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Santos et al. AMB Expr (2019) 9:205 https://doi.org/10.1186/s13568-019-0932-0 MINI-REVIEW Open Access Microbial inoculants: reviewing the past, discussing the present and previewing an outstanding future for the use of benefcial bacteria in agriculture Mariana Sanches Santos1,2, Marco Antonio Nogueira1 and Mariangela Hungria1,2* Abstract More than one hundred years have passed since the development of the frst microbial inoculant for plants. Nowa- days, the use of microbial inoculants in agriculture is spread worldwide for diferent crops and carrying diferent microorganisms. In the last decades, impressive progress has been achieved in the production, commercialization and use of inoculants. Nowadays, farmers are more receptive to the use of inoculants mainly because high-quality products and multi-purpose elite strains are available at the market, improving yields at low cost in comparison to chemical fertilizers. In the context of a more sustainable agriculture, microbial inoculants also help to mitigate envi- ronmental impacts caused by agrochemicals. Challenges rely on the production of microbial inoculants for a broader range of crops, and the expansion of the inoculated area worldwide, in addition to the search for innovative microbial solutions in areas subjected to increasing episodes of environmental stresses. In this review, we explore the world market for inoculants, showing which bacteria are prominent as inoculants in diferent countries, and we discuss the main research strategies that might contribute to improve the use of microbial inoculants in agriculture. Keywords: Biological nitrogen fxation, Plant-growth-promoting bacteria, Azospirillum, PGPB, PGPR, Inoculation, Rhizobia, Chemical fertilizers Introduction increase, the concepts of agriculture sustainability, recov- Humanity has always been concerned about food pro- ery of degraded areas, and mitigation of environmental duction to attend the increasing population and, for a impacts are gaining more respect (Canfeld et al. 2010; long time, the solution was to expand agriculture to new Godfray et al. 2010). In this context, microbial inocu- areas. However, this scenario has changed in recent dec- lants—denominated as biofertilizers in some countries— ades, frst due to limitations of unexplored cultivable have received increasing attention, gaining prominence land, but also reinforced by the development of new tech- and market scale in agriculture. nologies that allow higher yields, in addition to increasing Inoculants are products that have in their composi- environmental concerns, leading to agricultural prac- tion living microorganisms capable of benefting the tices aiming at achieving sustainable production. Tere- development of diferent plant species. Te most antique fore, although the global demand for food continues to microorganisms used as inoculants are the “rhizobia”, diazotrophic bacteria able to colonize the rhizosphere and establish nodules in the roots of their host plants, *Correspondence: [email protected]; biotecnologia. composed by several species of the Fabaceae family. [email protected] 1 Embrapa Soja, Cx. Postal 231, Londrina, Paraná 86001-970, Brazil Te symbiosis legumes-rhizobia leads to the process Full list of author information is available at the end of the article of biological nitrogen fxation (BNF), which very often © The Author(s) 2019. 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 http://creat iveco mmons .org/licen ses/by/4.0/. Santos et al. AMB Expr (2019) 9:205 Page 2 of 22 can fully supply the plant´s demands on N. Moreo- (Fig. 1). Other top countries in the use of inoculants are ver, other diazotrophic bacteria, such as Azospirillum, Argentina and India (Mazid and Khan 2014; Hungria and establish less straight relationships with the host plant, Mendes 2015; Okon et al. 2015; Sruthilaxmi and Babu but are also able to supply, at least partially, the plant’s 2017). demands on N. Both Azospirillum and rhizobia, among However, there are limiting factors that restrict the use other diazotrophic and non-diazotrophic bacteria are of inoculants in some areas. Biotic and abiotic stresses named as plant-growth-promoting bacteria (PGPB) or may afect the efectiveness of the product, making them plant-growth-promoting rhizobacteria (PGPR), as they inefcient in cases such as nutrient-poor or unbalanced may beneft the plants by a variety of single or combined soils, salinity, water stress, increasing temperatures, pests processes, including the production of phytohormones, and diseases, among others (Bashan et al. 2014; Das et al. siderophores, phosphate solubilization, induction of 2017; Khan et al. 2017; Tilakarathna and Raizada 2017; plant intrinsic systemic resistance to