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Microbial formulation and growth of cereals, pulses, oilseeds and vegetable crops

Abstract

Effective microbes (EM) are the coexisting naturally occurring useful microbes applied as inoculant to enhance the beneficial microflora of the soil ecosystem to facilitate agricultural production. The participating microbial consortium includes lactic acid and photosynthetic bacteria, actinomycetes, fermenting fungi, and yeast, among others. These microbes are physiologically well-matched and coexist in a provided medium. EM formulation could be applied to a target crop in the most appropriate manner and form, and is easy to handle. It could be applied in several manners, as soil application, foliar application and as seed treatment. Microbial formulation in agricultural practices for enhancing productivity is sustainable and eco-friendly approach. When applied, EM formulations reportedly have positive effect on several crop growth parameters. It enhances the productivity, biomass accumulation, photosynthetic efficiency, and antioxidative response to abiotic stress in rice. EM formulations reportedly augment the trace elements contents, root and shoot weight, nodulation and pod yield in rajmah, while it boosts the root and shoot weight, nodulation and seed yields in bean, and drought and virus tolerance, shoot weight, pod number and biomass in soybean. Reportedly, formulated EM perks up the chlorophyll, N, P, carbohydrate and protein contents in sunflower, whereas it stimulates the root and shoot growth, leaf number, fungal disease resistance in groundnut. It could lead to an improved root growth, plant height, chlorophyll content, pod yield, fungal disease resistance, Cr-resistance and pest resistance in okra. This review compiles and provides critical insight to the effects of EM formulations on various crops, particularly the cereals (rice), pulses (rajmah, bean and soybean), oilseeds (sunflower and groundnut) and vegetable (okra).

Introduction

Healthy soil ecology entails the ability of soil to save the flora against soil-borne pathogenic microbes and parasites. Soil ecosystem balances the relationship between the pathogenic and numerous useful microbes working together in synergy [1]. The obliging saprobic microflora ferments and decomposes the soil organic material and supplement to the nutrient pool for the plants, while additionally augmenting the soil particles helping in its moisture and nutrient holding capacities [1]. Applying animal manures and liquid compost (composed of plant growth constituents and useful microbes) to the soil is a scientific approach towards sustainable farming. It could be used to improve soil quality, promote plant growth and protect the crops from pathogenies [2]. Although an integral component of crop ecosystem, the active soil microbes are little recognised in agricultural management strategies, and their role needs to be augmented further [3].

Continuous and indiscriminate use of chemicals poses a negative impact on soil, environment, and ultimately human health, in the same sequence. Use of chemical fertilisers indiscriminately leads to soil pollution gradually deteriorating the soil fertility. Although productivity increased appreciably to feed the starving population with the onset of green revolution (in early 70s), the use of chemical fertilisers and pesticides glorified then had an obvious long-term adverse effect [4]. Since then, the synthetic chemicals have taken the front seat in current global agriculture. Excess accumulation of such chemicals in crops bioaccumulates and biomagnifies along the food chain thereby adversely affecting human and animal health. Chemical run-offs from agri-systems when flooded further add to the awe. So, concerted scientific investigations to utilize agricultural resources efficiently and enhance productivity through biological means instead of chemicals are underway. Applying organic practices along with effective microbes (EMs) for yield enhancement on a sustainable basis is a promising approach. Nutrients recycling becomes efficient through this by saprobes, and the urgency for chemical fertiliser dwindles [4,5,6].

Using microbes solely or in a consortium could enhance the productivity of most farming systems significantly as the microbes and plants have been evolutionarily interacting in nature [7, 8]. Among various microbial communities active in agricultural faming systems, fungi, bacteria, actinomycetes and yeasts have been recommended as potential EMs [1]. Applying composts and animal manure in an agricultural system along with EMs (as EM formulations) to the soil environment promotes plant growth. As the EMs persist in the soil environment for a long time, their beneficial effects in the growth and development of the crops is manifested better [9, 10].

