African Journal of
Agricultural Research

  • Abbreviation: Afr. J. Agric. Res.
  • Language: English
  • ISSN: 1991-637X
  • DOI: 10.5897/AJAR
  • Start Year: 2006
  • Published Articles: 6853

Review

Bioformulations based on plant growth promoting rhizobacteria for sustainable agriculture: Biofertilizer or Biostimulant?

Marcel Yévèdo Adoko
  • Marcel Yévèdo Adoko
  • Laboratoire de Biologie et Typage Moléculaire en Microbiologie, Département de Biochimie et de Biologie Cellulaire, Faculté des Sciences et Technique, Université d'Abomey-Calavi, 05 BP 1604 Cotonou Bénin.
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Nadège Adoukè Agbodjato
  • Nadège Adoukè Agbodjato
  • Laboratoire de Biologie et Typage Moléculaire en Microbiologie, Département de Biochimie et de Biologie Cellulaire, Faculté des Sciences et Technique, Université d'Abomey-Calavi, 05 BP 1604 Cotonou Bénin.
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Agossou Pacôme Noumavo
  • Agossou Pacôme Noumavo
  • Laboratoire de Biologie et Typage Moléculaire en Microbiologie, Département de Biochimie et de Biologie Cellulaire, Faculté des Sciences et Technique, Université d'Abomey-Calavi, 05 BP 1604 Cotonou Bénin. 2Laboratoire de Microbiologie et de Technologie Alimentaire, Faculté des Sciences et Technique, Université d'Abomey-Calavi, 04 BP 1107 Cotonou Bénin.
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Olaréwadjou Amogou
  • Olaréwadjou Amogou
  • Laboratoire de Biologie et Typage Moléculaire en Microbiologie, Département de Biochimie et de Biologie Cellulaire, Faculté des Sciences et Technique, Université d'Abomey-Calavi, 05 BP 1604 Cotonou Bénin.
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Adolphe Adjanohoun
  • Adolphe Adjanohoun
  • Institut National des Recherches Agricoles du Bénin, 01 BP 884 Cotonou Bénin.
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Lamine Baba-Moussa
  • Lamine Baba-Moussa
  • Laboratoire de Biologie et Typage Moléculaire en Microbiologie, Département de Biochimie et de Biologie Cellulaire, Faculté des Sciences et Technique, Université d'Abomey-Calavi, 05 BP 1604 Cotonou Bénin.
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  •  Received: 19 August 2021
  •  Accepted: 23 September 2021
  •  Published: 30 September 2021

 ABSTRACT

Integrated production in sustainable agriculture aims to improve the efficiency of biological inputs through plant-based bioformulations or microorganisms, which are an excellent source of natural fertilisers. A variety of plant stimulants are increasingly used in crop production for environmentally sustainable agriculture. These products have different names and the designations are confusing. The aim of this work is to clarify what is meant by biofertilizer and biostimulant. A biofertilizer is a bacterial or fungal inoculant applied to plants with the aim of increasing the availability of nutrients and their use by plants, regardless of the nutrient content of the inoculant itself. A plant biostimulant is substance or microorganism applied to plants for the purpose of improving the nutritional efficiency, abiotic stress tolerance and/or quality characteristics of crops, regardless of its nutrient content. By extension, plant biostimulants also refer to commercial products containing mixtures of these substances and/or microorganisms. Plant Growth Promoting Rhizobacteria (PGPR) can be called biofertilisers or biostimulants; PGPR formulations are biostimulants. It can be noted that biofertilisers are included in biostimulants.

Key words: Biostimulant, biofertilizer, Plant Growth Promoting Rhizobacteria (PGPR), bioformulation, sustainable agriculture.


