Front. Sustain. Food Syst. Frontiers in Sustainable Food Systems Front. Sustain. Food Syst. 2571-581X Frontiers Media S.A. 10.3389/fsufs.2021.606308 Sustainable Food Systems Review Potential Use of Beneficial Microorganisms for Soil Amelioration, Phytopathogen Biocontrol, and Sustainable Crop Production in Smallholder Agroecosystems Koskey Gilbert 1 2 Mburu Simon Wambui 1 3 Awino Richard 1 Njeru Ezekiel Mugendi 1 * Maingi John M. 1 1Department of Biochemistry, Microbiology and Biotechnology, Kenyatta University, Nairobi, Kenya 2Institute of Life Sciences, Scuola Superiore Sant'Anna, Pisa, Italy 3Department of Biological Sciences, Chuka University, Chuka, Kenya

Edited by: Duraisamy Saravanakumar, The University of the West Indies St. Augustine, Trinidad and Tobago

Reviewed by: Naeem Khan, University of Florida, United States; Praveen Guleria, DAV University, India

*Correspondence: Ezekiel Mugendi Njeru njeru.ezekiel@ku.ac.ke

This article was submitted to Crop Biology and Sustainability, a section of the journal Frontiers in Sustainable Food Systems

29 04 2021 2021 5 606308 14 09 2020 30 03 2021 Copyright © 2021 Koskey, Mburu, Awino, Njeru and Maingi. 2021 Koskey, Mburu, Awino, Njeru and Maingi

This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

Smallholder agroecosystems play a key role in the world's food security providing more than 50% of the food produced globally. These unique agroecosystems face a myriad of challenges and remain largely unsupported, yet they are thought to be a critical resource for feeding the projected increasing human population in the coming years. The new challenge to increase food production through agricultural intensification in shrinking per capita arable lands, dwindling world economies, and unpredictable climate change, has led to over-dependence on agrochemical inputs that are often costly and hazardous to both human and animal health and the environment. To ensure healthy crop production approaches, the search for alternative ecofriendly strategies that best fit to the smallholder systems have been proposed. The most common and widely accepted solution that has gained a lot of interest among researchers and smallholder farmers is the use of biological agents; mainly plant growth promoting microorganisms (PGPMs) that provide essential agroecosystem services within a holistic vision of enhancing farm productivity and environmental protection. PGPMs play critical roles in agroecological cycles fundamental for soil nutrient amelioration, crop nutrient improvement, plant tolerance to biotic and abiotic stresses, biocontrol of pests and diseases, and water uptake. This review explores different research strategies involving the use of beneficial microorganisms, within the unique context of smallholder agroecosystems, to promote sustainable maintenance of plant and soil health and enhance agroecosystem resilience against unpredictable climatic perturbations.

plant growth promoting microorganisms biocontrol agents microbial inoculants smallholder agroecosystems soil fertility food security Office of the Royal Society10.13039/501100008134

香京julia种子在线播放

    1. <form id=HxFbUHhlv><nobr id=HxFbUHhlv></nobr></form>
      <address id=HxFbUHhlv><nobr id=HxFbUHhlv><nobr id=HxFbUHhlv></nobr></nobr></address>

      Introduction

      Biological soil fertility restoration techniques within the smallholder agroecosystems, in combination with other agronomic management practices, would provide the much-needed solutions for revitalizing the declining global food production (Raimi et al., 2017). Beneficial soil microbiota such as plant growth promoting microorganisms (PGPMs), comprising of specific groups of bacteria and fungi, provide essential agroecosystem services that support plant growth (Rouphael and Colla, 2020) and ameliorates soil productivity (Santos et al., 2019). PGPMs maintain key agroecological cycles fundamental for soil nutrient enrichment, crop nutrient improvement, plant tolerance to biotic and abiotic stresses, biocontrol of pests and diseases, and water uptake enhancement (Lobo et al., 2019; Goswami and Deka, 2020). They are actively involved in healthy plant development and growth through secretion of hormonal growth regulators, and resistance induction against phytopathogens (Dakora et al., 2015). Besides, versatile PGPMs could be used to bioremediate polluted fields and increase the land available for production as in the case of heavy metals polluted soils (Gouda et al., 2018). These agroecosystem services are primarily important in supporting crop production in smallholder agroecosystems, which are characteristically defined by limited resource inputs.

      PGPMs promote plant growth and productivity through various direct and indirect approaches. Several direct mechanisms have been established through previous studies and can be broadly classified into phytostimulants (Babalola and Glick, 2012), biofertilizers (Kalayu, 2019), rhizomediators, or stress regulators (Stamenković et al., 2018). Indirect mechanisms mainly occur in form of biocontrol of phytopathogens through competition for nutrients, enzymatic lysis, antibiosis (Köhl et al., 2019), secretion of volatile organic compounds (VOCs) (Sun and Tang, 2013), and triggering of antioxidative defense mechanism (Sandhya et al., 2010; Malik et al., 2020) and induced systemic resistance (ISR) response in the host plant (Heil and Bostock, 2002). PGPM biofertilizers promote plant growth by enhancing nutrient availability to the plants and the most studied pathways include N fixation (Ahemad and Kibret, 2014; Fukami et al., 2018b), P and K solubilization (Sharma et al., 2013; Soumare et al., 2020), S oxidation, Fe and C sequestration (Kannahi and Senbagam, 2014; Velivelli et al., 2014). PGPMs enhance the availability of P, K, Zn, Se, and Fe in the soil through biochemical processes such as solubilization, chelation, mineralization, oxidation and reduction reactions (Ahmed and Holmström, 2014; Velivelli et al., 2014; Rouphael and Colla, 2020). PGPMs are also known to secrete phytohormones such as auxins (Lin and Xu, 2013; Azizoglu, 2019), cytokinin, abscisic acid, ethylene, brassinosteroids, jasmonic acid, salicylic acid, strigolactones, and gibberellins (Goswami and Deka, 2020; Saad et al., 2020) that act as plant growth stimulators and stress controllers.

