymes
Majority of soil actinobacteria are saprophytic in nature and core of decomposition, which was aided by the synthesis of various classes of extracellular enzymes including nucleases, lipases, glucanases, xylanases, amylases, proteinases, peptidases, peroxidases, chitinases, cellulases, ligninases, pectinase, hemicellulase, and keratinase. All these enzymes together contribute to its biocontrol potential against a wide range of phytopathogens, because the cell wall of most fungal and bacterial pathogens consist of polymers such as chitin, glucan, cellulose, proteins, and lipids (Gupta et al. 1995; Fodil et al. 2011). Among them, chitinases are of great importance and many Streptomyces spp. are observed to inhibit both fungal pathogens and insect pests (Tahmasebpour et al. 2014; Karthik et al. 2015; Yandigeri et al. 2015).
Other secondary metabolites
According to the literature survey, there are around 300,000 to 600,000 natural compounds derived from living sources. Among them, the major contributors are found to be microbes (60–80,000), of which actinobacteria accounts for ~60% of new antibiotics. This is supported by the genetic makeup of biosynthetic pathways and their enzyme activities for branching, alkylations, condensations, isomerizations, and oxidations. The single genus, Streptomyces, is the major producer (39%) of secondary metabolites (Olano et al. 2008; Berdy 2012). In addition, they have the capacity to produce a wide variety of compounds including polyene macrolides, actinomycins, aminoglycosides, streptothricins, anthracyclines, cyclopolylactones, and quinoxaline peptides. Non-Streptomyces actinobacteria also found to produce compounds such as glycopeptides and orthosomycins (Nicolaou et al. 2009).
It is also noted that half of the microbial metabolites express one or multiple bioactivities including antibiotic or enzyme inhibitory activities or other activity. In the context of agriculture, more than 3000 pesticide and herbicide activities, including phytotoxic, plant growth regulatory, insecticide, larvicide, acaricide, algicide, and nematicide activities were reported. The major advantage of using secondary metabolites from actinobacteria over the fungal metabolites is lower phytotoxic activity. More than 50% of fungal metabolites were observed to be phytotoxic which contrasts with the 2% of phytotoxic actinoproducts (Berdy 2012). These kinds of actinobacteria have a competitive edge over other microbial communities as it increases their chances of survival. This characteristic has been exploited more than five decades ago and studied by several researchers for the biological control of plant pathogens and disease suppression (Weindling et al. 1950; Chamberlain and Crawford 1999; Meschke et al. 2012). Several commercial formulations with the antibiotic or microbes as an active ingredient are marketed as biocontrol products. Representatives include, Actinovate® and Actino-Iron® by Streptomyces lydicus WYEC 108 (Crawford et al. 2005), Arzent™ by four different strains of Streptomyces hygroscopicus (Hamby and Crawford 2000) and Mycostop® by Streptomyces griseoviridis K61 (Figueiredo et al. 2010). Besides this, Blasticidin-S from Streptomyces griseochromogenes and kasugamycin from Streptomyces kasugaensis against rice blast disease, mildiomycin from Streptomyces rimofaciens against powdery mildew disease, oxytetracycline form S. rimosus for the control of bacterial diseases, and polyoxins from Streptomyces cacaoi for the control of fungal incidences at field levels demonstrates the importance of secondary metabolites from actinobacteria for sustainable agriculture. Several reviews depicting the importance of actinobacteria and its compounds as biocontrol agents are available (Copping and Menn 2000; Copping and Duke 2007).
Host plant resistance
Host plant resistance is one of the key tools for management of phytopathogens and pests in which the protection is conferred systemically even in the non-exposed parts of the plant. Plants were reported with two types of non-specific defense systems: (1) induced systemic resistance (ISR) primed by the influence of beneficial microbes and (2) systemic acquired resistance (SAR) primed by the influence of pathogens (Schuhegger et al. 2006). The ISR mediated by rhizobacteria predisposes the plants to resist further attacks. On the contrary, the SAR is induced by pathogens, resulting in the activation of resistance mechanisms in other uninfected parts of plants. In general, the defense systems are mediated by signaling molecules such as jasmonic acid (JA), salicylic acid (SA), and ethylene (ET) (Pieterse et al. 1996). JA activates defense-related genes: defensins, thionins, and pectinase inhibitors (Hause et al. 2002). The SA induces genes that encode the pathogenesis-related proteins (PRs) such as chitinase, β-1,3 glucanases, and thaumatin such as proteins and peroxidases (Uknes et al. 1992). Actinobacteria are demonstrated as inducers of plant immunization against different pathogens such as Rhizoctonia, Fusarium, Pythium, Phytophthora, and Colletotrichum (Raaijmakers et al. 2009). Endophytic actinobacterium Streptomyces sp. was able to control take-all disease of wheat and potato scab under the field conditions (Liu et al. 1996; Coombs et al. 2004). Conn et al. (2008) observed that endophytic Streptomyces sp. EN27 and Micromonospora sp. EN 43 are able to induce resistance in Arabidopsis thaliana by up-regulating genes involved in SAR. Culture filtrates of EN 43 also induced SAR and the JA/ET pathway. The bacterial determinants involved in triggering ISR include secondary metabolites, siderophores, and colonization efficiency. Recently, many studies on Streptomyces-induced host plant resistance were evaluated on range of crops including forage crops, vegetable crops, and economically important woody species such as Arabidopsis (Bernardo et al. 2013), potato (Arseneault et al. 2014), oak (Kurth et al. 2014), and Eucalyptus (Salla et al. 2016), and such an opportunity for encasing actinobacteria for grain legumes needs to be exploited.