abiotic and biotic Samago et al. 2018). To circumvent these factors, several stresses, among others (Bhattacharyya and Jha 2012; studies have been addressed to gain better knowledge on Malusá and Vassilev 2014; Fukami et al. 2017, 2018a, b). the intrinsic properties of PGPB, seeking at understand- Other microorganisms have also been increasingly used ing their optimum growth conditions and interaction in agriculture for biological control of pests and diseases with the host plants (Flores-Félix et al. 2018; Goulart- (Ciancio et al. 2016; Berg et al. 2017; Singh et al. 2017; Machado et al. 2018; Jiménez-Gómez et al. 2018). Eforts Xiang et al. 2017), but this review will only deal with have also been applied to improve the efciency of micro- inoculants carrying strains that facilitate plant growth. organisms already available and in the identifcation of Moreover, we will name all rhizobia and other bacte- new elite strains to be used as inoculants under unfavora- ria carrying diferent mechanisms that promote plant ble and stressful environmental conditions, such as areas growth as PGPB. frequently experiencing drought, soils with low nutrient Currently, soybean (Glycine max (L.) Merr.) is the availability or with salinity, among others (Benidire et al. most inoculant-consuming crop worldwide, carrying 2017; Koskey et al. 2017; Youseif et al. 2017). Tere is an bacteria belonging to the genus Bradyrhizobium. Bra- increasing number of studies aiming to isolate, identify zil is probably the global leader in the use of inoculants and evaluate the capacity of plant-growth promotion of for the soybean crop (Hungria and Mendes 2015; Okon bacteria with a variety of plant species, with potential to et al. 2015; ANPII 2016) where approximately 78% of be transformed into new microbial inoculants in a near the copping area—nowadays 36.5 million hectares—is future (Yanni et al. 2016; Koskey et al. 2017; Manasa et al. inoculated yearly (ANPII 2018). Additionally, inocula- 2017; Muleta et al. 2017). tion of common beans (Phaseolus vulgaris L.), cowpea Another technology with increasing application relies (Vigna unguiculata (L.) Walp.), maize (Zea mays L.) on the use of mixed inoculants, aiming to promote plant and co-inoculation of soybean and common bean with growth by combining distinct mechanisms of diferent rhizobia and Azospirillum have also increased in Brazil microorganisms. Mixed inoculants can provide excellent (Hungria et al. 2010, 2015), so that the number of doses results and show the great potential of being increasingly commercialized in the last years has impressively grown used by the farmers (Juge et al. 2012; Hungria et al. 2013, 2015; Chibeba et al. 2015; Bulegon et al. 2017; Ferri et al. 2017). Te objective of this short review is to explore the cur- rent market of inoculants, highlighting what has been produced and marketed lately in several countries, and the impact on agricultural sustainability. We also explore new ideas, new objectives and new strategies that are needed to generate information for the development of new products, breaking down barriers needed to expand the use of microbial inoculants in agriculture. Inoculant carriers Since the beginning of the manufacturing of inocu- lants, the industry has been concerned about generat- Fig. 1 Market of microbial inoculants in Brazil in the last 15 years ing increasingly efcient products, at a low cost, whose (million doses) handling attends to the needs and the quality required Santos et al. AMB Expr (2019) 9:205 Page 3 of 22 by farmers. An important aspect is the choice of the car- based on liquid formulations began to gain space, espe- rier for the microorganisms, which should, among other cially from the late 1990s onwards. In Brazil, the frst things, provide long cellular viability and be of easy appli- liquid inoculant was approved by the Ministry of Agri- cation. In 1896, in the USA, the frst inoculant commer- culture for commercial used in 2000, and a decade later cially produced, “Nitragin” (Fig. 2), used gelatin, and later, almost 80% of the inoculants sold in the country were in nutrient medium was employed as carrier for bacterial liquid formulations (Fig. 2); similar proportion is found cells. Due to the high mortality rate, these carriers were in Argentina (ANPII 2018). Liquid inoculants consist of soon replaced by peat, which remained as the “gold” car- microbial cultures suspended in liquid medium rich in rier until the end of the 1990s, when the scenario began nutrients and cell protectors. Tey are easily handled and to change (Fig. 2) (Williams 1984). compatible with mechanized sowing, ofering an advan- Peat is a solid material, consisting of organic soil natu- tage over solid inoculants at sowing.

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