      The PGPMs functionality and vigor, however, depend on intrinsic soil properties, environmental and agronomic management factors. Nutrient availability, soil pH, water, temperature, crop genotype, and cultural management are some of the key drivers determining the survival and function of PGPMs in the soil (Gouda et al., 2018; Gupta et al., 2019). For maximum farm benefits to be realized in a highly heterogenous smallholder systems (Njeru et al., 2020), tradeoffs in balancing the highlighted determinants have to be considered and appropriate farm management practices are ought to be carried out. For instance, the choice of crop species and diversity is critical in stimulating specific plant-microbe interactions and consequently the intended output (Orrell and Bennett, 2013; Saad et al., 2020). The authors suggest the use of multiple cropping systems that promote synergy and minimize the yield gap between the potential and realized production, a phenomenon that is commonly seen in smallholder systems. Additional methods efficient in augmenting indigenous soil PGPMs can be integrated to enhance microbial bio-functionality. These include the use of organic amendments such as farmyard manure and vermicompost (Mosa et al., 2018; Koskey et al., 2020), biotechnological approaches such as plant breeding (Bakker et al., 2012), crop management practices such as agroforestry, rotation, intercropping, cover cropping, and practicing reduced soil disturbance (Ventorino et al., 2012; Hontoria et al., 2019; Elagib and Al-Saidi, 2020).

      The increasing demand among smallholder farmers to cut input costs and the need for sustainable nutrient management practices is driving the growing adoption and use of microbial-rich fertilizers in smallholder setups (Raimi et al., 2017). Commercial microbial inoculants (commonly used as biofertilizers or bioenhancers) containing single species or multiple strains of rhizobia, Pseudomonas spp., Azotobacter spp., Bacillus spp., Trichoderma spp., Aspergillus spp., and Glomus spp. (Figure 1) have been largely used in smallholder agroecosystems for crop production (Koskey et al., 2017; Bargaz et al., 2018; Adeyemi et al., 2019). Previous field researches carried out in different agroecosystems around the world have reported varying levels of successes on the use of PGPMs to support crop performance quantitatively and qualitatively (Pellegrino et al., 2012; Mishra et al., 2019; Saad et al., 2020). However, little has been done focusing on the use of PGPMs to address various challenges facing smallholder agroecosystems in the context of changing climatic conditions. Therefore, this review explores different available strategies involving the use of beneficial microorganisms as biofertilizers, within the unique context of smallholder agroecosystems, to promote sustainable maintenance of plant and soil health, and enhance agroecosystem resilience against unpredictable climatic perturbations.

      Plant growth promoting microorganisms (PGPMs) play a significant role in provision of beneficial ecosystem services in resource-limiting smallholder farming systems. Together with crops such as legumes (Phaseolus vulgaris L.), they form multifunctional interactions that enhance nutrient availability and uptake, pest and disease suppression, soil organic matter (SOM) accumulation and formation of soil aggregates, that collectively increase crop productivity.

      Roles and Challenges of Smallholder Agroecosystems in Global Food Security

      Eradicating hunger, poverty, and food insecurity while ensuring sustainable use of natural resources for agriculture, as highlighted in the United Nations Sustainable Development Goals (SDGs), is paramount in a world faced with a myriad of economic, social, political, and environmental challenges (Pérez-Escamilla, 2017). Globally, ~700 million people have no access to sufficient food while about 2 billion people face nutritional deficiencies, of which about 50% of the food insecure individuals are from Asia, 35% from Africa, and 10% from Latin America (FAO, 2018). This is likely to increase due to the current global health and economic crisis due to the Coronavirus disease 2019 (Covid-19) pandemic. Smallholder agroecosystems, predominantly found in developing countries, are considered critical food security resources that will support food production for the increasing human population in the coming years. Currently, it is estimated that smallholder agroecosystems account for more than 50% of the food produced globally (Herrero et al., 2017). In Africa, they contribute about 75% of the total crop production and 50% of the animal products (Nyambo et al., 2019) and, thus, are significantly involved in rural poverty reduction, economic development, and food security. However, compared to large-scale profit-driven systems, smallholder agroecosystems have limited land size, stringent financial resources, low market sharing, and product range, thus, are faced with more risks and vulnerabilities (Kuivanen et al., 2016; Herrero et al., 2017).

      The productivity of smallholder agroecosystems largely depends on the services naturally provided by the ecosystem such as soil fertility, nutrient cycling, water availability, pest control, and pollination (Altieri et al., 2012). Farmers' decision and selection of their appropriate agronomic management practices affect the extent of agroecosystem functioning. External pressures such as poverty, unreliable climatic conditions, and farmer's need for immediate satisfaction exert pressure on land use and cause negative impacts on the ecosystem (IFAD and UNEP, 2013). Agricultural intensification coupled with the use of harmful agrochemical inputs has negatively impacted on smallholder agroecosystems (Bationo et al., 2012). Their long-term sustainability in the face of new challenges such as the shrinking per capita arable lands, emerging diseases, dwindling world economies, and unpredictable climate change, is on the balance. Notwithstanding their benefits, economic and policy marginalization, low investment support, and the increasing land fragmentation of small farms threaten their contribution to global food security, leaving many farmers vulnerable (IFAD and UNEP, 2013). The rising environmental awareness, depletion of natural resources, and human health nutritional concerns have led to a paradigm shift among the farmers from over-dependence on agrochemical inputs to the use of ecofriendly biological agents for agricultural production (Herrero et al., 2017; Alori and Babalola, 2018). To increase the use and adoption of biological agents in smallholder agroecosystems, more robust integrated pathways that encourage food production based on local innovations, practices, and resources should be established. Tapsoba et al. (2020) emphasize that smallholder farmers should be involved in re-designing agricultural production. This way, farmers are likely to integrate new techniques into their current farm management practices to meet their agrosociological and economic needs. The authors warn that some agricultural initiatives may remain localized and isolated despite evidence of success in other agroecosystems. It is, therefore, necessary to have the right network of stakeholders on a territorial scale to support agricultural initiatives and their implementation.

