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Plant Growth-Promoting Bacteria As Inoculants in Agricultural Soils

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Plant Growth-Promoting Bacteria As Inoculants in Agricultural Soils Genetics and Molecular Biology, 38, 4, 401-419 (2015) Copyright © 2015, Sociedade Brasileira de Genética. Printed in Brazil DOI: http://dx.doi.org/10.1590/S1415-475738420150053 Review Article Plant growth-promoting bacteria as inoculants in agricultural soils Rocheli de Souza, Adriana Ambrosini and Luciane M.P. Passaglia Departamento de Genética, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil. Abstract Plant-microbe interactions in the rhizosphere are the determinants of plant health, productivity and soil fertility. Plant growth-promoting bacteria (PGPB) are bacteria that can enhance plant growth and protect plants from disease and abiotic stresses through a wide variety of mechanisms; those that establish close associations with plants, such as the endophytes, could be more successful in plant growth promotion. Several important bacterial characteristics, such as biological nitrogen fixation, phosphate solubilization, ACC deaminase activity, and production of sidero- phores and phytohormones, can be assessed as plant growth promotion (PGP) traits. Bacterial inoculants can con- tribute to increase agronomic efficiency by reducing production costs and environmental pollution, once the use of chemical fertilizers can be reduced or eliminated if the inoculants are efficient. For bacterial inoculants to obtain suc- cess in improving plant growth and productivity, several processes involved can influence the efficiency of inocula- tion, as for example the exudation by plant roots, the bacterial colonization in the roots, and soil health. This review presents an overview of the importance of soil-plant-microbe interactions to the development of efficient inoculants, once PGPB are extensively studied microorganisms, representing a very diverse group of easily accessible benefi- cial bacteria. Keywords: nitrogen fixation, siderophore production, plant-bacteria interaction, inoculant, rhizosphere. Received: February 20, 2015, Accepted: May 22, 2015. Introduction through the modulation of ACC deaminase expression, and The rhizosphere can be defined as the soil region production of phytohormones and siderophores, among where processes mediated by microorganisms are specifi- several others. cally influenced by the root system (Figure 1A). This area Interactions between plants and bacteria occur includes the soil connected to the plant roots and often through symbiotic, endophytic or associative processes extends a few millimeters off the root surface, being an im- with distinct degrees of proximity with the roots and sur- portant environment for the plant and microorganism inter- rounding soil (Figure 1A). Endophytic PGPB are good actions (Lynch, 1990; Gray and Smith, 2005), because inoculant candidates, because they colonize roots and cre- plant roots release a wide range of compounds involved in ate a favorable environment for development and function. attracting organisms which may be beneficial, neutral or Non-symbiotic endophytic relationships occur within the detrimental to plants (Lynch, 1990; Badri and Vivanco, intercellular spaces of plant tissues, which contain high lev- 2009). The plant growth-promoting bacteria (or PGPB) be- els of carbohydrates, amino acids, and inorganic nutrients long to a beneficial and heterogeneous group of microor- (Bacon and Hinton, 2006). ganisms that can be found in the rhizosphere, on the root Agricultural production currently depends on the surface or associated to it, and are capable of enhancing the large-scale use of chemical fertilizers (Wartiainen et al., growth of plants and protecting them from disease and 2008; Adesemoye et al., 2009). These fertilizers have be- abiotic stresses (Dimkpa et al., 2009a; Grover et al., 2011; come essential components of modern agriculture because Glick, 2012). The mechanisms by which PGPB stimulate they provide essential plant nutrients such as nitrogen, plant growth involve the availability of nutrients originat- phosphorus and potassium. However, the overuse of fertil- ing from genetic processes, such as biological nitrogen fix- izers can cause unanticipated environmental impacts (She- ation and phosphate solubilization, stress alleviation noy et al., 2001; Adesemoye et al., 2009). To achieve maximum benefits in terms of fertilizer savings and better Send correspondence to Luciane M.P. Passaglia. Departamento growth, the PGPB-based inoculation technology should be de Genética, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Av. Bento Gonçalves 9500, Caixa Postal 15.053, utilized along with appropriate levels of fertilization. More- 91501-970 Porto Alegre, RS, Brazil. E-mail: over, the use of efficient inoculants