The sludge and organic wastes treated by the EMs could be applied as biofertilizer, wherein the EM participants as well as the essential nutrients could be healthy inputs for crop growth. The beneficial bacteria and fungi present in the biofertilizers help improve chemical and biological characteristics of the soil thereby ensuring agricultural productivity [11, 12]. In biofertilizer, various microbial communities, viz., fungi, bacteria, actinomycetes and yeasts, are used as inoculant and they majorly promote plant growth through activities like fixing N2, phosphate and potassium solubilisation, exopolysaccharides secretion, biocontrol agent, organic matter decomposition, and siderophores production [3, 13]. The various mechanisms of action performed by the EMs promoting plant growth and development are graphically presented in Fig. 1. Diazotrophs like Rhizobium sp. and Bradyrhizobium sp. are the major N2-fixers [14]. Azospirillum, a free-living N2-fixer reportedly enhances the growth in non-leguminous crops [15]. Pseudomonas putida and Pseudomonas fluorescens are not only good biocontrol agents but also stimulate crop growth through biological N2-fixation and by enticing hormonal secretion for plant growth [16]. Azotobacter and Azospirillum application as EMs reportedly enhance strawberry production [17, 18]. Phosphorus, which is the key nutrient in soil and is present in complex unavailable forms, is made available for the plant through the activity of phosphate solubilising microbes. Han and Lee [19] reported the benefits of phosphate solubilising bacteria Bacillus megaterium and potassium solubilising bacteria Bacillus mucilaginosus in enhanced nutrient uptake by eggplant in nutrient-limited soil. Coinoculating two or more microbes might improve the yield and growth as compared to a single one due to the added benefits of their concerted efforts [19].

Fig. 1
figure1

The various mechanisms of action by EMs for plant growth and development

Photosynthetic and lactic acid bacteria, fermentative fungi, actinomycetes and yeasts or their combinations are a part of a formulated EM [20,21,22]. EMs as environmental probiotics are added to the prebiotic that result in formulated EM. In a formulated EM, the biotic (as environmental probiotic) and abiotic (as the prebiotic) are two important ingredients, wherein the microbes act as a probiotic and the carbon and other nutrient sources act as prebiotics. Kato et al. [20] and Raja and Bharani [22] collected beneficial microbes from nature and formulated the EM using lactic acid bacteria (Lactobacillus plantarum, Lactobacillus casei, Streptoccus lactis), photosynthetic bacteria (Rhodopseudomonas palustris, Rhodobacter sphaeroides), yeasts (Saccharomyces cerevisiae, Candida utilis), actinomycetes (Streptomyces albus, S. griseus), and fungi (Aspergillus oryzae, Mucor hiemalis) [20, 22]. Formulated EM application along with organic fertiliser enhances the growth, nutrient uptake and grain yield of sweet corn as compared to chemical fertilisers [20]. As wood waste residue provides a suitable environment for the EM to thrive, and a high quality compost could be produced, EM formulation could be used in industrial wood waste management [21].

Impact of EMs on various crops

EM formulations are available commercially as well as prepared by researchers themselves for pilot- and field-scale studies. The detail information of some commercially available as well as self-made EM formulations, along with the participating microbes on plant growth promotion is furnished in Table 1.

Table 1 A compilation of various EM formulations and their crop wellbeing benefits

Commercial liquid formulation EM-1 containing lactic acid bacteria (Lactobacillus plantarum), yeast (Candida utilis), and actinomycetes (Streptomyces albus) decomposes fruits and vegetables refuge and the resultant compost performs better in terms of increased leaf surface area, total leaves, total chlorophyll content, shoot length, plant height, branches and foliage count [22]. Another EM formulation composed of Bacillus sp. Pseudomonas aeruginosa, Streptomyces sp. was used in seed treatment of sunflower for improving crop performance, that also help in preventing sunflower from necrosis disease [31]. EM culture consisting of photosynthetic bacteria (Rhodopseudomonas palustris and Rhodobacter sphaeroides), lactic acid bacteria (Lactobacillus plantarum, Lactobacillus casei and Streptococcus lactis), yeasts (Sacharomyces sp.), and actinomycetes (Streptomyces sp.) reportedly produces bioactive substances including enzymes, controls soil-borne diseases and accelerates lignin decomposition in the soil [32]. EMs are mutually compatible, and live for an extended period [33]. EMs could suppress the growth and activity of the indigenous putrefactive microbes that add to malodours in plants [34]. Problems in handling of organic urban waste like bad odour, fly population control and pathogenic microbes’ devaluation in piling of waste could be prevented by applying formulated EMs [34].

EM Application has been successfully tried on vegetable crops in New Zealand and Sri Lanka, herbage grasses in Holland and Austria, and apples in Japan. Bokashi (nutrients and EM-enriched compost) was applied in these studies, that increased the yield over a period of time [35]. As the first solid form of EM formulation for agricultural applications, Bokashi compost was prepared using organic refuge like saw-dust mixed with nitrogen-rich materials like rice husk, corn bran, wheat bran, fish meal and oil cake [36]. Bokashi base material is normally prepared by mixing molasses with water, followed by the addition of EM consortia. The resultant mixture is further mixed with dry ingredients (mixture of rice bran, oil cake, fish meal, etc.). The final mixture is allowed to ferment in airtight container, for 4–5 (in summer) to 7–8 (in winter) days under tropical conditions. After fermentation, a sweet and fermented odour suggests that Bokashi is ready for application. Bokashi reportedly facilitates nutrient release from soil, improves soil carbon mineralisation, and enhances the soil properties. It also increases the photosynthesis and protein activity in crops, increases crop resistance to water stress, facilitates spreading of the roots, and suppresses the pests and plant diseases in agricultural practices [35,36,37].