PGP actinobacteria as helper bacteria
Actinobacteria are able to promote N-fixing symbiosis (Solans 2007; Solans and Vobis 2013) and also in other symbiotic relationships of legumes and non-legumes plants by their role as helper bacteria; however, it is documented in very few reports. Actinobacteria are found to promote mycorrhizal symbioses via the promotion of hyphal elongation of symbiotic fungi (Schrey and Tarkka 2008). Such an enhanced mycorrhizal symbiosis was observed on the roots of sorghum and clover by Streptomyces coelicolor and Streptomyces spp. MCR9 and MCR24, respectively (Abdel-Fattah and Mohamedin 2000; Franco-Correa et al. 2010).
Solans and their research group have studied the helper effect of actinobacteria with various host plants. This was demonstrated in the system of Ochetophila trinervis and Frankia, with the co-inoculation of Streptomyces MM40, Actinoplanes ME3, and Micromonospora MM18 (Solans 2007). The same actinobacteria were studied in other symbiotic systems of Medicago sativa–Sinorhizobium meliloti (Solans et al. 2009) and Lotus tenuis–Mesorhizobium loti (Solans et al. 2015). It was noticed that the plants co-inoculated with actinobacteria and rhizobium showed increased nodulation and plant growth compared to the plants with single inoculations. Similar results were noted by other researchers as well. The combination of Streptomyces kanamyceticus and Bradyrhizobium japonicum increased nodulation and shoot N composition of soybean by up to 55 and 41%, respectively (Gregor et al. 2003). Soe and Yamakawa (2013) examined the effect of co-inoculation of Bradyrhizobium yuanmingense MAS34 and Streptomyces griseoflavus P4 in enhancing nodulation, N2 fixation, and seed yield in different soybean varieties. The results of these researchers clearly demonstrated the importance of actinobacterial inoculants in growth promotion of leguminous and non-leguminous plants.
PGP actinobacteria as stress relievers
Abiotic stress factors such as extreme temperatures, drought, flooding, salinity, metal stress, and nutrient stress are likely to cause serious impacts on crop yields and impose severe pressure on soil and water resources. According to the estimates from Food and Agricultural Organization (FAO), abiotic stress factors will result in 30% land degradation in the next 25 years and up to 50% by the year 2050 if precautionary measures are not taken (Munns 2002).
Actinobacteria are known to possess better tolerance towards temperature, salinity, and metals; inoculation of such tolerant strains is observed to promote plant growth. Aly et al. (2003, 2012) observed the PGP effect of Streptomyces sp. on maize and wheat under saline conditions. Palaniyandi et al. (2014) observed enhanced biomass and lateral roots of Arabidopsis seedlings under in vitro conditions of 1 mol l−1NaCl upon the inoculation with Streptomyces sp. PGPA39 exhibiting salt tolerance and other PGP traits. Srivastava et al. (2015) attempted to study the mechanism underlying actinobacteria-mediated stress tolerance in chickpea. They used Streptomyces rochei SM3 against the challenges of Sclerotinia sclerotiorum and NaCl on chickpea. Treatment with SM3 suppressed chickpea mortality due to S. sclerotiorum infection (48%) and increased biomass accumulation (20%) in the salt-stressed conditions. Physiological responses showed increased phenylalanine ammonia lyase and catalase activities, along with the accumulation of phenolics and proline in SM3-treated plants. Investigation at genetic level further showed that the strain SM3 triggered the ET responsive ERF transcription factor (CaTF2) under the challenged conditions. Drought tolerant endophytic actinobacteria, Streptomyces coelicolor DE07, Streptomyces olivaceus DE10, and Streptomyces geysiriensis DE27, with intrinsic water stress tolerance from −0.05 to −0.73 MPa and IAA production were isolated from arid and drought affected regions. Co-inoculation of endophytes DE10 and DE27 recorded the highest yield in wheat (Yandigeri et al. 2012). In addition, induction of higher osmotic pressure of plant cells, callose accumulation, and cell wall lignification as a strategy for drought tolerance has been documented for Streptomyces padanus (Hasegawa et al. 2004, 2005). Recent studies on Streptomyces pactum Act12, a multifunctional strain with drought resistance, metal resistance (Cao et al. 2016), and antagonistic traits against phytopathogenic fungus (Zhao et al. 2011) explores the role of these in-kind actinomycetes for arid and semi-arid regions.