can be considered an [email protected]. important strategy for sustainable management and for re- 402 Souza et al. Figure 1 - Rhizosphere/bacteria interactions. A) Different types of association between plant roots and beneficial soil bacteria; B) After colonization or association with roots and/or rhizosphere, bacteria can benefit the plant by (i) tolerance toward abiotic stress through action of ACC deaminase; (ii) de- fense against pathogens by the presence of competitive traits such as siderophore production; (iii) increase of fertility and plant growth through biological nitrogen fixation (BNF), IAA (indole-3-acetic acid) production, and phosphate solubilization around roots. ducing environmental problems by decreasing the use of there is no single mechanism for promoting plant growth. chemical fertilizers (Alves et al., 2004; Adesemoye et al., Studies have been conducted regarding the abilities of vari- 2009; Hungria et al., 2010, 2013). ous bacteria to promote plant growth, among them the The success and efficiency of PGPB as inoculants for endophytic bacteria. Endophytes are conventionally de- agricultural crops are influenced by various factors, among fined as bacteria or fungi that colonize internal plant tis- which the ability of these bacteria to colonize plant roots, sues, can be isolated from the plant after surface disinfec- the exudation by plant roots and the soil health. The root tion and cause no negative effects on plant growth (Gaiero colonization efficiency of PGPB is closely associated with et al., 2013). Many bacteria promote plant growth at vari- microbial competition and survival in the soil, as well as ous stages of the host plant life cycle through different with the modulation of the expression of several genes and mechanisms (Figure 1B). Here we discuss five important cell-cell communication via quorum sensing (Danhorn and mechanisms of PGPB. Fuqua, 2007; Meneses et al., 2011; Alquéres et al., 2013; Beauregard et al., 2013). Plant roots react to different envi- Biological nitrogen fixation ronmental conditions through the secretion of a wide range All organisms require nitrogen (N) to synthesize bio- of compounds which interfere with the plant-bacteria inter- molecules such as proteins and nucleic acids. However, the action, being considered an important factor in the effi- main source of N in nature, the atmospheric nitrogen (N ), ciency of the inoculants (Bais et al., 2006; Cai et al., 2009, 2 is not accessible to most living organisms, including euka- 2012; Carvalhais et al., 2013). Soil health is another impor- ryotes. Biological nitrogen fixation (BNF) is the process re- tant factor that affects the inoculation efficiency, due to sponsible for the reduction of N to ammonia (NH ) several characteristics such as soil type, nutrient pool and 2 3 (Newton, 2000; Franche et al., 2009) and is performed in toxic metal concentrations, soil moisture, microbial diver- diazotrophic microorganisms, particularly bacteria and sity, and soil disturbances caused by management prac- archaea (Dixon and Kahn, 2004). tices. Diazotrophic microorganisms perform BNF through Mechanisms of Plant Growth Promotion nitrogenase, a highly conserved enzyme that comprises two metalloproteins, FeMo-protein and Fe-protein (Dixon and The mechanisms by which bacteria can influence Kahn, 2004). Although there are many morphological, plant growth differ among species and strains, so typically physiological and genetic differences between the diazo- PGPB in agricultural soils 403 trophics, as well as an enormous variability of environ- Burkholderia also includes species that fix N2. B. ments where they can be found, they all contain the enzyme vietnamiensis, a human pathogenic species, was efficient in nitrogenase (Moat and Foster, 1995; Boucher et al., 2003; colonizing rice roots and fixing N2 (Govindarajan et al., Zehr et al., 2003; Dixon and Kahn, 2004). Klebsiella 2008). In addition to Burkholderia, the potential of BNF oxytoca M5a1 was the first diazotrophic bacterium that had and endophytic colonization of bacteria belonging to the the genes involved in the synthesis and functioning of genera Pantoea, Bacillus and Klebsiella was also con- nitrogenase (nif,N2 fixation) identified and characterized. firmed in different maize genotypes (Ikeda et al., 2013). In the genome of this bacterium, 20 nif genes are grouped in Gluconacetobacter diazotrophicus is another well-studied a 24-kb chromosomal region, organized into 8 operons: endophyte (Baldani et al., 1997; Oliveira et al., 2002; nifJ, nifHDKTY, nifENX, nifUSVWZ, nifM, nifF, nifLA, and Muthukumarasamy et al., 2005; Bertalan et al., 2009). In nifBQ (Arnold et al., 1988). The nifD and nifK genes en- conditions of N deficiency, the G. diazotrophicus strain code the FeMo-protein, and nifH encodes the Fe-protein Pal5 isolated
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