Liquid EM formulations have been used in agricultural practice extensively. Foliar application of EM formulation was compared with chemical fertilisers on onion, watermelon, garlic and tomato, and the yields were higher in EM application. Foliar application of EMs evades various biotic and abiotic factors and other limitations in soil microenvironment, thereby increasing the yield and quality of crops, fruits and vegetables [24]. Foliar application alongside NPK amendment of soil resulted in 120% grain yield, 217% in nodular number and 167% in nodular biomass, while an additional green manure amendment increased the grain yield by 145% [25]. Compared to the control, foliar spray of EM formulation at 15-d interval for three times gave higher pod yields in okra [38].

Role of EMs in agro-ecosystem

Plant growth by EMs may proceed either through direct or indirect action [39]. Direct action refers to soil amelioration, production of plant growth substances, soil fertility improvement by mobilising soil mineral components, N2-fixation, phosphate and minerals solubilization, phytohormones production, and deamenase activity. The indirect action, on the other hand, refers to the biocontrol activities that inactivate or kill plant pathogens thereby providing a healthy cropping environment.

Plant growth-promoting rhizobacteria (PGPR), plant growth-promoting bacteria (PGPB) and vesicular-arbuscular mycorrhizae (AMF) fungi are various growth promoting microbes (PGPM). PGPR provides a favorable environment for plant–microbe interaction. N2-fixers like Rhizobium, Sinorhizobium, Bradyrhizobium, Azorhizobium, Mesorhizobium, Allorhizobium are potential mutually-benefitting plant growth promoting endosymbionts [39]. Genera like Azospirillum, Enterobacter, Klebsiella and Pseudomonas proficiently colonize root surfaces and fix nitrogen [40]. PGPB like Pseudomonas fluorescens and Bacillus subtilis induce PGPRs to produce plant growth-promoting substances [41]. As a classic case of symbiosis, the amino acids, carbohydrates, active enzymes and organic acids secreted by the plant roots are used by the EMs, and the EMs secrete amino acids, various vitamins, nucleic acids and hormones for the plant in return.

ACC (1-aminocyclopropane-1-carboxylic acid) deaminase producing microbes like actinomycetes would take-up and metabolise ACC to α-ketoglutarate and NH3, thereby decreasing ethylene concentration (excess concentration adversely affects growth) in plant. These actinomycetes individually or as coinoculants reportedly fix N2, solubilize phosphate, and produce siderophore in sugarcane [42]. Soil actinomycetes could produce numerous antibiotics and extracellular enzymes that inhibit plant pathogens. Numerous actinomycetes protect plants against diseases [43]. Soil salinity particularly in coastal belts is a challenge for crop growth and wellbeing [44], and Enterobacter sp. UPMR18 reportedly enables okra plant to withstand salt stress [45]. Okra plant has better germination percentage and higher leaf chlorophyll contents by rhizospheric EM symbionts [42].

Interactive role of participating microbes in a formulated EM

Coexistence of various microbial species is a prerequisite in a formulated EM. Microbial interactions occur through secondary metabolites, siderophores, quorum sensing system, biofilm formation, and cellular transduction signalling [46]. The ultimate interaction unit is the gene expressed in each organism in response to an environmental (biotic or abiotic) stimulus that is responsible for the production of molecules for microbial interactions [46]. The participating microbes in an EM formulation may interact with each other through mutualism, commensalism, and protocooperation. A case example of mutualism is the blue green algae and fungus where they exchange nutrition among one another [46]. The algae get protection from environmental stress by the surrounded fungal hyphae which in turn gets carbon that is fixed by algae (algal photosynthesis). Similarly, a commensalism association is seen in cellulose and lignin degrading fungi to glucose and organic acids that are utilised by bacteria further [47].

Protocooperation is a mutualism in which both the microbial partners benefit from each other without depending on each other for survival [48]. Here, favor is extended by one organism to its associate by providing carbonaceous products. Nutritional association for several vitamins, amino acids and purines is observed between bacteria and fungi in terrestrial ecosystems. Nutritional protocooperation may be formed between various bacteria and fungi in which various vitamins, amino and purine are produced by certain microbes that could be utilised by the partner microbes. Proteous vulgaris and Bacillus polymyxa may form nutritional protocooperation for nicotinic acid and biotin, respectively [49]. While formulating an EM, other various interactions of little relevance are antagonism, competition, parasitism, and predation. The survival of one microbe may be at stake (due to the inhibitory or lytic effect of the other partner) when these microbial associations are negative.