Responding to stress, plant synthesizes higher level of ET called ‘stress ethylene’ which leads to plants’ premature death. In fact, some of the effects of stress cannot solely be attributed to the stress itself but are also due to autocatalytic ethylene synthesis (Van Loon 1984). These effects can be controlled by the action of an enzyme of microbial origin, 1-aminocyclopropane-1-carboxylate (ACC) deaminase which converts the ethylene precursor ACC to ammonia and α-ketobutyrate. Characterization of this enzyme effects on stress management is observed for the past two decades, and now considered as a key phenomenon of PGP traits (Glick 1995). Many of the actinobacteria are shown to produce ACC deaminase such as Streptomyces, Amycolatopsis, Nocardia, Mycobacterium, Rhodococcus, and others (Nascimento et al. 2014). Siddikee et al. (2010) isolated several halotolerant actinobacteria strains with ACC deaminase, from the soil of barren fields and the rhizosphere of naturally growing halophytic plants and found that they can increase canola plant growth. Similarly, Selvakumar et al. (2015) identified ACC deaminase producing Citricoccus zhacaiensis B-4, an osmotolerant actinobacterium from the banana rhizosphere and observed improved percent germination, seedling vigor and germination rate on onion seeds (cv. Arka Kalyan) at osmotic potentials up to −0.8 MPa. El-Tarabily (2008) showed that ACC deaminase producing Streptomyces filipinensis 15 and S. atrovirens 26 could reduce tomato endogenous ACC levels in both roots and shoots, resulting in increased plant growth. Similarly, Palaniyandi et al. (2013) also showed that some Streptomyces spp. of yam rhizospheres could produce ACC deaminase. Dastager et al. (2010) indicated that the cowpea PGP bacterium Micrococcus sp. NII-0909 produced ACC deaminase under free-living conditions. Idris et al. (2004) isolated endophytic Curtobacterium, Okibacterium, and Rhodococcus strains with ACC deaminase activity from Thlaspi goesingense. All these suggest that, irrespective of habitat, i.e., rhizospheric/endophytic or stressed/non-stressed soil, actinobacteria with ACC deaminase can be used for the dual purposes of enhancing productivity and stress control.
PGP actinobacteria in bioremediation of metals
Metal pollution of agricultural lands has risen mainly by anthropogenic activities, led to the shrinkage of healthy agricultural cropland, and hence demands the farmers to use contaminated sites for crop cultivation. According to the Environmental Protection Agency (EPA) report, the United States had more than 40,000 contaminated sites. In addition, 100,000 ha of cropland, 55,000 ha of pasture, and 50,000 ha of forest have been lost by heavy metal contamination and demands for reclamation process (Ragnarsdottir and Hawkins 2005). PGPR reside in metalliferous soil with higher metal solubilizing and extracting capacity can play decisive role in the context of bioremediation besides enhancing phytoremediation process. Metal mobilizing property of these microbes is aided by its own substances such as siderophores, organic acids, polymeric substances, biosurfactants, and glycoprotein and also by the reactions such as metal reduction and oxidization and biosorption. Mechanism behind the metal mobilization was reviewed in detail by Ma et al. (2011), Rajkumar et al. (2012), and Sessitsch et al. (2013), and a review on current research status of bioremediation involving actinobacteria has been given by Alvarez et al. (2017). From the published data, it is understood that actinobacteria with metal mobilizing and PGP traits were evaluated mostly on non-edible/hyper accumulating plants and on toxic metals in the area of phytoremediation. Such works on edible crops were a few. Some of the representative reports stating the potential of PGP actinobacteria with metal mobilization traits were given in Table 1.
PGP actinobacteria as nutrient enhancer
Actinobacteria influence the soil fertility through the involvement of many components and serve as nutrient enhancer. Besides producing siderophores and solubilizes phosphate, they are known to produce cocktail of enzymes which include amylase, chitinase, cellulase, invertase, lipase, keratinase, peroxidase, pectinase, protease, phytase, and xylanase which make the complex nutrients into simple mineral forms. This nutrient cycling capacity makes them as an ideal candidate for natural fertilizers (Jog et al. 2016). In addition, the metal mobilizing ability can be applied for biofortification approaches for enhancing seed mineral nutrients such as Fe, Zn, and Se. However, limited studies are available on legumes. A recent study had revealed that arbuscular mycorrhizal fungal colonization on chickpea roots enhanced the crop growth, and grain Fe and Zn contents (Pellegrino and Bedini 2014). Verma et al. (2013) documented the effect of two PGPR isolates, Mesorhizobium sp. and Pseudomonas sp., on chickpea in enhancing yield and Fe acquisition under greenhouse and field conditions. Similar results were reported by Rudresh et al. (2005) using a consortium of Rhizobium sp., phosphate solubilizing Bacillus megaterium sub sp. phospaticum and Trichoderma sp. on chickpea under greenhouse and field conditions. Recent study of Khalid et al. (2015) on chickpea further supports the ability of PGP bacterial strains with siderophore producing capacity in increasing Fe concentration. Some of the PGP Streptomyces from our microbial collection were found to increase the grain Fe and Zn contents by 38 and 30%, respectively, in chickpea (Sathya et al. 2016). Though the effects of actinobacteria were not reported in the context of biofortification, previously demonstrated effects on their metal mobilization property along with PGP reveals that, actinobacteria are capable of mobilizing minerals and metals in a wide range of food crops including cereals, oil seeds, and leguminous crops.
Conclusion
The present review documents the potential of PGP actinobacteria and highlights its unique properties in plant growth induction, defense pathways, and stress management. The available information suggests that actinobacteria represent a hidden repertoire and sustainable source for bioactive and chemically novel natural products, which can explored to a great extent in various fields of agricultural sector. However, such an extent of success especially on legumes under field conditions is limited. This indicates the existence of large gaps between research and development of potential actinobacterial inoculums for field application. Therefore, generation of comprehensive knowledge on screening, characterization, and formulation strategies and understanding of molecular mechanisms behind their action and evaluation at field levels are necessary.