 INTRODUCTION

The uncontrolled and excessive use of chemical inputs to increase agricultural productivity is argued by some to be degrading the soil and endangering the ecosystem, which is further argued to pose a serious threat to human health (Nellemann et al., 2009). It is therefore imperative to move towards modern agriculture and to look for new biotechnological advances that allow a reduction in the use of chemical inputs without affecting crop yields and farmers' income (Chbani et al., 2013). Recent efforts have been devoted to the production of high quality, nutrient-rich food in a sustainable manner to ensure biosecurity (Raja, 2013). Consumption of organic food is associated with health beliefs and subjective well-being, leading to increased values and market demand (Apaolaza et al., 2018). Recent studies highlight that organic food has significant human and environmental health benefits (Gomiero, 2018). Moreover, in the coming years, agriculture will be pushed to become more sustainable as a global response to climate change. This significant growth in organic farming is not only due to agricultural change, but also represents the implementation of important changes in society and their relationship with agriculture (Lobley et al., 2009). Nowadays, there are several biological products to manage and improve crops (Benfatto et al., 2015). Among these products, we have biostimulants and biofertilisers. These two terms are often misused. In view of the confusion surrounding biofertilisers and biostimulants, it was necessary to look for objectively available information in the literature to clarify these two concepts. The aim of this review is to clarify the notions of biofertilisers, biostimulants and to find a correct name for Plant Growth Promoting Rhizobacteria (PGPR) and PGPR formulations. This review gives an overview of the definition of the concepts of plant biofertilisers and biostimulants, as well as their mode of action. It will also briefly describe the benefits and some interesting results of biofertilisers and biostimulants and present some biofertilisers and/or biostimulants products currently on the market. At the end, we will clarify the relationship between the two concepts and specify the appropriate name for PGPR and PGPR formulations.


 CONCEPTS CLARIFICATION

Biofertilisers

Definition and modes of action

Biofertilizer can be interpreted in different ways (El-Ghamry et al., 2018). A biofertilizer is a bacterial or fungal inoculant applied to plants with the aim of increasing the availability of nutrients and their utilisation by plants, regardless of the nutrient content of the inoculant itself. Biofertilizer is a substance containing living microorganisms that, when applied to the seed, plant surface or soil, colonise the rhizosphere or plant interior, promoting growth, yield and increasing the supply or availability of primary nutrients to the host plant.

Biofertilizer is a product that is not chemically synthesised, biodegradable and can be used as a fertilisers containing live phosphate solubilising and nitrogen fixing microorganisms PGPR (Roychowdhury et al., 2014). They promote plant growth by increasing nutrient supply (Adjanohoun et al., 2012), increasing the root  biomass   or   root   area    (Vessey,    2003).  Some biofertilisers are able to produce sufficient growth-promoting phytohormones (IAA) and substances that control pathogen proliferation (HCN) (Noumavo et al., 2015). Biofertilisers add nutrients through natural nitrogen fixation processes, solubilising phosphorus and stimulating plant growth through the synthesis of growth-promoting substances (Agbodjato et al., 2018; Nilabja Ghosh, 2007). They provide environmentally friendly organic agricultural inputs and may be more cost-effective than chemical fertilisers, and can associate symbiotically with plant roots. The microorganisms involved can easily and safely convert complex organic materials into simple compounds, so that plants can easily assimilate them.

Benefits and some interesting results

The main role of biofertilisers application is to increase plant growth and yield without deleterious environmental side effects (Mishra et al., 2013). They maintain the natural soil habitat, and stimulate plant growth. Microbial biofertilisers play a crucial role in maintaining soil fertility at the appropriate level and improving soil structure by influencing the aggregation of soil particles (Rashid et al., 2015). They also may contribute to a better plant-water relationship (Xiang et al., 2012), provide protection against drought, make plants less prone to certain soil-borne diseases, mycotoxin-producing fungi (Simarmata et al., 2016) and reduce the incidence of insect pests (Dey et al., 2014). Biofertilisation is a practice to restore the functionality of soils destroyed by chemical inputs. Biofertilisers are most commonly used in maize, wheat, rice, sugarcane and sorghum crops in different soils and regions. Today, their use has been extended to species as different as pine, alfalfa, cactus, lettuce, strawberry, etc. (Singh and Singh, 2018; Mehnaz, 2015). According to a study by Schütz et al. (2018), inoculation with biofertilisers increased average crop yields by 16.2% compared to controls. Similarly, Amogou et al. (2021) obtained increases in height, leaf area, fresh biomass and yield of maize of 27.19, 32.23, 47.89 and 46.98% respectively after the use of microbial biofertilisers combined with 25% of the recommended dose of NPK-Urea in Benin.