Plant-microbe interaction

Plants constantly interact with an enormous soil microflora (Fig. 2). Ecological interactions like mutualism, commensalism, amensalism, protocooperation and antagonism might contribute to the overall soil health and plant wellbeing [13, 46, 50]. Lichen is an association of green or cyanobacterial algae with fungus (ascomycetes). The alga is saved from environmental stresses by the fungal hyphae, while the fungus obtains nutrients and oxygen from the photosynthetic algae. Similarly, the leguminous plant acquires readily available fixed nitrogen source from Rhizobium, and the Rhizobium is protected by the leguminous plant from environmental stress in return. Frankia (an actinomycete) forms a symbiotic association with Alnus and Casuarina (non-legume plants) supplementing them with the fixed nitrogen and obtains organic nutrients in return. Mycorrhizal fungi associate with the plant roots and obtain carbohydrates, while it increases the surface area for water, N, P and inorganic nutrients to be absorbed by plants in return. Endomycorrhizal symbioses help plant withstand environmental stress and enhance the soil structure by forming hydrostable aggregates [51, 52].

Fig. 2
figure2

Microbe-microbe and plant-microbe interactions for sustainable agriculture

Amensalistic association suppresses the growth of one partner by the other through toxins (like antibiotics) production. Here, a soil pathogenic microbe is inhibited by amensal partner where the later remains unaffected thereby benefitting crop growth. Some amensals also release harmful gases like hydrogen cyanide (HCN), ethylene, methane, nitrite, sulphides and other volatile compounds of sulphur [52]. In agriculture, synergism is seen between VAM fungus-legume plants and Rhizobium. In this association, nitrogen is fixed by Rhizobium for the plants to uptake the fixed nitrogen. Phosphorus uptake by plant is also elevated which results in increased crop yields and improved soil fertility.

Antagonism association is the most common in nature which is governed essentially by antibiotic production. Here, an organism directly or indirectly inhibits the activities of the other, e.g., the soil Bacillus sp., Pseudomonas fluorescens and Streptomyces sp. produce antibacterial and antifungal antibiotics that help suppress various plant pathogens. Thiobacillus sp. reduces the soil pH up to 2.0 thereby restricting the growth of pH-sensitive microbial species. In lichen, the O2 produced by algae prevents anaerobic microbes from colonisation, while the cyanide produced by fungi is toxic to numerous other microbes [13, 46, 50, 52].

Microbial (EM) formulation

Probiotics (EMs)

As mentioned earlier, the EMs predominantly consist of physiologically compatible lactic acid and photosynthetic bacteria, yeasts, fermenting fungi and actinomycetes [10, 53, 54]. Adding photosynthetic bacteria to the soil provides a heathy environment for growth of other EMs. VAM fungi increases the soil phosphate solubility and coexist with the N2-fixing Azotobacter and Rhizobium. Lactic acid bacteria secrete lactic acid that sterilizes the soil, and suppresses the thriving harmful microbes (like Fusarium) and nematodes, and stimulates the decomposition of lignocellulosic organic materials in soil [55]. Bioactive substances like phytohormones and enzymes produced by fungi help promote active cell/root division, while providing useful substrates for EMs, viz., lactic acid bacteria and actinomycetes [56]. Fermenting fungi help decompose organic matters and rapidly producing alcohol, esters and antimicrobial substances that help suppress harmful insects and maggots [57]. Actinomycetes are other critical antimicrobial producers from amino acids secreted by photosynthates that would suppress the harmful soil microbes. Thus, various EM species complement each other and form mutually-beneficial relationships in the soil [57]. EMs enhance the quality of soil profile and thereby facilitate crop growth and development [58].

Prebiotic/carriers for microbial inoculants

Microbial formulation is a carrier-based preparation to provide microbes with better survival for longer duration. Prebiotic carriers provide the desired nutrients to augment the EMs. EMs are formulated with the prebiotic to facilitate storage, commercialisation and easy field application. The affordability and availability are the two significant factors while selecting a carrier.