References
Abd-Alla MH, El-Sayed ESA, Rasmey AHM (2013) Indole-3-acetic acid (IAA) production by Streptomyces atrovirens isolated from rhizospheric soil in Egypt. J Biol Earth Sci 3:B182–B193
Abdel-Fattah GM, Mohamedin AH (2000) Interactions between a vesicular–arbuscular mycorrhizal fungus (Glomus intraradices) and Streptomyces coelicolor and their effects on sorghum plants grown in soil amended with chitin of brawn scales. Biol Fertil Soils 32:401–409
Alvarez A, Saez JM, Costa JS, Colin VL, Fuentes MS, Cuozzo SA, Benimeli CS, Polti MA, Amoroso MJ (2017) Actinobacteria: current research and perspectives for bioremediation of pesticides and heavy metals. Chemosphere 166:41–62
Aly MM, El-Sabbagh SM, El-Shouny WA, Ebrahim MKH (2003) Physiological response of Zea mays to NaCl stress with respect to Azotobacter chroococcum and Streptomyces niveus. Pak J Biol Sci 6:2073–2080
Aly MM, El Sayed HEA, Jastaniah SD (2012) Synergistic effect between Azotobacter vinelandii and Streptomyce spp. isolated from saline soil on seed germination and growth of wheat plant. J Am Sci 8:667–676
Amarowicz R, Pegg RB (2008) Legumes as a source of natural antioxidants. Eur J Lipid Sci Technol 110:865–878
Arseneault T, Pieterse CM, Gérin-Ouellet M, Goyer C, Filion M (2014) Long-term induction of defense gene expression in potato by Pseudomonas sp. LBUM223 and Streptomyces scabies. Phytopathology 104:926–932
Benson DR, Silvester WB (1993) Biology of Frankia strains, actinomycete symbionts of actinorhizal plants. Microbiol Mol Biol Rev 57:293–319
Berdy J (2012) Thoughts and facts about antibiotics: where we are now and where we are heading. J Antibiot 65:385–395
Bernardo KT, Franco CMM, Chataway T (2013) Proteomic analysis in Arabidopsis thaliana inoculated with a beneficial endophytic Streptomyces sp. in response to a challenge by the pathogen Fusarium oxysporum. In: Schneider C, Leifert C, Feldmann F (eds) Endophytes for plant protection: the state of the art. Proceedings of the 5th international symposium on plant protection and plant health in Europe, 26–29 May 2013, Humboldt University Berlin, Berlin-Dahlem, Germany, pp 78–87
Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbiol Biotechnol 28:1327–1350
Bouizgarne B (2013) Bacteria for plant growth promotion and disease management. In: Maheshwari DK (ed) Bacteria in agrobiology: disease management. Springer, Berlin, pp 15–47
Cao S, Wang W, Wang F, Zhang J, Wang Z, Yang S, Xue Q (2016) Drought-tolerant Streptomyces pactum Act12 assist phytoremediation of cadmium-contaminated soil by Amaranthus hypochondriacus: great potential application in arid/semi-arid areas. Environ Sci Pollut Res Int 15:14898–14907
Ceremonie H, Debellé F, Fernandez MP (1999) Structural and functional comparison of Frankia root hair deforming factor and rhizobia Nod factor. Can J Bot 77:1293–1301
Challis GL, Ravel J (2000) 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 187:111–114
Chamberlain K, Crawford DL (1999) In vitro and in vivo antagonism of pathogenic turf grass fungi by Streptomyces hygroscopicus strains YCED9 and WYE53. J Ind Microbiol Biotechnol 23:641–646
Chen YP, Rekha PD, Arun AB, Shen FT, Lai WA, Young CC (2006) Phosphate solubilizing bacteria from subtropical soil and their tricalcium phosphate solubilizing abilities. Appl Soil Ecol 34(1):33–41
Conn VM, Walker AR, Franco CMM (2008) Endophytic actinobacteria induce defense pathways in Arabidopsis thaliana. Mol Plant Microbe Interact 21:208–218
Coombs JT, Michelsen PP, Franco CMM (2004) Evaluation of endophytic actinobacteria as antagonists of Gaeumannomyces graminis var. tritici in wheat. Biol Control 29:359–366
Copping LG, Duke SO (2007) Natural products that have been used commercially as crop protection agents. Pest Manag Sci 63:524–554
Copping LG, Menn JJ (2000) Biopesticides: a review of their action, applications and efficacy. Pest Manag Sci 56:651–676
Crawford DL, Kowalski M, Roberts MA, Merrel G, Deobald LA (2005) Discovery, development and commercialization of a microbial antifungal biocontrol agent Streptomyces lydicus WYEC108: history of a decade long endeavour. Soc Ind Microbiol News 55:88–95
Crowley DA (2006) Microbial siderophores in the plant rhizosphere. In: Barton LL, Abadia J (eds) Iron nutrition in plants and rhizospheric microorganisms. Springer, Netherlands, pp 169–189
Dastager SG, Deepa CK, Pandey A (2010) Isolation and characterization of novel plant growth-promoting Micrococcus sp. NII-0909 and its interaction with cowpea. Plant Physiol Biochem 48:987–992
Dey R, Pal KK, Tilak KVBR (2014) Plant growth promoting rhizobacteria in crop protection and challenges. In: Goyal A, Manoharachary C (eds) Future challenges in crop protection against fungal pathogens. Springer Science, New York, pp 31–58