      Use of PGPM Inoculants in Enhancing the Productivity of Smallholder Agroecosystems; Opportunities and Challenges Use of Nitrogen Fixing PGPMs as Biofertilizers

      Nitrogen (N) is one of the essential elements required by plants for proper growth, development, and productivity, and plays a pivotal role in various structural, biochemical, and physiological processes (Giller et al., 2019). Therefore, to achieve good crop productivity and quality, N application in form of nitrogenous-based fertilizers or amendments is inevitable. The production of inorganic N fertilizer through the Haber-Bosch industrial chemical process revolutionized agriculture and significantly increased crop production. However, there are serious human health, economic, and environmental concerns raised on the excessive and continuous use of chemically derived inorganic N fertilizers (Reddy and Saravanan, 2013), and hence the introduction of N biofertilizer formulations as a viable and sustainable alternative. Biological nitrogen fixation (BNF) is a process that naturally involves legumes and rhizobia symbionts, and/or plants and a group of free-living PGPMs known as diazotrophs (Giller et al., 2019). Through the BNF, inert atmospheric N2 gas is converted via a series of enzymatically regulated complex reaction mechanisms into N containing organic compounds utilizable by the plants (Gupta et al., 2019). In symbiotic association, nodule forming rhizobia produces nitrogenase enzyme complex in the presence of leghemoglobin molecules and convert N2 into ammonium and nitrate ions which are readily absorbed by the plants. In return, plant hosts the bacteria inside the root nodules and provide photosynthates such as C that rhizobia uses as an energy source (Wang et al., 2013; Choudhary and Varma, 2017).

      In smallholder farming systems, the use of microbial inoculants containing diazotrophs and symbiotic PGPMs is on the rise. Major groups of N-fixing bacteria commonly used include Rhizobium spp., Azorhizobium spp., Mesorhizobium spp., Bradyrhizobium spp., Thiobacillus spp., Azospirillum spp., Sinorhizobium spp., Clostridium spp., Azotobacter spp., Cyanobacteria, and Frankia spp. (Yeager et al., 2005; Mus et al., 2018; Raimi et al., 2019). It has been demonstrated that inoculating legumes with a single or a consortium of N-fixing bacteria improves soil fertility, plant growth, yield, and nutrition quality (Kawaka et al., 2014; Mabrouk et al., 2018; Menge et al., 2018). Inoculation also enhances root development, nodulation, water stress tolerance, and suppresses pathogenic infestation (Koskey et al., 2017; Alori and Babalola, 2018; Musyoka et al., 2020). Private sectors, research institutions and universities have partnered with smallholder farmers in delivering efficient inoculants. For instance, N2-Africa, a multi-stakeholder project, actively researched on N-fixing rhizobia strains and developed inoculants for use by African smallholder farmers in the production of soybean, common bean, chickpea, ground nut, and faba bean (Giller et al., 2019). In Kenya, the University of Nairobi in collaboration with the Microbiological Resources Center Network (MIRCEN) partnered with MEA Fertilizer Ltd to produce Biofix®, a cheap Rhizobium based bioinoculant for use in the cultivation of legumes (Odame, 1997). In South Africa, BioControl Products SA (Pty) Ltd produces Azospirillum based N-fixing bioinoculants such as Azo-N® and Azo-N Plus® for cultivating grain and cover crop legumes (Raimi et al., 2017). Currently, more bacterial species are being identified for use as potential N-fixing bioinoculants (Ouma et al., 2016; Koskey et al., 2018; Gabasawa, 2020; Musyoka et al., 2020). Most of these trials have shown promising results under greenhouse-controlled conditions. Repeated field trials should be done to ascertain their performance under different ecological conditions of smallholder agroecosystems.

      Generally, BNF can supply more than half of the plant N needs and can significantly reduce the use and overdependence on external chemical N fertilizers in agriculture (Bado et al., 2018). For instance, in Australia, diazotrophic N-fixation is estimated to provide the annual N demand of 20–80 kg N ha−1 year−1 for perennial grasses (Gupta et al., 2019). In Ghana, symbiotic N fixation is estimated to provide up to 16–145 kg N ha−1 year−1 for legumes (Kermah et al., 2018). Therefore, BNF could reduce substantially the use of additional basal or top-dresser inorganic N fertilizers and thus cutting the input cost for the smallholder farmers. BNF contribution and N quantification within smallholder agroecosystems, however, remains poorly understood due to the high cost of resources and technical expertise needed, and difficulty to implement at the grassroot level (Mhango et al., 2017; Bado et al., 2018). Despite a large and diverse genetic pool of N-fixing bacteria (Giller et al., 2019) and legume species suitable for different African agroclimatic conditions (Kebede, 2020), their utilization in promoting soil fertility and plant growth has not been achieved. Hence, new sustainable methods that are affordable, simpler, rapid, and easier to implement in smallholder setups should be developed to fill the aforementioned gap.

      Use of Nutrient (P, K, Fe) Solubilizing and Mobilizing Microorganisms as Biofertilizers

      Soil nutrients such as phosphorus (P), potassium (K), and iron (Fe) often limit plant growth and development because of their low solubility in the soil (Giovannini et al., 2020). They are firmly fixed and are not readily available for plant uptake, and their shortage could be detrimental to healthy growth and physiological development of the plant (Parani and Saha, 2012). Smallholder farmers rely on the external application of inorganic P-fertilizers whose efficiency declines in the presence of too much rainfall. Granular P-inorganic fertilizers precipitate to form metal-cation complexes in rainy tropical ecosystems and thus become unavailable for plant use (Dissanayaka et al., 2018). Most soils of East and West Africa experience N, P, and K deficiency (Bationo et al., 2012). Therefore, the use of low-cost P and K solubilizing and mobilizing microorganisms that take part in P and K geo-cycles would be of paramount importance to alleviate soil nutrient deficiency and losses. They mineralize organic P and K through a series of complex enzymatic and hydrolytic reactions (Thakur et al., 2014) and also secrete organic acids such as gluconic, lactic, and oxalic acids that hydrolyze inorganic P compounds found in the soil (Sharma et al., 2013). Figure 2 shows the effect of maize (Zea mays L.) and cowpea [Vigna unguiculata (L.) Walp.] inoculation with P solubilizing bacteria (PSB) under controlled greenhouse conditions. There was an improved growth of maize and cowpea plants inoculated with PSB compared to the un-inoculated controls. Similarly, field studies have reported an enhanced growth, yield and improved nutritional values on crops inoculated with PSBs (Kalayu, 2019; Soumare et al., 2020). The most commonly used P and K solubilizing microorganisms (PSMs) include bacteria such as Pseudomonas spp., Enterobacter spp., Burkholderia spp., and Bacillus spp., and fungi such as Penicillium spp., Trichoderma spp., and Aspergillus spp. (Aseri et al., 2009; Sangeeth et al., 2012; Selvi et al., 2017). Although these studies evidently show increase in P solubilization when a single or a combination of bacteria species are used, the mechanism of action leading to synergism in delivering P to the plants remains unclear.