Few of the desirable characteristics of a quality carrier are lump-free material that is easy to process, moisture absorption capacity, ease of sterilization, cost efficient, plentily available and a good inherent pH buffering capacity. While dry formulations are produced using solid carriers like soil (peat, coal, clay, and inorganics), organic (composts, soybean meal, wheat bran, and sawdust), or inert (vermiculite, perlite, kaolin, bentonite, and silicates) materials, liquid formulations can be prepared using mineral oil, organic oils, oil-in-water suspensions, molasses, humic acid, and landfill leachates [59, 60]. These have been detailed in Table 2.

Table 2 A compilation of possible prebiotics for EM formulation

Solid carrier base

A formulation can be prepared by mixing compatible beneficial microbes with the prebiotic. Microbial viability and shelf-life in formulation are important in formulation. Majority of formulations use charcoal, talc or other inert carrier material. Pseudomonas fluorescens formulation was mixed with talc and 1% carboxymethyl cellulose and used against leaf disease. Alginate-base formulation of Bacillus subtilis and Pseudomonas corrugata was easy to prepare and dry, and could be stored up to 3 years [68].

Compost is a good nutrient natural carrier for the EMs. It is biodegradable and non-polluting, usually processed from abundant natural waste materials. While supporting soil microbes to survive, it also facilitates plant growth. Composting has been established as one of the low-cost alternatives to minimize the volume of solid waste disposed of to the environment [59, 69]. This form of transformation of various organic wastes into compost is safe and economical [70, 71]. By converting the biowastes into composts, the nutrients in the waste can be utilized better creating a zero-waste system [71]. The converted compost would contain a substantial amount of EMs that are helpful for plant growth and yield.

Talc and charcoal based formulations of Bacillus sp. increases the growth of mung bean and rice [72]. Bacillus sp. shows antagonistic effects against various phytopathogens, including Rhizoctonia solani (ITCC-186) and Fusarium oxysporum (ITCC-578). Likewise, alginate-base formulation of Bacillus subtilis and Pseudomonas corrugata (PGPRs) reportedly benefit the crops [68]. A solid base Piriformospora indica (root endophyte) formulation as bioinoculant enhances the growth of Phaseolus vulgaris L. [73]. This solid base formulation also increases the adaptability of Phaseolus vulgaris L. to greenhouse conditions.

Liquid carrier base

The EM could be formulated using aqueous, oil or polymer liquid base. The liquid base contains nutrients, cellular protection and additives to promote survival after seed or soil applications [74]. Such prebiotics in EM formulation are glycerol, vermicompost wash, indole acetic acid, and malic acid. Such a PGPM formulation of Bacillus licheniformis, Bacillus sp., Pseudomonas aeruginosa, Streptomyces fradiae shows good microbial survival even after 120-d storage period [74, 75]. The seed germination and plant height increase by using liquid formulation treatment in sunflower [74, 75].

Means to apply EM formulations

The various ways to apply agricultural EM formulations include applying it directly into the soil (soil application), spraying it on leaves (foliar application), and soaking the seeds in it prior to sowing [58]. Seeds are soaked in 0.1% EM suspension for half an hour (for smaller seeds) or up to 4–6 h (for larger seeds). The seeds are carefully semi-dried before sowing ensuring that they do not clump.

In foliar application, the crops benefit from the EM through the foliage. Foliar spray is effective when applied in the evening or early morning. A dilution of 1:1000 with water is often recommended [58]. Foliar application of EM with soil application of fermented plant extract enhances the yields of cucumber and reduces the instance of pickle worm infection [56]. Foliar application of 0.1% EM improves the quality and enhances the yield of tea (by 25%), cabbage (by 14%), and sugar corn (by 12.5%) [32]. The impact of foliar-applied EM and seed treatment on groundnut, along with 0.1, 0.5 and 1.0% (v/v) EM concentrations foliar application on garlic, onion, tomato and watermelon at one- and two-week intervals are effective [32].

Several soil applications of EM formulations for enhanced growth have been reported. Soil application of EM maintains the photosynthetic efficiency of bean plant 2 weeks longer [26]. Application of compost-based effective microbes (Candida tropicalis, Phanerochaete chrysosporium, Streptomyces globisporous, Lactobacillus sp.) along with chemical fertilizer dosage enhances the carotenoid pigment of calendula and marigold by 46 and 12%, respectively [27]. The specific microbes and their modes of action in plant growth are provided in Table 3 with the impact of rhizosphere-associated EM on plant growth in Table 4. The potential microbial candidates for EM formulation are compiled in Table 5.

Table 3 EMs and their specific roles in plant growth promotion
Table 4 Rhizosphere associated EMs and their impacts on plant growth
Table 5 Various EMs for formulation

Climatic (abiotic) factors and the efficacy of EM formulation

Although EMs are meant to particularly promote plant growth in harsh (drought, salinity, CO2, high/low temperatures) climatic conditions [38], climatic factors could also affect the growth and survival of EMs thereby affecting plant growth and productivity [81].