Dimkpa CO, Svatos A, Merten D, Büchel G, Kothe E (2008) Hydroxamate siderophores produced by Streptomyces acidiscabies E13 bind nickel and promote growth in cowpea (Vigna unguiculata L.) under nickel stress. Can J Microbiol 54:163–172
Dimkpa CO, Merten D, Svatoš A, Büchel G, Kothe E (2009) Siderophores mediate reduced and increased uptake of cadmium by Streptomyces tendae F4 and sunflower (Helianthus annuus), respectively. J Appl Microbiol 107:1687–1696
El-Tarabily KA (2008) Promotion of tomato (Lycopersicon esculentum Mill.) plant growth by rhizosphere competent 1-aminocyclopropane-1-carboxylic acid deaminase-producing streptomycete actinomycetes. Plant Soil 308:161–174
El-Tarabily KA, Sivasithamparam K (2006) Non-streptomycete actinomycetes as biocontrol agents of soil-borne fungal plant pathogens and as plant growth promoters. Soil Biol Biochem 38:1505–1520
El-Tarabily KA, Nassar AH, Sivasithamparam K (2008) Promotion of growth of bean (Phaseolus vulgaris L.) in a calcareous soil by a phosphate-solubilizing, rhizosphere-competent isolate of Micromonospora endolithica. Appl Soil Ecol 39(2):161–171
FAO (2014) Food and Agriculture Organization. International year of pulses. http://www.un.org/en/ga/search/view_doc.asp?symbol=A/RES/68/231&referer=http://www.un.org/en/events/observances/years.shtml&Lang=E. Last Accessed 11th Feb 2016
Fedorov MV, Kalininskaya TA (1961) A new species of nitrogen fixing Mycobacterium and its physiological properties. Mikrobiologiya 30:7–11
Fiedler HP, Krastel P, Müller J, Gebhardt K, Zeeck A (2001) Enterobactin: the characteristic catecholate siderophore of Enterobacteriaceae is produced by Streptomyces species. FEMS Microbiol Lett 196:147–151
Figueiredo MVB, Seldin L, Araujo FF, Mariano RLR (2010) Plant growth promoting rhizobacteria: fundamentals and applications. In: Maheshwari DK (ed) Plant growth and health promoting bacteria. Microbiology monographs. Springer, Berlin, pp 21–43
Fodil D, Badis A, Jaouadib B, Zarai N, Ferradji FZ, Boutoumi H (2011) Purification and characterization of two extracellular peroxidases from Streptomyces sp. strain AM2, a decolorizing actinomycetes responsible for the biodegradation of natural humic acids. Int Biodeterior Biodegrad 65:470–478
Franco-Correa M, Quintana A, Duque C, Suarez C, Rodríguez MX, Barea JM (2010) Evaluation of actinomycete strains for key traits related with plant growth-promotion and mycorrhiza helping activities. Appl Soil Ecol 45:209–217
Ghodhbane-Gtari F, Essoussi I, Chattaoui M, Jaouani A, Daffonchio D, Boudabous A, Gtari M (2010) Isolation and characterization of non-Frankia actinobacteria from root nodules of Alnus glutinosa, Casuarina glauca and Elaeagnus angustifolia. Symbiosis 50:51–57
Glick BR (1995) The enhancement of plant growth by free-living bacteria. Can J Microbiol 117:109–117
Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica 2012:15
Gopalakrishnan S, Pande S, Sharma M, Humayun P, Kiran BK, Sandeep D, Vidya MS, Deepthi K, Rupela O (2011) Evaluation of actinomycete isolates obtained from herbal vermicompost for the biological control of Fusarium wilt of chickpea. Crop Prot 30:1070–1078
Gopalakrishnan S, Vadlamudi S, Alekhya G, Prakash B, Kudapa H, Varshney RK (2015a) Evaluation of Streptomyces sp. obtained from herbal vermicompost for broad spectrum of plant growth-promoting activities in chickpea. Org Agric 5:123–133
Gopalakrishnan S, Vadlamudi S, Alekhya G, Prakash B, Kudapa H, Varshney RK (2015b) The extent of grain yield and plant growth enhancement by plant growth-promoting broad-spectrum Streptomyces sp. in chickpea. SpringerPlus 4:31
Gregor AK, Klubek B, Varsa EC (2003) Identification and use of actinomycetes for enhanced nodulation of soybean co-inoculated with Bradyrhizobium japonicum. Can J Microbiol 49:483–491
Gupta R, Saxena RK, Chaturvedi P, Virdi VS (1995) Chitinase production by Streptomyces viridificans: its potential in fungal cell wall lysis. J Appl Bacteriol 78:378–383
Hamby MK, Crawford DL (2000) The enhancement of plant growth by selected Streptomyces species. In: American Society for Microbiology, 100th general meeting, Los Angeles, CA. Abstract no: 567
Hamdali H, Hafidi M, Virolle MJ, Ouhdouch Y (2008) Growth promotion and protection against damping-off of wheat by two rock phosphate solubilizing actinomycetes in a P-deficient soil under greenhouse conditions. Appl Soil Ecol 40(3):510–517
Hamdali H, Smirnov A, Esnault C, Ouhdouch Y, Virolle MJ (2010) Physiological studies and comparative analysis of rock phosphate solubilization abilities of Actinomycetales originating from Moroccan phosphate mines and of Streptomyces lividans. Appl Soil Ecol 44:24–31