Biostimulants

Definition and modes of action

Biostimulants are products, other than fertilisers, that promote plant growth if applied in small quantities (Du Jardin, 2015; Kauffman et al., 2007). They are products that have a stimulating effect on the growth and development of the plant, likely to provoke a defence reaction from  the latter. Other authors consider biostimulants as stimulators of natural defences, and focus only on the phytoprotective aspect of these products (Lambert, 2006). According to Yakhin et al. (2017), a biostimulant is a biologically derived product that improves plant productivity as a result of emergent properties caused by constituent complexes, and not as a sole consequence of the presence of essential nutrients, plant growth regulators or plant protective compounds. Biostimulants can be microorganisms (PGPR, Arbuscular Mycorrhizal Fungi (AMF)), natural or naturally occurring substances (humic acids, amino acids, algae extract, plant extract), and synthetic substances (chitosan) (Katiyar et al., 2015; Hadwiger, 2013). They can be used alone, in the soil or in the growing medium, by spraying on plants or by coating seeds (EBIC, 2014). Biostimulants are products that promote or improve water uptake, nutrient uptake, bioavailability and nutrient assimilation efficiency, tolerance to abiotic stresses, crop quality, crop yield, maintenance of growth and production levels, under optimal conditions, stimulation and fortification of plants (Yakhin et al., 2017; Faessel et al., 2014).

Biostimulants are not considered fertilisers, as such, because they do not provide a sufficient amount of nutrients. Biostimulants are materials, other than fertilisers, that promote plant growth when applied in small quantities (Kauffman et al., 2007). However, they are classified as a fertiliser from a regulatory point of view for marketing.

Benefits and some interesting results

Biostimulants have a very positive impact on the environment and the preservation of resources by promoting a better use of nutrients by plants (EBIC, 2012). They contribute to the reduction of greenhouse gas emissions (through a better use of nitrogen). Biostimulants contribute to the preservation of unrenewable resources through better absorption of certain nutrients. According to Calvo et al. (2014), biostimulants enhance the uptake of water and nutrients from the soil, increase root growth and make plants more resistant to water and heat stress and excessive salinity, all of which reduce the need for pesticides (Childs and Beeson, 2000). The height, stem diameter, leaf area, above-ground biomass and below-ground biomass of maize under the influence of biostimulants were improved by 83.06, 44.57, 102.94, 86.84 and 42.68% respectively, compared to the control under greenhouse conditions (Adoko et al., 2021).

Biofertilisers and/or biostimulants currently on the market

Table 1 gives an overview of some products available on the French market. From Table 1 the biofertilisers and/or biostimulants found on the French market can be grouped into five categories. Biofertilisers and/or biostimulants formulated with a single strain of fungi; a single strain of bacteria; a combination of fungi; a combination of bacteria and a combination of fungi and bacteria (Alabouvette and Cordier, 2018).


 RELATIONSHIP BETWEEN BIOFERTILISERS AND BIOSTIMULANTS

Biostimulants are classified according to the origin and nature of the resources used for their manufacture, their function, their use or the type of effects observed. According to Torre et al. (2016), there are five groups of biostimulants. Humic substances, algae extract, protein and amino acid hydrolysates, inorganic salts and microorganisms (beneficial bacteria and fungi). According to Yakhin et al. (2017), humic substances and PGPR are classified as biofertilisers, phytostimulants and biopesticides. Du Jardin et al. (2015) consider biofertilisers as a subcategory of biostimulants. Algae extracts and microorganisms are considered by other authors as biofertilisers (Torre et al., 2016; Roychowdhury et al., 2014).


 WHAT IS THE CORRECT TERM FOR PGPR AND PGPR FORMULATION?