There was an improved interaction between legume and rhizobia at elevated ambient CO2 concentration [82]. Atmospheric CO2 fortification facilitates the activity of Rhizobium leguminosarum over other strains [83]. The nitrogen content of plant tissues in common bean decreases at elevated atmospheric CO2 condition [84]. Elevated CO2 stimulates microbial growth in rhizosphere wherein the plant and rhizobia compete for nitrogen which leads to a low N-nutritional status in plant. The population of HCN-producing Pseudomonas sp. (inhibiting root parasitic fungi) is reduced at an elevated CO2 conditions, and the fractions of siderophore-producing and nitrate-dissimilating strains decrease. A study confirmed the dominance of Pseudomonas sp. in rye, and Rhizobium sp. in white clover at elevated CO2 concentration [85]. Pseudomonas mendocina enhances lettuce growth at elevated CO2 condition [86]. At elevated CO2 condition, the plant biomass, foliar K concentration and water content increase.

Temperature variation could affect microbial activity for plant growth. Decreased temperature may enhance the activity of certain PGPM, while it may be the reverse in some other cases. The root and shoot significantly increase with the activity of Mycobacterium sp., Pseudomonas fluorescens and Pantoea agglomerans at 16 °C in winter wheat crop in loamy-sandy soil as compared to at 26 °C [87]. The rhizobia isolated from nodules of woody legume Prosopis glandulosa shows improved growth at 36 °C than 26 °C [88]. Bacteria colonising at various sites may respond differently to varying temperature, e.g., an endophyte Burkholderia phytofirmans reduces colonisation in tomato rhizosphere when the temperature increases from 10 to 30 °C while the endophytic colonisation remains unaffected [89].

Various reports on the effect of drought on the efficacy of effective microbes are available. Azospirillum strains improve the plant-water interaction. Azospirillum application increases wheat, maize and sorghum yields in water-limiting conditions. Pseudomonas putida or Bacillus megaterium and AM fungi (Glomus coronatum, Glomus constrictumor and Glomus claroideum) association induce development and drought forbearance in plants [90].

Recombinant DNA technology application has been a successful approach to improve microbial property which in turn stimulates the plant to withstand drought [91]. Trehalose-producing microbes pose the ability to support and promote plant growth under drought stress. There are numerous microbial types that stimulate and promote plant growth under drought stress and these include Burkholderia phytofirmans, Paenibacillus polymyxa, and Actinobacteria [81]. PGPB may stimulate cell division of root and root hairs that eventually help plant to take-up water from deeper soil layer [92]. PGPB may support plant growth under drought situation by regulating abscisic acid and ethylene production [93].

Effect of EMs on crops

There are several reports of beneficial effects of EMs on crops. This review discusses the effect of EM formulations particularly on cereals, pulses, oilseeds, and vegetable crops. The rationale behind these selected groups of crops is based on the economic value and their popularity among the Indian farming community. EM formulations and their effect on crops are shown in Table 6.

Table 6 EM formulations and their effect on crops

Cereals

Rice (Oryza sativa) is the staple cereal crop in India, and is a principal food for the half of the world’s population. Approximately 480 MMT milled rice are produced annually to feed the increasing global population. Flooding is the conventional approach for rice cropping which means that there is a need for a huge quantity of water. Yet, around 50% of the rice cultivated area worldwide suffers from drought. Water deficit impacts the crops negatively and might result in a significant yield reduction, especially during critical stages of crop growth [104, 105].

Drought stress affects the crop yield significantly as the nutrient uptake by plants decreases. Thus, attempts to engineer draught-tolerant crops requiring less water while maintaining or enhancing the production are being made. Genetically variant drought tolerant variety could have enhanced proline and abscisic acid production, stabilized superoxide dismutase activity for photosynthesis and improved root system [106]. Using a consortium of advantageous microbes is a prospect towards enhancing drought-resistant plant. Soil microbes like AMF attached to plant roots interact with specific microbial communities to develop an array of activities to enhance crop growth and yield under drought stress conditions [107].