      Application of phosphate solubilizing bacteria (PSB) enhances P availability without disturbing the soil biochemical composition, improves plant growth, photosynthetic activity, crop nutritional values, and yield. The photo shows a greenhouse experiment carried out by the Kenyatta University FLAIR research students on the effect of PSB inoculation on Zea mays L. and Vigna unguiculata (L.) Walp. (A) Un-inoculated Zea mays L. plant, (B) PSB inoculated Zea mays. L plant, (C) PSB inoculated Vigna unguiculata (L.) Walp, and (D) Un-inoculated Vigna unguiculata (L.) Walp. Inoculated plants showed improved growth and enhanced photosynthetic activity.

      Arbuscular mycorrhizal fungi (AMF) are also well-known for P mobilization and solubilization and this has led to the development of mycorrhizal inoculants (Tabassum et al., 2017). AMF colonize the roots of nearly 90% of the terrestrial plants and increase the plant root surface area for the absorption of nutrients and water. Primarily, AMF actively participates in P and K mobilization and solubilization and this has been demonstrated both in the greenhouse and in the field with various crops including cereals, legumes, vegetables, fruits and trees (Wu et al., 2005; Njeru et al., 2017; Avio et al., 2018). The most commonly used AMF inoculants include Funneliformis mosseae, Glomus etunicatum, and Rhizophagus irregularis (Giovannini et al., 2020; Musyoka et al., 2020). Iron starvation in the soil causes a specific group of plants and soil microbes to secrete siderophores, iron specific chelating molecules, that play a vital role in iron transportation and regulating its bioavailability (Novo et al., 2018). Multifunctional biofertilizers containing Bacillus subtilis, Pseudomonas aeruginosa, Penicillium chrysogenum, and Streptomyces griseus not only secrete ferric ion-specific chelating biomolecules but also stimulate antagonistic actions against rhizosphere pathogens (Ahmed and Holmström, 2014; Kannahi and Senbagam, 2014).

      In Kenya, smallholder farmers utilize Rhizatech® inoculant (Table 1) containing a combination of three AMF species produced and distributed by Dudu Tech Ltd company (Faye et al., 2020). In South Africa, Mycoroot (Pty) Ltd produces a number of Mycoroot® branded AMF inoculants that solubilize P, K, Cu, Zn, and Fe, and improve plant tolerance against abiotic stresses. Organo® biofertilizer produced by Amka Products (Pty) Ltd, South Africa, contains Bacillus spp., Enterobacter spp., Pseudomonas spp., Stenotromonas spp., and Rhizobium spp (Raimi et al., 2017). These PGPMs secrete siderophores and multifunctional plant growth promoting hormones such as gibberellin, IAA, and cytokinin (Saad et al., 2020). Pseudomonas fluorescens, produced by BioControl Products SA (Pty) Ltd as NAT-P®, and Bacillus subtilis produced by Ag-Chem Africa SA (Pty) Ltd as B-RUS®, are some of the commonly used multifunctional inoculants available for farmers (Raimi et al., 2017). In addition to P-K-solubilization, they produce siderophores that bind iron (Fe3+) suppressing its availability to phytopathogens, and indole acetic acid (IAA) responsible for stimulating root growth and plant cell elongation (Parani and Saha, 2012).

      Selected examples of bio-inoculant products and their roles in smallholder agroecosystems.

      Bioinoculant product name Main PGPMs components (declared or based on previous studies) Manufacturer /Distributor Roles declared by the manufacturer or reported through research References
      Bonasol® A consortium of Azospirillum brasiliense, Pseudomonas fluorescens, Pseudomonas spp., Bacillus subtilis, and Glomus intraradices Abiosa (Mexico) Enhance P and K nutrition in tomato, pepper, and chili crops Jiménez-Gómez et al., 2017
      Biofix® N-fixing bacteria MEA Ltd (Kenya) Enhance N fixation and yields of legumes (snow peas, common beans, soybeans) Odame, 1997; Koskey et al., 2017
      Ajay azo/rhizo/azospirillum® Azotobacter spp., Rhizobium spp., and Azospirillum spp. Ajay bio-tech (India) limited N-fixation and P-solubilization in legumes and cereals Alori and Babalola, 2018; Celador-Lera et al., 2018
      Nitrofix® Azospirillum chroococcum Agri-Life (India) Produces phytohormones such as auxins and increases N and P uptake in legumes and vegetables Wu et al., 2005; Azizoglu, 2019
      QuickRoots® Bacillus amyloliquefaciens and Trichoderma virens Bayer group-acceleron Solubilize P, enhance root development, moisture, and NPK uptake in corns Celador-Lera et al., 2018; Kalayu, 2019; Saad et al., 2020
      LegumeFix® Rhizobium spp. Legume technology (UK) N fixation and growth enhancement in various legumes Masso et al., 2016; Faye et al., 2020
      Azotobacterin® Azospirillum brasiliense B-4485 JSC “Industrial innovations” (Russia) Increase (up to 20%) in yields of maize, barley, and wheat Fukami et al., 2018a; Misra et al., 2020
      VitaSoil® A consortium of rhizospheric PGPMs Symborg (Spain) Soil nutrient amelioration and growth promotion in cereals and legumes Celador-Lera et al., 2018; Misra et al., 2020
      Pro-soil® Consortium of Bacillus subtilis, Rhodopseudomonas palustris, and Streptococcus thermophilus Efficient microbes South Africa Increase nutrient uptake in grasses and legumes and balances NPK levels in the soil Iriti et al., 2019
      TwinN® A consortium of N-fixing diazotrophs, P solubilizers and plant growth microbial inducers Mapleton Agri Biotec Pt Ltd (Australia) Increase crop growth and productivity, N and P acquisition, auxins secretion and induce disease resistance to plants Azizoglu, 2019
      Rhizatech® Various strains of AMF Glomus intraradices, G. claroideum, G. etunicatum, and G. mosseae Dudutech Ltd (Kenya) Increase the absorption and translocation of P, N, S, Zn, and Cu Kavoo-Mwangi et al., 2013; Mukhongo et al., 2017
      Trichotech® Trichoderma asperellum strain kd Dudutech Ltd (Kenya) Biocontrol of soil borne fungal diseases caused by Fusarium, Pythium and Rhizoctonia in horticultural crops Preininger et al., 2018
      Zander mycorrhiza® Different strains of AMF Zander coporation (UK) Enhance plant nutrition (NPK), growth and health, and induce plant tolerance to water stress in arid zones Faye et al., 2020
      Myco apply® Various endo-AMF species including Glomus intraradices, G. aggregatum, G. etunicatum, G. mosseae, and ecto-AMF species like Rhizopogon villosulus, R. amylopogon, Scleroderma cepa, among others Mycorrhizal applications, Inc. (USA) Increase solubility of P, Zn, Cu, Fe, and Mn and secretion of enzymes and siderophores Faye et al., 2020
      Symbion VAM plus® Bacillus megaterium var. phosphaticum and two AMF strains Glomus fasciculatum and Gigaspora spp. T. Stanes and company Ltd (India) Enhance the absorption of P, water and other micro elements and induce water stress and fungal diseases resistance Khalid et al., 2017; Mukhongo et al., 2017; Mishra et al., 2019
      ECO-T® Trichoderma asperellum Plant health products (Pty) Ltd (South Africa) Biofungicide against Pythium, Fusarium, and phytophthora diseases and promotes the development of healthy root systems Kavoo-Mwangi et al., 2013
      PHC biopak® Bacillus licheniformis, B. megaterium, Paenibacillus azotofixans, B. subtilis, and B. polymyxa Plant health care Inc. (USA) Stimulates NPK uptake and enhance the survival, growth, and productivity of crops Egamberdiyeva, 2007; Kavoo-Mwangi et al., 2013
      Mycor® Glomus intraradices Iftech (France) Stimulates root growth and P acquisition and increases plant resistance against climatic stress Rowe et al., 2007; Kavoo-Mwangi et al., 2013; Mosa et al., 2018
      SumaGrow® A consortium of N-fixers, P-solubilizers, and other plant nutrient-mobilizing microbes suspended in organic humid acid carrier Bio soil enhancers, Inc. (BSEI), USA Increase crop yields and nutritional values of food and forage crops, reduce fertilizer dependence, and ameliorates soil pH gradient under extreme environmental conditions Rivera et al., 2015; Preininger et al., 2018