Hasegawa S, Meguro A, Nishimura T, Kunoh H (2004) Drought tolerance of tissue-cultured seedlings of mountain laurel (Kalmia latifolia L.) induced by an endophytic actinomycete. I. Enhancement of osmotic pressure in leaf cells. Actinomycetologica 18:43–47
Hasegawa S, Meguro A, Toyoda K, Nishimura T, Kunoh H (2005) Drought tolerance of tissue-cultured seedlings of mountain laurel (Kalmia latifolia L.) induced by an endophytic actinomycete. II. Acceleration of callose accumulation and lignification. Actinomycetologica 19:13–17
Hause B, Maier W, Miersch O, Kramell R, Strack D (2002) Induction of jasmonate biosynthesis in arbuscular mycorrhizal barley roots. Plant Physiol 130:1213–1220
He LY, Zhang YF, Ma HY, Su LN, Chen ZJ, Wang QY, Qian M, Sheng XF (2010) Characterization of copper resistant bacteria and assessment of bacterial communities in rhizosphere soils of copper-tolerant plants. Appl Soil Ecol 44:49–55
Idris R, Trifonova R, Puschenreiter M, Sessitsch A, Puschenreiter M, Wenzel WW (2004) Bacterial communities associated with flowering plants of the Ni hyper accumulator Thlaspi goesingense. Appl Environ Microbiol 70:2667–2677
Igarashi Y, Iida T, Yoshida R, Furumai T (2002) Pteridic acids A and B, novel plant growth promoters with auxin-like activity from Streptomyces hygroscopicus TP-A0451. J Antibiot 55:764–767
Imbert M, Bechet M, Blondeau R (1995) Comparison of the main siderophores produced by some species of Streptomyces. Curr Microbiol 31:129–133
Jog R, Nareshkumar G, Rajkumar S (2012) Plant growth-promoting potential and soil enzyme production of the most abundant Streptomyces spp. from wheat rhizosphere. J Appl Microbiol 113:1154–1164
Jog R, Pandhya M, Nareshkumar G, Rajkumar S (2014) Mechanism of phosphate solubilization and antifungal activity of Streptomyces spp. isolated from wheat roots and rhizosphere and their application in improving plant growth. Microbiology 160:778–788
Jog R, Nareshkumar G, Rajkumar S (2016) Enhancing soil health and plant growth promotion by actinomycetes. In: Gopalakrishnan S, Sathya A, Vijayabharathi R (eds) Plant growth promoting actinobacteria. Springer, Singapore, pp 33–45
Joshi PM, Juwarkar AA (2009) In vivo studies to elucidate the role of extracellular polymeric substances from Azotobacter in immobilization of heavy metals. Environ Sci Technol 43:5884–5889
Karthik N, Binod P, Pandey A (2015) Purification and characterisation of an acidic and antifungal chitinase produced by a Streptomyces sp. Bioresour Technol 188:195–201
Khalid S, Asghar HN, Akhtar MJ, Aslam A, Zahir ZA (2015) Biofortification of iron in chickpea by plant growth-promoting rhizobacteria. Pak J Bot 47:1191–1194
Khamna S, Yokota A, Peberdy JF, Lumyong S (2010) Indole-3-acetic acid production by Streptomyces sp. isolated from some Thai medicinal plant rhizosphere soils. EurAsia J BioSci 4:23–32
Kloepper JW, Schroth MN (1978) Plant growth-promoting rhizobacteria on radishes. Proceedings of the 4th international conference on plant pathogenic bacteria, vol 2. Station de Pathologie Vegetaleet de Phytobacteriologie, INRA, Angers, pp 879–882
Kurth F, Mailänder S, Bönn M, Feldhahn L, Herrmann S, Große I, Buscot F, Schrey SD, Tarkka MT (2014) Streptomyces-induced resistance against oak powdery mildew involves host plant responses in defense, photosynthesis, and secondary metabolism pathways. Mol Plant Microbe Interact 27:891–900
Lee J, Postmaster A, Soon HP, Keast D, Carson KC (2012) Siderophore production by actinomycetes isolates from two soil sites in Western Australia. Biometals 25:285–296
Liu D, Anderson NA, Kinke LL (1996) Selection and characterization of strains of Streptomyces suppressive to the potato scab pathogen. Can J Microbiol 42:487–502
Ma Y, Prasad MNV, Rajkumar M, Freitas H (2011) Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnol Adv 29:248–258
Martinez-Hidalgo P, Olivares J, Delgado A, Bedmar E, Martínez-Molina E (2014) Endophytic Micromonospora from Medicago sativa are apparently not able to fix atmospheric nitrogen. Soil Biol Biochem 74:201–203
Matsukawa E, Nakagawa Y, Iimura Y, Hayakawa M (2007) Stimulatory effect of indole-3-acetic acid on aerial mycelium formation and antibiotic production in Streptomyces spp. Actinomycetologica 21:32–39
Meschke H, Walter S, Schrempf H (2012) Characterization and localization of prodiginines from Streptomyces lividans suppressing Verticillium dahliae in the absence or presence of Arabidopsis thaliana. Environ Microbiol 14:940–952
Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250