Rice readily forms mycorrhizal associations in upland conditions. However, this is uncommon in flooded conditions as the anoxic condition develops at plant-soil interface. To encourage arbuscular mycorrhiza (AM) symbiosis, aerobic non-flooded farming conditions to boost establishment of AM fungi in the rice roots may be resorted [108]. AMF stimulate the metabolic response in plant under drought stress [109]. AMF Glomus intraradices enhances rice growth under drought condition where the shoot weight increases by 50% with AM symbiosis compared to the non-AM plants [94]. The photosynthesis increases by 40% along with the accumulation of antioxidant molecule glutathione. AM symbiosis reduces hydrogen peroxide and decreases oxidative damage to the lipids [94, 110]. Positive association in Pseudomonas putida or Bacillus megaterium and AM fungi (Glomus coronatum, Glomus constrictum or Glomus claroideum) in drought situations positively affect crop development and drought forbearance [90]. PGPR like Azospirillum brasilense, Phyllobacterium brassicacearum and AM fungi increases crop survival in drought and nutrient limitation like situations. Biomass growth and grain yield increase in rice by applying these microbial formulations [95, 111].

Pulses

Majority of the global population depend on pulses for the major amount of their protein requirements. Pulses primarily include chickpea, rajmah, black gram, green gram, beans and lentil. Of these, black gram is a major food crop in India [41]. Green gram (Vigna radiata) and black gram (Vigna mungo) grown under tropical and subtropical conditions are important food legume as protein source. As these are almost free from gassiness causing factors, green gram and black gram seeds are preferred to feed babies.

India is on the way to develop alternative agricultural practices to obtain higher pulses yield to fulfil the need of its larger population. EM formulation enhances crop growth and yield in both leguminous and non-leguminous pulses. Pseudomonas lurida-NPRp15 and Psedomonas putida-PGRs4 either individually or in combination with Rhizobium leguminosarum-FB1 are effective in growing rajmah [96]. While individual inoculant increases plant dry biomass, nitrogen, phosphorus, potassium, zinc and iron contents, Pseudomonas lurida NPRp15 and Rhizobium leguminosarum FB1 (or Pseudomonas putida PGRs4, Pseudomonas lurida NPRp15 and Rhizobium leguminosarum FB1) combination enhance the root and shoot dry weight, nutrient uptake, nutrient content, nodulation and pod yield in rajmah [96]. The EM of Rhizobium, phosphate-solubilising Bacillus megaterium (M-3) and N2-fixing Bacillus subtilis (OSU-142) has also been encouraging on bean plant. These are effective in nutrient uptake, nodulation, shoot and root dry weight, seed yield and plant growth. These are equally more effective as compared to chemical fertiliser as well [97].

Oilseeds

Sunflower (Helianthus annuus) is an important oilseed crop and is the second most important source of global vegetable oil. India ranks 4th by area and 8th in production of sunflower. Karnataka, Andhra Pradesh and Maharashtra are the major sunflower growers contributing about 91% of the total sunflower cultivation area and 82% of total sunflower production [112]. Wheat bran compost containing Rhizobium sp. and Trichoderma hamatum, either individually or in combination, shows an increase in total chlorophyll, root and shoot lengths, minerals (nitrogen and phosphorus), carbohydrate and protein contents in sunflower [98]. Applying symbiotic nitrogen-fixer Bradyrhizobium japonium (strain TAL-102) EM as biofertilizer or in combination with farm (or green) manure in soybean has positive benefit. Coinoculating Bradyrhizobium japonicum and biofertilizer with farmyard manure exhibits the highest biomass of the shoot, number and biomass of pods compared to other treatments [113]. EM formulation of Azospirillum brasilense and Pseudomonas fluorescens individually or mixed has been applied on groundnut plant through seed treatment, soil application, seedling root tip and foliar spray [99]. Azospirillum brasilense enhances tap root growth, whereas Pseudomonas fluorescens is effective in lateral root growth. A consortium mix enhances leaf numbers and shoot growth. Out of all treatments, soil application is the most effective [99].

Drought tolerance of oilseed plant could increase by applying suitable microbial formulation. Sunflower seeds treated with Pseudomonas putida could withstand drought [31]. Besides drought tolerance, EM is effective against plant pathogens in sunflower. Applying Trichoderma hazianum suspension on sunflower crop prevents it from Plasmopora halstedii (downy mildew). Seed treatment of sunflower with mixed consortium of Bacillus sp., Pseudomonas aeruginosa and Streptomyces sp. is fruitful against sunflower necrosis viral disease [31]. EM formulation increases disease resistance in groundnut; actinomycetes could prevent stem rot disease (by Sclerotium rolfsii) [100]. Actinomycetes inhibit Sclerotium rolfsii by producing various antibiotics/chemical agents, viz., hydrogen cyanide, lipase, siderophores and indole acetic acid [100].