      Despite their novel potential use as agro-inputs, various biotic and abiotic factors may mask the performance of several upcoming commercial bioinoculants in delivering nutrients to the plant (Wahid et al., 2020). Comparative studies on their performance in various smallholder agroecosystems characterized by varying soil typologies should be assessed. Recent studies have suggested that a second generation of multi-trait bioinoculants should be developed based on specific biostimulatory synergism of different PGPMs (Rouphael and Colla, 2020). However, little work has been done to adequately understand the synergistic role of AMF, P-solubilizing bacteria, and siderophore producers and how smallholder farming conditions affect their functional roles. Without scientific experiments to answer these considerations, the economic benefits in the use of bioinoculants in smallholder setups will remain elusive.

      PGPMs in Enhancing the Adaptation of Crops to Abiotic Stresses

      Crop production in rain-fed smallholder agroecosystems is mainly limited by various abiotic stresses that interfere with the genetic regulation of key cellular pathways in plants and severely affect the plant's physiological functioning and morphology (Sindhu et al., 2020). High temperatures, water stress, salinity, and floods are some of the important abiotic plant stressors experienced by smallholder farmers in SSA and may cause up to 70% of crop yield losses (Bationo et al., 2012). As the average global temperatures increase, the risk of widespread desertification heightens and this could traverse across many developing nations, hitting on the majority of the vulnerable smallholder farmers the hardest. The search for new plant breeds that could cope up with the stressors is a long-drawn and costly process considering the unique crop diversity of smallholder agroecosystems. Exploiting the unique environment-tolerant properties of microorganisms, their huge genetic diversity, and interaction with various plants could be crucial in addressing the management of abiotic stress in agriculture (Grover et al., 2011).

      Agroforestry is an important practice central to climate change mitigation, soil and water conservation, energy and food sources. There is evidence that farmer-managed agroforestry is responsible for the significant increase in food production, tree diversity, and the greening trends in the Sahel region of Senegal, Niger, and Mali (Elagib and Al-Saidi, 2020). The choice of tree species used in agroforestry depends on various environmental, social, and economic factors. Recently, many development programs in collaboration with the local farmers of the Sahel region have engaged to combat the rising desertification through the use of leguminous trees such as acacia (Sileshi et al., 2020). Legumes such as Acacia seyal, A. senegal, and A. albida have successfully demonstrated their ability to interact with the indigenous AMF and rhizobia species of the Sahel region of West Africa and are considered potential agents for carbon sequestration and land restoration in the region (Fofana et al., 2020). Based on these and other evidence, integration of biofertilization and optimization of agroforestry techniques in the context of an integrated fight against desertification should be considered. The search for potential microbial candidates for ameliorating various abiotic stresses, restoring soil fertility, and enhancing crop productivity should be done in areas vulnerable to the effects of climate change (Goswami and Deka, 2020).

      PGPMs exhibiting growth-promoting and stress-tolerant traits such as secretion of volatile organic compounds (VOCs), osmoprotectants (proline, glutamate, trehalose), siderophores, gibberellic and IAA production, P-solubilization, and exopolysaccharides (EPS) (Table 2) could be ideal for use in dryland agroecosystems (Grover et al., 2011; Gouda et al., 2018). For instance, in semiarid regions of India, EPS-producing drought-tolerant strains of Pseudomonas spp. with various plant-growth inducing traits, osmoregulation, and antioxidant properties on maize have been identified (Sandhya et al., 2010). EPS cement and stabilizes soil aggregates together creating a biofilm that increases water retention and regulates nutrient and water flow within the plant roots (Grover et al., 2011). In Brazil, an impressive soybean yield enhancement and increased tolerance to water stress have been reported through co-inoculation with Azospirillum brasilense and Bradyrhizobium japonicum (Hungria et al., 2015). PGPMs such as Pseudomonas spp., Burkholderia spp., Funneliformis mosseae, Enterobacter spp., and Rhizophagus irregularis stimulate osmolyte regulation mechanisms that control plant cell wall integrity and induce plant tolerance to water and salinity stresses (Agami et al., 2016; Gouda et al., 2018).