PGPR are soil microorganisms that naturally stimulate plant growth and yield. They play their roles either by solubilising and assisting in nutrient acquisition or by releasing phytohormones or biocontrol agents to protect the plant from various pathogens (Glick, 2012). The rhizobacteria solubilise metals such as phosphorus (P), zinc (Zn), iron (Fe), potassium (K), into soluble forms that are available to plants. These soluble forms of metals significantly improve plant nutrition and growth (Kamran et al., 2018; Gupta et al., 2015). Also, the phytase produced by some PGPR allows the release of phosphorus associated with organic compounds. In addition, they produce organic acids to reduce metal toxicity (Ahemad, 2015).

There are several categories of PGPR depending on their modes of action. Somers et al. (2004) classified PGPR into four subgroups: biofertilisers (increase in nutrient availability to the plant), phyto-stimulators (increase in plant growth, ability to produce phytohormones), rhizo-remediators (degradation of organic pollutants) and finally biopesticides (control of diseases, production of fungicidal and antibiotic metabolites). Du Jardin et al. (2015) consider all categories of PGPR as biostimulants. PGPR can be called biofertilisers or biostimulants.

In addition to rhizobacteria, PGPR formulations contain binders and other organic and mineral substances. Formulations based on Plant Growth Promoting Rhizobacteria (PGPR) are then called biostimulants.


 CONCLUSION

In recent years there has been an increase in the number of natural products that stimulate plant growth and yield. A biofertilizer is any bacterial or fungal inoculant that increases the availability of nutrients and their use by plants, regardless of its nutrient content. Biofertilisers are microbial biostimulants. Biofertilizer is a product that is not chemically synthesised, biodegradable and can be used as a fertiliser containing living microorganisms. Biostimulants are products, other than fertilisers, that promote plant growth if applied in small quantities. Biostimulants are substances or microorganisms that function to stimulate natural processes to increase nutrient uptake and efficiency, tolerance to abiotic stresses and crop quality independent of nutrient content. Biostimulants are broader than biofertilisers. Biofertilisers are included in biostimulants. They are therefore microbial biostimulants. PGPR can be called biofertilisers or biostimulants; PGPR formulations are biostimulants.


 CONFLICT OF INTERESTS

The authors have not declared any conflict of interests.



 REFERENCES

Adjanohoun A, Noumavo PA, Sikirou R, Allagbé M, Gotoechan-Hodonou H, Dossa KK, Yèhouénou B, Glèlè Kakaï R, Baba-Moussa L. (2012). Effets des rhizobactéries PGPR sur le rendement et les teneurs en macroéléments du maïs sur sol ferrallitique non dégradé au Sud-Bénin. International Journal of Biological and Chemical Sciences 6(1):279-288. 
Crossref

 

Adoko MY, Sina H, Amogou O, Agbodjato NA, Noumavo PA, Aguégué RM Assogba SA, Ahoyo Adjovi N, Dagbénonbakin G, Adjanohoun A, Baba-Moussa L (2021). Potential of Biostimulants Based on PGPR Rhizobacteria Native to Benin's Soils on the Growth and Yield of Maize (Zea mays L.) under Greenhouse Conditions. Open Journal of Soil Science 11(3):177-196.
Crossref

 
 

Agbodjato NA, Amogou O, Noumavo PA, Dagbenonbakin G, Hafiz AS, Kamirou R, Alladé AM, Adebayo O, Baba-Moussa F, Adjanohoun A, Baba-Moussa L (2018). Biofertilising, Plant-Stimulating and Biocontrol Potentials of Isolated PGPR Rhizobacteria in Central and Northern Benin. African Journal of Management Research 12(28):664-672.