Nascimento FX, Rossi MJ, Soares CRFS, McConkey B, Glick BR (2014) New insights into 1-aminocyclopropane-1-carboxylate (ACC) deaminase phylogeny, evolution and ecological significance. PLoS One 9:e99168
Nicolaou KC, Chen JS, Edmonds DJ, Estrada AA (2009) Recent advances in the chemistry and biology of naturally occurring antibiotics. Angew Chem Int Ed 48:660–719
Olano C, Lombó F, Méndez C, Salas JA (2008) Improving production of bioactive secondary metabolites in actinomycetes by metabolic engineering. Metab Eng 10:281–292
Palaniyandi S, Yang SH, Damodharan K, Suh JW (2013) Genetic and functional characterization of culturable plant-beneficial actinobacteria associated with yam rhizosphere. J Basic Microbiol 53:985–995
Palaniyandi SA, Damodharan K, Yang SH, Suh JW (2014) Streptomyces sp. strain PGPA39 alleviates salt stress and promotes growth of ‘Micro Tom’tomato plants. J Appl Microbiol 117(3):766–773
Pellegrino E, Bedini S (2014) Enhancing ecosystem services in sustainable agriculture: biofertilization and biofortification of chickpea (Cicer arietinum L.) by arbuscular mycorrhizal fungi. Soil Biol Biochem 68:429–439
Pieterse CM, Van Wees SC, Hoffland E, Van Pelt JA, Van Loon LC (1996) Systemic resistance in Arabidopsis induced by biocontrol bacteria is independent of salicylic acid accumulation and pathogenesis-related gene expression. Plant Cell 8:1225–1237
Raaijmakers JM, Paulitz TC, Steinberg C, Alabouvette C, Moenne-Loccoz Y (2009) The rhizosphere: a playground and battlefield for soil borne pathogens and beneficial microorganisms. Plant Soil 321:341–361
Ragnarsdottir KV, Hawkins D (2005) Trace metals in soils and their relationship with scrapie occurrence. Geochim Cosmochim Acta 69:A194–A196
Rajkumar M, Sandhya S, Prasad MNV, Freitas H (2012) Perspectives of plant-associated microbes in heavy metal phytoremediation. Biotechnol Adv 30:1562–1574
Rudresh DL, Shivaprakash MK, Prasad RD (2005) Effect of combined application of Rhizobium, phosphate solubilizing bacterium and Trichoderma spp. on growth, nutrient uptake and yield of chickpea (Cicer aritenium L.). Appl Soil Ecol 28:139–146
Salla TD, Astarita LV, Santarém ER (2016) Defense responses in plants of Eucalyptus elicited by Streptomyces and challenged with Botrytis cinerea. Planta 243:1055–1070
Sathya A, Vijayabharathi R, Srinivas V, Gopalakrishnan S (2016) Plant growth-promoting actinobacteria on chickpea seed mineral density: an upcoming complementary tool for sustainable biofortification strategy. 3 Biotech 6(2):1–6
Schrey SD, Tarkka MT (2008) Friends and foes: streptomycetes as modulators of plant disease and symbiosis. Antonie van Leeuw 94:11–19
Schuhegger R, Ihring A, Gantner S, Bahnweg G, Knappe C, Vogg G, Hutzler P, Schmid M, Breusegem FV, Eberl L, Hartmann A, Langebartels C (2006) Induction of systemic resistance in tomato by N-acyl-l-homoserine lactone-producing rhizosphere bacteria. Plant Cell Environ 29:909–918
Schultze M, Kondorosi A (1998) Regulation of symbiotic root nodule development. Ann Rev Genet 32:33–57
Schütze E, Klose M, Merten D, Nietzsche S, Senftleben D, Roth M, Kothe E (2014) Growth of streptomycetes in soil and their impact on bioremediation. J Hazard Mater 267:128–135
Schumann P (2000) Introduction to the taxonomy of actinobacteria. In: Dworkin M et al (eds) The prokaryotes: an evolving electronic resource for the microbiological community. Springer, New York
Sellstedt A, Richau KH (2013) Aspects of nitrogen-fixing actinobacteria, in particular free-living and symbiotic Frankia. FEMS Microbiol Lett 342:179–186
Selvakumar G, Bhatt RM, Upreti KK, Bindu GH, Shweta K (2015) Citricoccus zhacaiensis B-4 (MTCC 12119) a novel osmotolerant plant growth-promoting actinobacterium enhances onion (Allium cepa L.) seed germination under osmotic stress conditions. World J Microbiol Biotechnol 31:833–839
Sessitsch A, Kuffner M, Kidd P, Vangronsveld J, Wenzel WW, Fallmann K, Puschenreiter M (2013) The role of plant-associated bacteria in the mobilization and phyto-extraction of trace elements in contaminated soils. Soil Biol Biochem 60:182–194
Shaharokhi S, Bonjar S, Saadoun GHI (2005) Biological control of potato isolates of Rhizoctonia solani by Streptomyces olivaceus strain 115. Biotechnology 4:132–138
Shutsrirung A, Chromkaew Y, Pathom-Aree W, Choonluchanon S, Boonkerd N (2013) Diversity of endophytic actinomycetes in mandarin grown in northern Thailand, their phytohormone production potential and plant growth promoting activity. Soil Sci Plant Nutr 59:322–330
Siddikee MA, Chauhan PS, Anandham R, Han GH, Sa T (2010) Isolation, characterization, and use for plant growth-promotion under salt stress, of ACC deaminase-producing halotolerant bacteria derived from coastal soil. J Microbiol Biotechnol 20:1577–1584