      Plant growth promoting rhizobacteria (PGPR) and their plant growth promoting traits and mechanisms.

      Plant growth promoting rhizobacteria (PGPR) Plant growth promoting traits and mechanisms Host/associated plant References
      Achromobacter marplatensis and Achromobacter xylosoxidans Production of phytohormones IAA and promote vegetative growth and yield Tomato (Solanum lycopersicum L.) Salem, 2016; Abdel-Rahman et al., 2017
      Aeromonas veronii and Acetobacter diazotrophicus Production of phytohormone indole-3-acetic acid (IAA) Rice (Oryza sativa L.) Etesami et al., 2015
      Azospirillum brasilense Promote secretion of nod-gene inducing flavonoids Common bean (Phaseolus vulgaris L.) Coniglio et al., 2019
      Azospirillum spp. and Azotobacter spp. Nutrient uptake Maize (Zea mays L.) Abdel Latef et al., 2020
      Azotobacter chroococcum Enhance resistance against armyworm Maize (Zea mays L.) Song et al., 2020
      Bacillus amyloliquefaciens Induces systemic resistance against tomato leaf curl virus disease Tomato (Lycopersicon esculentum L.) Guo et al., 2019
      Bacillus aryabhattai Production of phytohormones Soybean (Glycine max (L.) Merr.) Park et al., 2017
      Bacillus cereus Biotic stress resistance against bacterial speck disease caused by Pseudomonas syringae pv. tomato Tomato (Solanum lycopersicum L.) Niu et al., 2012
      Bacillus pumilus and B. subtilis Resistance against downy mildew disease Millet (Pennisetum glaucum L.) Kushwaha et al., 2020
      Bacillus subtilis Absorption of K+ Tobacco (Nicotiana tabacum) Ding et al., 2020
      Bacillus thuringiensis Bio-pesticide Maize (Zea mays L.) Sanchis, 2011; Melo et al., 2016
      Bradyrhizobium spp. Biological nitrogen fixation Soybean (Glycine max (L.) Merr.) Mburu et al., 2020
      Enterobacter spp. Production of phytohormones IAA Lettuce (Lactuca sativa L.) Park et al., 2015
      Gluconacetobacter diazotrophicus Enhance nitrogen fixation and induce tolerance to NaCl Wheat (Triticum aestivum L.) and sorghum (Sorghum bicolor L.) Velázquez-Hernández et al., 2011
      Klebsiella variicola, Enterobacter roggenkampii, and Pseudomonas koreensis Nitrogen fixation Sugarcane (Saccharum officinarum L.) Wei et al., 2014; Li et al., 2017; Guo et al., 2020
      Paenibacillus alvei and Bacillus velezensis Confer resilience to water stress and crown rot disease caused by Fusarium pseudograminearum Sorghum bicolor (L.) Carlson et al., 2020
      Pseudomonas fluorescens Production of 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase to confer resilience against salinity Groundnuts (Arachis hypogea L.) Saravanakumar and Samiyappan, 2007
      Pseudomonas aeruginosa and P. fluorescens Cytokinin production Soybean [Glycine max (L.) Merr.] Kumawat et al., 2019
      Pseudomonas fluorescens Promotes early plant development and enhances yield and leaf nutrition Canola (Brassica napus L.), tomato (Solanum lycopersicum L.), and banana (Musa spp.) Gamez et al., 2019; Premachandra et al., 2020
      Pseudomonas putida, P. fluorescens, Bacillus megaterium and B. polymyxa Phosphate solubilization Potato (Solanum tuberosum) and legumes Browne et al., 2009; Dawwam et al., 2013
      Pseudomonas spp. Promote nodulation in mung bean (Vigna radiata L.) Vigna radiata (L.) Kumari et al., 2018
      Pseudomonas spp., Burkholderia spp., and Acidithiobacillus spp. K solubilization Soybean [Glycine max (L.) Merr.] Jaiswal et al., 2016
      Rhizobium leguminosarum and Bradyrhizobium japonicum Amelioration of arsenic toxicity Legumes Seraj et al., 2020
      Sinorhizobium meliloti Confer acid tolerance Alfalfa (Medicago sativa L.) Draghi et al., 2017
      Streptomyces cellulosae Confer resistance against tobacco mosaic virus Tomato (Solanum lycopersicum L.) Abo-Zaid et al., 2020
      Trichoderma erinaceum Biocontrol agent, stress resilience inducer, and promotes plant growth Rice (Oryza sativa L.) Swain et al., 2018
      Trichoderma harzianum Enhances production of auxins and biomass production Cucumber (Cucumis sativus L.) Zhang et al., 2013

      High soil salinity, caused by excessive water evaporation and accumulation of chloride salts such as NaCl and MgCl2, negatively affect soil microbial biomass, seed germination, and plant development via osmotic potential or ion-specific damage mechanisms (Sindhu et al., 2020). In Uganda, smallholder farmers use Symbion vam plus® biofertilizer produced by T. Stanes and Company Ltd, and contains Bacillus megaterium, Glomus spp., and Gigaspora spp. that improve salinity tolerance and bioavailability of nutrients such as Fe, Cu, Zn, and P (Mukhongo et al., 2016). Gururani et al. (2013) reported increased potato (Solanum tuberosum) tuberization, enhanced tolerance to salt, drought and heavy metal stresses upon inoculation with two Bacillus spp. that induce changes in the expression of reactive oxygen species (ROS), scavenging enzymes, and proline content. Oxidative stress is commonly associated with drought, salinity and high-temperature conditions and also during plant-pathogen interaction. Fukami et al. (2018a) reported an enhanced induced systemic tolerance (IST) on maize against salinity stress following co-inoculation with Azospirillum brasilense and Rhizobium tropici that significantly affected antioxidant enzymes and proline content in the leaves.

      The area of multi-microbial combinations to equip plants with abiotic stress tolerance is still equivocal and involves many genes of which some have not been identified yet. Thus, further research at the gene regulation level should elucidate the superior performance or lack of additive or synergistic effects that are observed when a combination of certain PGPMs are applied in the field (Ouma et al., 2016; Njeru et al., 2017). Understanding the complex plant-microbe interactions, stress tolerance, response, and adaptation as influenced by the changing soil and environmental factors will be important. Advanced biotechnological tools for identifying the potential microbial candidates with abiotic stress-tolerant properties should be employed and tested for their efficiency under different smallholder agroecosystems.