 
 

Ahemad M (2015). Phosphate-solubilizing bacteria-assisted phytoremediation of metalliferous soils: a review. Biotechnology 5(2):111-121.
Crossref

 
 

Alabouvette C, Cordier C (2018). Fertilité biologique des sols : des microorganismes utiles à la croissance des plantes. Innovations Agronomiques, INRAE, 2018, 69, ff10.15454/UIJG8Lff. ffhal02058232f

 
 

Amogou O, Noumavo AP, Agbodjato NA, Sina H, Dagbénonbakin G, Adoko MY, Salako VK, Glèlè Kakaï R, Adjanohoun A, Baba-Moussa L (2021). Rhizobacterial inoculation in combination with mineral fertilizer improves maize growth and yield in poor ferruginous soil in center of Benin. BioTechnologia 102(2):141-155. 
Crossref

 
 

Apaolaza V, Hartmann P, D'Souza C, López CM (2018). Eat organic Feel good? The relationship between organic food consumption, health concern and subjective wellbeing. Food Quality and Preference 63:51-62. 
Crossref

 
 

Benfatto D, Matteo R, Di Franco F, San Lio RM, Ugolini L, Lazzeri L (2015). The use of bio-based liquid formulations in pest control of citrus groves. Industrial Crops and Products 75:42-47.
Crossref

 
 

Calvo P, Nelson L, Kloepper JW (2014). Agricultural uses of plant biostimulants. Plant Soil 383(1):3-41. 
Crossref

 
 

Chbani A, Mawlawi H, Zaouk L (2013). Evaluation of brown seaweed (Padina pavonica) as biostimulant of plant growth and development. African Journal of Agricultural Research 8(13):1155-1165.
Crossref

 
 

Childs K, Beeson R C (2000). The Effect of Biostimulant. Drenches on Root Growth of Woody Ornamentals. Ornamental Outlook, 26-28.

 
 

Dey BK, Pfeifer K, Dutta A (2014). The H19 long noncoding RNA gives rise to microRNAs miR-675-3p and miR-675-5p to promote skeletal muscle differentiation and regeneration. Genes and Development 28(5):491-501.
Crossref

 
 

Du Jardin P (2015). Plant Biostimulants: Definition, Concept, Main Categories and Regulation. Scientia Horticulturae196:3-14.
Crossref

 
 

EBIC (2012). What are biostimulants?

View

 
 

EBIC (2014). European Biostimulants Industry Council:

View

 
 

El-Ghamry A, Mosa AA, Alshaal T, El-Ramady H (2018). Nanofertilisers vs. biofertilisers: new insights. Environment, Biodiversity and Soil Security 2:51-72. 
Crossref

 
 

Faessel L, Gomy C, Nassr N, Tostivint C, Hipper C, Dechanteloup A (2014). Produits de stimulation en agriculture visant à améliorer les fonctionnalités biologiques des sols et des plantes. Étude des connaissances disponibles et recommandations stratégiques, rapport d'étude au ministère de l'Agriculture, de l'Agroalimentaire et de la Forêt, Bio by Deloitte et RITTMO Agroenvironnement 148 p.

 
 

Ghosh N (2007). Promoting Biofertilizer in INDIA. Instiute of Economic growth University of Enclave.

 
 

Glick BR (2012). Plant Growth-Promoting Bacteria Mechanisms and Applications. Scientifica 15. 
Crossref

 
 

Gomiero T (2018). Food quality assessment in organic vs. conventional agricultural produce: findings and issues. Applied Soil Ecology 123:714-728. 
Crossref

 
 

Gupta G, Parihar SS, Ahirwar NK, Snehi SK, Singh V (2015). Plant growth promoting rhizobacteria (PGPR): current and future prospects for development of sustainable agriculture. Journal of Microbial & Biochemical Technology 7(2):096-102. 
Crossref

 
 

Hadwiger LA (2013). Multiple effects of chitosan on plant systems: solid science or hype. Plant Science 208:42-9. 
Crossref

 
 

Kamran M, Cui W, Ahmad I, Meng X, Zhang X, Su W, ... Liu T (2018). Effect of paclobutrazol, a potential growth regulator on stalk mechanical strength, lignin accumulation and its relation with lodging resistance of maize. Plant Growth Regulation 84(2):317-332. 
Crossref

 
 

Katiyar D, Hemantaranjan A, Singh B (2015). Chitosan as a promising natural compound to enhance potential physiological responses in plant: a review. Indian Journal of Plant Physiology 20(1):1-9. 
Crossref

 
 

Kauffman GL, Kneivel DP, Watschke TL (2007). Effects of a biostimulant on the heat tolerance associated with photosynthetic capacity, membrane thermostability, and polyphenol production of perennial ryegrass. Crop Science 47(1):261-267.
Crossref

 
 

Lambert L (2006). Découvrez les biostimulants, Québec Vert, Médias Transcontinental 28(2):67.