Soe KM, Yamakawa T (2013) Evaluation of effective Myanmar Bradyrhizobium strains isolated from Myanmar soybean and effects of co-inoculation with Streptomyces griseoflavus P4 for nitrogen fixation. Soil Sci Plant Nutr 59:361–370
Solans M (2007) Discaria trinervis-Frankia symbiosis promotion by saprophytic actinomycetes. J Basic Microbiol 47:243–250
Solans M, Vobis G (2013) Biology of actinomycetes in the rhizosphere of nitrogen-fixing plants. In: Amoroso MJ, Benimeli CS, Cuozzo SA (eds) Actinobacteria application in bioremediation and production of industrial enzymes. CRC Press, Boca Raton, pp 1–25
Solans M, Vobis G, Wall LG (2009) Saprophytic actinomycetes promote nodulation in Medicago sativa–Sinorhizobium meliloti symbiosis in the presence of high N. J Plant Growth Regul 28:106–114
Solans M, Ruíz OA, Wall LG (2015) Effect of actinobacteria on Lotus tenuis–Mesorhizobium loti symbiosis: preliminary study. Symbiosis 65:33–37
Srivastava S, Patel JS, Singh HB, Sinha A, Sarma BK (2015) Streptomyces rochei SM3 induces stress tolerance in chickpea against Sclerotinia sclerotiorum and NaCl. J Phytopathol 163(7–8):583–592
Tahmasebpour B, Samimifar P, Dehnad A, Ebrahimi MA, Khaniki B (2014) Chitinase as the most important secondary metabolites of Streptomyces bacteria. Int J Sch Res Gate 2:306–315
Trivedi P, Pandey A, Sa T (2007) Chromate reducing and plant growth-promoting activities of psychrotrophic Rhodococcus erythropolis MTCC 7905. J Basic Microbiol 47:513–517
Uknes S, Mauch-Mani B, Moyer M, Potter S, Williams S, Dincher S, Ryals J (1992) Acquired resistance in Arabidopsis. Plant Cell 4:645–656
Ul-Hassan A, Wellington EM (2009) Actinobacteria. In: Schaechter M (ed) Encyclopedia of microbiology. Academic Press, New York, pp 26–44
Valdes M, Perez N-O, Los Santos EP, Caballero-Mellado J, Pena-Cabriales JJ, Normand P, Hirsch AM (2005) Non-Frankia actinomycetes isolated from surface-sterilized roots of Casuarina equisetifolia fix nitrogen. Appl Environ Microbiol 71:460–466
Van Loon LC (1984) Regulation of pathogenesis and symptom expression in diseased plants by ethylene. In: Fuchs Y, Chalutz E (eds) Ethylene: biochemical, physiological and applied aspects. Martinus Nijhoff/Dr W. Junk Publishers, The Hague, pp 171–180
Verma JP, Yadav J, Tiwari KN, Kumar A (2013) Effect of indigenous Mesorhizobium spp. and plant growth-promoting rhizobacteria on yields and nutrients uptake of chickpea (Cicer arietinum L.) under sustainable agriculture. Ecol Eng 51:282–286
Vijayabharathi R, Sathya A, Gopalakrishnan S (2016) A Renaissance in plant growth-promoting and biocontrol agents by endophytes. In: Singh DP, Singh HB, Prabha R (eds) Microbial inoculants in sustainable agricultural productivity. Springer, India, pp 37–61
Wang W, Qiu Z, Tan H, Cao L (2014) Siderophore production by actinobacteria. Biometals 27:623–631
Weindling R, Katznelson H, Beale HP (1950) Antibiosis in relation to plant diseases. Ann Rev Microbiol 4:247–260
Wu SC, Cheung KC, Luo YM, Wong MH (2006) Effects of inoculation of plant growth-promoting rhizobacteria on metal uptake by Brassica juncea. Environ Pollut 140:124–135
Yandigeri MS, Meena KK, Singh D, Malviya N, Singh DP, Solanki MK, Yadav AK, Arora DK (2012) Drought-tolerant endophytic actinobacteria promote growth of wheat (Triticum aestivum) under water stress conditions. Plant Growth Regul 68:411–420
Yandigeri MS, Malviya N, Solanki MK, Shrivastava P, Sivakumar G (2015) Chitinolytic Streptomyces vinaceusdrappus S5MW2 isolated from Chilikalake, India enhances plant growth and biocontrol efficacy through chitin supplementation against Rhizoctonia solani. World J Microbiol Biotechnol 31:1217–1225
Zhao J, Xue QH, Wang LN, Duan CM, Xue L, Mao N (2011) Antagonistic effect of multifunctional actinomycete strain Act12 on soil-borne pathogenic fungi and its identification. Chin J Eco-Agric 19(2):394–398
Acknowledgements
This work has been undertaken as part of the CGIAR Research Program on Grain Legumes. ICRISAT is a member of CGIAR Consortium.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declared that they have no competing interest.
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made.
The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder.
To view a copy of this licence, visit https://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
Sathya, A., Vijayabharathi, R. & Gopalakrishnan, S. Plant growth-promoting actinobacteria: a new strategy for enhancing sustainable production and protection of grain legumes. 3 Biotech 7, 102 (2017). https://doi.org/10.1007/s13205-017-0736-3
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s13205-017-0736-3