      Use of Microorganisms in Suppression of Pests and Diseases

      Evidence-based concerns against the use of synthetic chemical pesticides are increasingly pushing for the need to develop environmentally friendly pest and disease management strategies. Teratogenic and carcinogenic effects of chemical pesticides have been well-documented (Nicolopoulou-Stamati et al., 2016; Bonner and Alavanja, 2017). Notwithstanding the injurious effects, the development of synthetic pesticides is a complex process and requires rigorous regulatory approval demands. Besides, they are often costly and beyond the reach of the resource-strained smallholder farmers that contribute immensely to global food security (Mburu et al., 2016; Constantine et al., 2020). In smallholder agroecosystems, pests and diseases cause agricultural losses ranging from 45 to 100% (McDonald and Stukenbrock, 2016), depending on the infestation level. Fall armyworm alone can potentially cause losses of up to 13 billion USD in the smallholding family units of Sub-Saharan Africa (Harrison et al., 2019). Other than significantly limiting yields, most fungal pathogens are well-known producers of mycotoxins that negatively impact human health (Zhou et al., 2018). Development of alternative green technologies in pest and pathogen control is a need of the hour that should be fast-tracked to boost crop production that could feed the growing human population with minimalist disturbance to the already shrunk natural ecosystems. Microorganisms have been widely used as biological control agents (BCAs) for a long time and have been established to antagonize and suppress destructive entomopathogens in several ways (Köhl et al., 2019).

      Most bacterial BCAs are of the genus Bacillus, with Bacillus thuringiensis being the most widely used bacterial biocontrol agent against common fungal pathogens and insects. Its derivatives are found in over 70% of bacterial biopesticides (Melo et al., 2016; Liu et al., 2019). Agrobacterium, Arthrobacter, Burkholderia, Azotobacter, Rhizobium, Serratia, Thiobacillus, and Pseudomonas are other bacteria genera with antibiotic attributes in-vitro and in-vivo (Saxena et al., 2000; Raaijmakers et al., 2002). Bacterial biopesticides, like most BCAs, are environmentally friendly and are inexpensive to develop and can be as effective as synthetic pesticides (McDonald and Stukenbrock, 2016; Köhl et al., 2019). Pseudomonas fluorescens has been established to be as effective in controlling the root decay agent Aphanomyces cochlioides in sugar beet as the commercial fungicides (Kristek et al., 2006). Most fungal BCAs are of the genera Aspergillus, Penicillium, Beauveria, Metarhizium, and Trichoderma (Abbey et al., 2019; McGuire and Northfield, 2020). Trichoderma species have been extensively studied for their antagonism against common soil-borne pathogens such as Rhizoctonia and Fusarium (Haldar and Sengupta, 2015; Köhl et al., 2019). Most destructive arthro-pests have also been successfully suppressed in smallholder agroecosystems through the use of Steinernema and Heterorhabditis nematodes (Arthurs and Heinz, 2006), baculoviruses and protozoa, such as Nosema (Sarwar, 2015; Hatting et al., 2019). BCAs act against pests and pathogens in several established ways, which can be direct or indirect. Understanding the modes of action of BCAs are integral in determining their efficacy in field conditions since in-vitro antagonism is not often reflected in-vivo (Köhl et al., 2019).

      Direct mechanisms of antagonism involve parasitism, antibiosis, and predation (Figure 3). Mycoparasitism is the primary mode of action of most strains of Trichoderma and Clonostachys spp. against fungal pathogens (Abbey et al., 2019). Bdellovibrio bacteriovorus is a biocontrol agent unique in its ability to invade and derive nutrients from the cytoplasmic contents of other pathogenic gram-negative bacteria (McNeely et al., 2017). The direct antagonistic mechanisms of microbial BCAs are aided by the agents' ability to secrete cell wall degrading enzymes; chitinases, proteases, cellulases, glucanases, esterases, and catalases (Alori and Babalola, 2018). These hydrolytic enzymes facilitate the penetration of pathogen's cell wall and pest's tissues. Bacillus thuringiensis, the prime entomopathogenic bacteria, produces endotoxins that disrupt insect cell structures, inducing osmotic cell lysis that causes significant ion leakage and functional integrity loss (Melo et al., 2016; Azizoglu, 2019). Steinernema and Heterorhabditis nematodes secrete lytic enzymes that enable them to invade and release bacteria into the insect's haemocoel (Arthurs and Heinz, 2006). The infected insects consequently die of septicaemia. Trichoderma asperellum, Trichoderma virens, Trichoderma atroviride, and Trichoderma harzianum, are well-known to possess a high level of chitinolytic activity against common soil-borne pathogens such as Fusarium, Aspergillus, Rhizoctonia, and Puccinia (Panwar et al., 2014; Abbey et al., 2019). At humidity of at least 60%, BCA Ampelomyces germinates its pycnidia on host surfaces and penetrates powdery mildew hyphae resulting in cytoplasm degeneration (Kiss, 2008).

      PGPMs are considered models of biotechnological interest in agronomy. Their positive effects on crops can be direct as in the case of stimulating plant growth by enhancing nutrient acquisition via mechanisms such as N fixation, P solubilization, siderophore production, and secretion of phytohormones. Indirect methods are mainly in form of biocontrol of plant pest and diseases which is achieved through antibiosis, antagonism, competition, predation, enzymatic lysis, and induction of plant systemic resistance.

      Other than parasitism, most BCAs also suppress pathogens directly through the production of antibiotic compounds that impede the proliferation of the target pathogens. Bassiacridin and beauvericin produced by Beauveria have insecticidal property against entomopathogens (McGuire and Northfield, 2020); bioactive lipopeptides produced by Bacillus subtilis necrotizes insect epithelial cells causing death (Melo et al., 2016; Liu et al., 2019). Microbial antagonists also suppress pathogens through indirect mechanisms, notably through competition and induced systemic resistance (Heil and Bostock, 2002). Most antagonist microbes possess aggressive colonization ability suppressing the pathogens hindering their establishment through competition. This mode of action is incredibly effective in controlling necrotrophic pathogens that require exogenous nutrients for their establishment (Tewari et al., 2019). Trichoderma strains can produce siderophores and out-compete pathogens for iron, which is essential for the pathogens' normal physiology (Ahmed and Holmström, 2014). Some secondary metabolites produced by Trichoderma strains are associated with systemic resistance in Lycopersicon esculentum against Leptosphaeria macularis and Botrytis cinerea (Abbey et al., 2019). It is imperative to note that the antagonistic mechanisms are complex, and microbial BCAs may suppress a pathogen through several mechanisms. Synergistic effects of co-inoculation of certain BCAs have led to higher efficacy in field conditions (Köhl et al., 2019), which can be explored further in smallholder agroecosystems for more significant results.