Vegetable plant

Okra (Abelmoschus esculentus) is grown throughout the tropical and warm temperate regions for its fibrous pods eaten as a vegetable. It is attacked by numerous insect pests. Various insect pest’s infestation that decrease the pod yield in okra include fruit borers, shoot borers, leaf hoppers, sucking insects, chewing insects, aphids, root feeding insects, and mites. They suck the cell sap of the plant thereby destroying the plant vigor. The crop is tolerant to the most of the insect pests in wet season, while leaf hoppers and aphids may cause damage during dry season [114]. Although chemical control of the pests is generally practiced for higher yield, use of chemicals alone is not advisable due to shorter interval in the periodical harvest. Thus, it becomes relevant to look for effective and eco-friendly alternatives.

Wokozim, kissan supreme tonic (KST) and EM formulation (foliar) applications in okra for pest control show that KST application is the most effective against sucking pest complex and pod borers resulting in the increase in pod yield. It has been shown that although EM application results in low pod yield as compared to KST and Wokozim but it results in higher final yield (8431 kg ha− 1) as compared to 8012 kg ha− 1 in control [38]. Siddiqui et al. [101] suggested that Trichoderma-enriched compost was more eco-friendly as against inorganic fertilisers, and enhanced crop yield by benefitting okra cultivation. EM formulation of Enterobacter sp. UPMR18 enhances the salt tolerance property of okra; while enhancing salt tolerance it also enhances its germination percentage as well as chlorophyll content [45].

Strains of Pseudomonas aeruginosa alone or with Trichoderma viride (entophytic bacteria) exhibit substantially enhanced disease resistance in okra against Fusarium oxysporum, Fusarium solani, Macrophomina phaseolina, Rhizoctonia solani and Meloidogyne javanica (the root knot nematode). It brings positive impact on plant growth by improving plant height, fresh shoot weight and root length [102]. Brucella K12 strain, a Cr(VI) reducing bacterium, reportedly enhances the growth/yield of okra in Cr-contaminated soils [103].

Conclusions

EMs enhance plant growth and productivity by fixing atmospheric N2 and supplementing the plants with the fixed nitrogen as ammonia. Additionally, the release of trace elements, secreted antioxidant, exopolysaccharides, bioactive compounds (vitamins, hormones and enzymes) by the EMs stimulate plant growth and productivity. Biocontrol agents secreted by the EMs protect the plants from harmful microbes as also from environmental stress. EMs contain primarily the photosynthetic and lactic acid bacteria, fermentative fungi, yeasts, actinomycetes, among others and could be formulated by adding a solid or a liquid carrier to it. The resulting EM formulation could be applied to the soil by spraying on leaves (foliar application), soaking seeds in it (seed treatment) and through irrigation (fertigation/soil application). The review discusses the impact of various EM formulations on cereals, pulses, oilseed and vegetable plants. Application of EM formulation improves grain productivity, biomass accumulation, photosynthesis efficiency and drought tolerance in cereals. It increases the trace elements, biomass, shoot weight, root weight, modulation, pod production in rajmah, and nodulation, root-shoot weight and seed yield in bean. It increases shoot weight, pod number and biomass in soybean. EM formulation positively affects root-shoot growth, chlorophyll, nitrogen, phosphorus, carbohydrate and protein content, drought tolerance, virus resistance, leaf number and fungal disease resistance in sunflower and groundnut. In vegetable plants like okra, EM formulation improves the shoot-root growth, plant height, chlorophyll content, pod yield, fungal disease resistance, Cr-resistance and insect pest resistance. Thus, for sustainable and more promising green agriculture, microbial formulations have an important and indispensable role to play in modern agriculture for cropping of cereals, pulses, oilseeds and vegetables.

Availability of data and materials

The datasets presented and analysed in this review are submitted together with the manuscript. Such datasets are available from corresponding author on reasonable request.

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Acknowledgements

The cooperation, encouragement and infrastructure extended by the affiliated Institute is duly acknowledged and appreciated.

Funding

The funding source for this project work was supported by Rajiv Gandhi National Fellowship scheme from the University Grants Commission (UGC), Government of India.

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KN and HS prepared the primary manuscript. PKS and AC helped in providing results, information and preparation of tables and figures. SM conceptualised, revised, corrected and edited the manuscript. All the authors have read and approve the final manuscript. KN and HS contributed equally as first authors.

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Correspondence to Snehasish Mishra.

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Naik, K., Mishra, S., Srichandan, H. et al. Microbial formulation and growth of cereals, pulses, oilseeds and vegetable crops. Sustain Environ Res 30, 10 (2020). https://doi.org/10.1186/s42834-020-00051-x

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Keywords

  • Agriculture
  • Effective microbe
  • EM formulation
  • Environmental probiotics
  • Microbe-microbe interaction
  • Plant-microbe interaction