 
 

Lobley M, Butler A, Reed M (2009). The contribution of organic farming to rural development: An exploration of the socioeconomic linkages of organic and non-organic farms in England. Land Use Policy 26(3):723-735. 
Crossref

 
 

Mehnaz S (2015). Azospirillum: a biofertilizer for every crop. In: Arora, N.K. (Ed.), Plant Microbes Symbiosis: Applied Facets. Springer India, New Delhi pp. 297-314. 
Crossref

 
 

Mishra A, Das D, Saren S (2013). Preparation of GPS and GIS based soil fertility maps for Khurda district, Odisha. Indian Agriculturist 57:11-20.

 
 

Nellemann C, Mac Devette M, Manders T, Eickhout B, Svihus B, Prins A G, Kaltenborn B P (2009). The environmental food crisis-The environment's role in averting future food crises. A UNEP rapid response assessment. United Nations Environment Programme, GRID-Arendal. Birkeland Trykkeri AS, Norway pp. 1-104.

 
 

Noumavo AP, Agbodjato AN, Gachomo EW, Salami HA, Baba-Moussa F, Adjanohoun A, Kotchoni and Baba-Moussa L (2015). Metabolic and Biofungicidal Properties of Maize Rhizobacteria for Growth Promotion and Plant Disease Resistance. African Journal of Biotechnology pp. 14811-819. 
Crossref

 
 

Raja N (2013). Biopesticides and biofertilisers: ecofriendly sources for sustainable agriculture. Journal of Biofertilisers and Biopesticides 4:112.
Crossref

 
 

Rashid HO, Yadav RK, Kim HR, Chae HJ (2015). ER stress: Autophagy induction, inhibition and selection. Autophagy 11(11):1956-1977.
Crossref

 
 

Roychowdhury D, Paul M, Banerjee SK (2014). A review on the Effects of Biofertilisers and Biopesticides on Rice and Tea Cultivation and Productivity. International Journal of Science Technology and Management 2(8):96-106.

 
 

Schütz L, Gattinger A, Meier M, Müller A, Boller T, Mäder P, Mathimaran N (2018). Improving crop yield and nutrient use efficiency via biofertilization. A global meta-analysis. Frontiers in Plant Science 8:2204. 
Crossref

 
 

Simarmata T, Turmuktini T, Fitriatin BN, Setiawati MR (2016). Application of bioameliorant and biofertilisers to increase the soil health and rice productivity. HAYATI Journal of Biosciences 23(4):181-184.
Crossref

 
 

Singh S, Singh V (2018). Maximizing wheat (Triticum aestivum) productivity and profitability using site specific nutrient management strategy. Annals of Plant and Soil Research 20(1):103−106.

 
 

Somers E, Vanderleyden J, Srinivasan M (2004). Rhizosphere bacterial signalling: a love parade beneath our feet. Critical Reviews in Microbiology 30(4):205-235. 
Crossref

 
 

Torre LA, Battaglia V. Caradonia F (2016). An overview of the current plant biostimulant legislations in different European Member States. Journal of the Science of Food and Agriculture 96(3):727-734. 
Crossref

 
 

Vessey JK (2003). Plant growth promoting rhizobacteria as biofertilisers. Plant Soil 255(2):571-586. doi: 10.1023/A:10260372 16893
Crossref

 
 

Xiang S, He Y, Zhang Z, Wu H, Zhou W, Krishna R, Chen B (2012). Microporous metal-organic framework with potential for carbon dioxide capture at ambient conditions. Nature Communications 3(1):1-9.
Crossref

 
 

Yakhin OI, Lubyanov AA, Yakhin IA, Brown PH (2017). Biostimulants in Plant Science: A global Perspective. Frontiers in Plant Science 7:2049. 
Crossref

 

 




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