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Plant Growth-Promoting Actinobacteria: a New Strategy for Enhancing Sustainable Production and Protection of Grain Legumes

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Plant Growth-Promoting Actinobacteria: a New Strategy for Enhancing Sustainable Production and Protection of Grain Legumes 3 Biotech (2017) 7:102 DOI 10.1007/s13205-017-0736-3 REVIEW ARTICLE Plant growth-promoting actinobacteria: a new strategy for enhancing sustainable production and protection of grain legumes 1 1 1 Arumugam Sathya • Rajendran Vijayabharathi • Subramaniam Gopalakrishnan Received: 2 November 2016 / Accepted: 19 April 2017 Ó Springer-Verlag Berlin Heidelberg 2017 Abstract Grain legumes are a cost-effective alternative for Introduction the animal protein in improving the diets of the poor in South-East Asia and Africa. Legumes, through symbiotic Grain legumes also called ‘Poor man’s meat’ are an nitrogen fixation, meet a major part of their own N demand essential entity in food and feed due to its protein, minerals, and partially benefit the following crops of the system by and other bioactive molecules. Increasing nutritional enriching soil. In realization of this sustainability advan- awareness increased the per-capita consumption of grain tage and to promote pulse production, United Nations had legumes across the world (Amarowicz and Pegg 2008). declared 2016 as the ‘‘International Year of pulses’’. Grain The symbiotic association of leguminous crops with rhi- legumes are frequently subjected to both abiotic and biotic zobia contributes 65% of nitrogen (N) needs. Their better stresses resulting in severe yield losses. Global yields of adaptation as an inter-crop with cereals or tuber crops helps legumes have been stagnant for the past five decades in in increased income generation and livelihood resilience of spite of adopting various conventional and molecular small holder farmers. However, production level of such breeding approaches. Furthermore, the increasing costs and leguminous crops has constraints in various forms such as negative effects of pesticides and fertilizers for crop pro- pest and pathogen attacks, infertile soils, and climate duction necessitate the use of biological options of crop changes. Development of improved cultivars through production and protection. The use of plant growth-pro- breeding and molecular techniques had been practiced; moting (PGP) bacteria for improving soil and plant health still, the productivity remains stagnant for the last two has become one of the attractive strategies for developing decades. All these together attracted the attention at global sustainable agricultural systems due to their eco-friendli- level, and thus, the general assembly of United Nations has ness, low production cost and minimizing consumption of announced this year as ‘International Year of Pulses (2016 non-renewable resources. This review emphasizes on how IYOP)’ to emphasize the need for focusing on pulses for the PGP actinobacteria and their metabolites can be used food and nutritional security and to create awareness and effectively in enhancing the yield and controlling the pests understanding of the challenges faced in pulse farming and and pathogens of grain legumes. trading (FAO 2014). A cleaner and greener approach towards the improve- Keywords Plant growth-promoting actinobacteria Á ment of leguminous crop production is the use of a cate- Legumes Á Metabolites Á Biocontrol Á Stress control gory 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 avail- & Subramaniam Gopalakrishnan ability of soil nutrients, supplying phytohormones, and [email protected] inducing systemic resistance against phytopathogens. There are voluminous data available on PGPR, but most of 1 International Crops Research Institute for the Semi-Arid Tropics (ICRISAT), Patancheru, Hyderabad, Telangana it belongs to the phylum Bacteroidetes, Firmicutes, and 502324, India Proteobacteria, of which the most commonly studied are 123 102 Page 2 of 10 3 Biotech (2017) 7:102 Azospirillum, Azotobacter, Bacillus, Pseudomonas, Glu- minimizing the deleterious effects of external stresses of conacetobacter, Enterobacter, Serratia, Paenibacillus, and either biotic or abiotic sources through the following Rhizobium (Bhattacharyya and Jha 2012). However, the modes: competition for nutrients, production of low reports on the plant growth-promoting (PGP) traits of molecular inhibitory substances such as ammonia, cyano- bacteria belonging to the phylum Actinobacteria are lim- gens, alcohols, aldehydes, sulfides, and ketones, cell-wall ited, despite its ubiquitous existence in bulk soil, rhizo- degrading enzymes, and secondary metabolites with bio- spheric soil, and plant tissues and their usefulness in cidal properties, in which the latter, two are the key phe- agriculture (Bhattacharyya and Jha 2012; Jog et al. 2012). nomenon deployed by the actinobacterial community (El- Hence, this review emphasizes to document mainly on PGP Tarabily and Sivasithamparam 2006; Glick 2012; Bouiz- traits of actinobacteria and how far it was studied in the garne 2013; Dey et al. 2014). context of growth-promotion, biocontrol against pests, and pathogens, as mitigators of abiotic stress, as a tool for Nitrogen fixation enhanced phytoremediation and bio-fortification. Nitrogen is the major essential crop nutrient available through the process called symbiotic N fixation. This was Actinobacteria diversity aided by the relationship between the members of the family Rhizobiaceae, Bradirhizobiaceae, and Phyllobacte- The bacteria belong to the phylum Actinobacteria are riaceae with the leguminous plants through the formation Gram-positive filamentous bacteria, with 6 classes, 25 of N-fixing specialized structure called nodules (Schultze orders, 52 families, and 232 genera and represent one of the and Kondorosi 1998). Frankia, a versatile N fixing acti- largest taxonomic units among the 18 major lineages cur- nobacteria, fixes N in non-legumes under both symbiotic rently recognized within the domain Bacteria (Stacke- and free-living conditions. It infects the root cells of acti- brandt and Schumann 2000). They can thrive in either bulk norhizal plants through either intracellular root-hair infec- soil or rhizospheric soil, and due to spore forming char- tion or intercellular root invasion (Benson and Silvester acteristics, they can remain dormant in agricultural soil for 1993). Besides this, several other endophytic actinobacteria a longer period. The actinobacteria population increases exhibited N-fixing ability which includes Arthrobacter, with the soil depth up to horizon ‘C’. It is estimated that Agromyces, Corynebacterium, Mycobacterium, Mi- actinobacteria are distributed with average 104–106 cromonospora, Propionibacteria, and Streptomyces (Sell- spores g-1 soil in various crops fields (Shaharokhi et al. stedt and Richau 2013). This was demonstrated long back 2005; Ul-Hassan and Wellington 2009). Though they are by Fedorov and Kalininskaya (1961) by their ability to mesophilic organisms, species of the family such as grow on N-free medium and acetylene reduction activity. Thermoactinomycetaceae are commonly found in compost Recent studies using 15N isotope dilution analysis and and manures at thermophilic growing temperature (Ul- identification of nif genes further support this phenomenon Hassan and Wellington 2009). They also stay as either (Valdes et al. 2005; Ghodhbane-Gtari et al. 2010). epiphyte or endophyte in plant tissues of wide host range Molecular studies have established the fact that many including barley, wheat, rice, soybean, cowpea, chickpea, actinobacteria can occur as endophytes in various legumi- banana, tomato, and medicinal plants. Among them, nous and non-leguminous plants without forming nodule. Streptomyces is the predominant genus followed by Acti- This is supported by the existence of nif sequence homol- nomadura, Microbispora, Micromonospora, Nocardia, ogy in both Rhizobium and Frankia, the absence of nod Nonomurea, Mycobacterium, Frankia, Actinoplanes, Sac- genes in the latter (Ceremonie et al. 1999). Even under field charopolyspora, and Verrucosispora (Martinez-Hidalgo conditions, enhanced nodulation of chickpea and soil N et al. 2014; Vijayabharathi et al. 2016). content observed upon the application of Streptomyces inoculants indicates their promotional effect and influence of rhizobia-legume symbiosis in a non-specific manner PGP traits of actinobacteria (Gopalakrishnan et al. 2015a, b). However, a detailed understanding of the mechanisms on this symbiotic mode As like other PGPR, actinobacteria also employ both direct needs to be established. and in-direct mechanisms to influence the plant growth and protection. The direct mechanisms involve the production Phosphate solubilization of vital factors for crop growth such as growth hormones and the assistive actions on nitrogen fixation, phosphate Influence of PGPR in enabling the availability of phos- solubilization, and iron acquisition. PGP actinobacteria phate to plants through various mechanisms is highlighted indirectly influence the plant growth by controlling and by various researchers across a range of soil conditions. In 123 3 Biotech (2017) 7:102 Page 3 of 10 102 the context of actinobacteria, Arthrobacter, Rhodococcus, Phytohormones Gordonia, Streptomyces,andMicromonospora have been reported for P solubilization in vitro and glass house Phytohormone producing capacity of several rhizospheric conditions (Chen et al. 2006; Hamdali et al. 2008;Jog and endophytic actinobacteria was demonstrated by various et al. 2014). Initial report on P solubilizing capacity of a researchers for indole acetic acid (IAA), cytokinins, and non-streptomycete
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