      Microbial Functional Identity vs. Functional Diversity in Delivering Agroecosystem Services

      Soil microbial communities mediate nearly every biogeochemical process occurring on earth crust controlling the functionality of an ecosystem (Escalas et al., 2019). Their ubiquitous nature, diversity richness, and ability to establish multiple interactions with higher organisms and among themselves, make them the best candidates in delivery of essential agroecosystem services (Brussaard et al., 2007). Understanding the importance of having a specific functional species or group of PGPMs here referred to as “functional identity” or “functional diversity,” respectively (definitions adapted from Barberi, 2015) is not well-established in smallholder agroecosystems. This drives the rising research demand for soil biodiversity in the quest for the delivery of beneficial agroecosystem services. In the previous decades, most of the commercial inoculants contained a single microbial species or strain targeting a specific crop genotype (Kaminsky et al., 2019). Economically, this no longer favors the smallholder agroecosystems that are nowadays characterized by a wide range of crop production.

      Currently, through research, various microbial species and strain combinations have been produced targeting a broad range of crop species depending on the market requirement and species compatibility. For instance, SumaGrow® bioinoculant (Table 1) produced by Bio Soil Enhancers Inc. (USA) contains a consortium of polyfunctional PGPMs comprising of N fixers, P mobilizers and solubilizers, micronutrient mobilizers, growth hormones, and organic humic acid, and enhance growth and yield in a wide range of crops including vegetables, cereals, legumes, trees, and fruits (Preininger et al., 2018). Co-inoculation or mixed inoculation of diverse multifunctional microbial groups as a single inoculant could maximize the chances of strain functional performance (Escalas et al., 2019) in particular the functional biodiversity effect when functional identity effect is suppressed. For instance, a mixture of PGPMs that enhance P solubilization (e.g., Bacillus spp.), phytopathogenic biocontrol (e.g., Pseudomonas spp.), BNF (e.g., Rhizobium spp.), and phytohormone production (e.g., Azospirillum spp.) could have synergistic or additive functional biodiversity effect on crops (Hungria et al., 2015; Rashid et al., 2016). However, the performance of co-inoculation is not always the case as its efficiency is affected by several factors including strain compatibility, concentration ratios, inoculation methods, plant genotypes, soil factors, and environmental conditions at the time of application (Kaminsky et al., 2019). Considering all these factors and the changing climatic conditions, the performance of the current inoculants may not be guaranteed in the near future. Thus, research should be done to deepen the understanding of complex interactions associated with mixing various inoculants to come up with new formulations for use with different crops. Efficient delivery methods of inoculant application in the context of the changing climate should also be investigated.

      PGPMs Contribution to Crop Yield and Nutritional Quality

      Studies have shown that there are significant benefits of using PGPM inoculants as biofertilizers or biostimulants in crop production (Chavoshi et al., 2018; Aliyu et al., 2019; Santos et al., 2019). A global meta-analysis of biofertilizer efficiency in enhancing crop nutrients and yields showed an average of 16 % increase in yield of all crops, with legumes showing a superior response to inoculation (Schütz et al., 2018). The beneficial effects of bioinoculation could be more in nutrient-limited soil conditions which reflects the case of SSA smallholder agroecosystems. According to Singh et al. (2017), Rhizobium biofertilizer inoculum when applied in semiarid and arid environments can supplement nutrient requirement in legumes and hence improving crop yield. Chavoshi et al. (2018) reported a maximum biomass accumulation of 7,985 kg ha−1 in red beans and a higher water use efficiency after inoculation with Bio-P and Bio-K fertilizers in limited water resources. In desert areas of the Sahel region, double inoculation of indigenous rhizobia and AMF isolates improved the survival rate and growth of Vachellia seyal (acacia) plantations (Fofana et al., 2020). The authors attribute the improved plant growth to the adaptation of the native bioinoculants to the pedoclimatic conditions of the region and the microbial synergism in delivering plant nutrients under water and heat stress conditions. The fact that PGPM inoculants mitigate water stress in crops and enhance crop health and productivity ensures that there is consistency in yields for smallholder farmers.

      The use of effective PGPMs enhances leaf photosynthesis, seed quality traits, and yield of legumes such as Phaseolus vulgaris L.) (Iriti et al., 2019). High-quality agricultural products are easily marketable and fetch high prices, therefore, bringing more fortune to smallholder farmers resulting in improved livelihoods. The choice and selection of superior native strains over exotic strains is often encouraged (Aliyu et al., 2019). For instance, the application of native strains of Bacillus spp. as PGPM in the cultivation of cumin (Cuminum cyminum Linn.) increased the seed oil content and yields compared to uninoculated control (Mishra et al., 2019). Studies have revealed that it is economical for smallholder farmers to apply polyfunctional microbial inoculants with multiple plant growth-promoting traits such as P solubilization, N fixation, and biocontrol compared to the use of single-trait inoculants (Reddy and Saravanan, 2013). However, some studies favor the promotion of functional identity over functional diversity when dealing with specific crop genotypes and environments (Njeru et al., 2017). Further studies to elucidate this disparity should be done in the context of smallholder agroecosystems paying attention to proper management of microbial inoculants as this could significantly affect microbial functioning, abundance, and effectiveness.

      The global demand for healthy food and fiber is expected to rise by 2050 to 70% (Singh and Trivedi, 2017). The increase in food demand needs to be satisfied from the existing arable land, which is already under pressure from the rising human population, harsh climatic conditions, and the decline in soil fertility and water availability. In addition, there is a need to safeguard farm produce from emerging and re-emerging pests and diseases. Despite the success of chemically associated conventional farming practices in increasing agricultural productivity, their future reliability is on the balance due to various health concerns arising from food contamination and disease resistance (Alori and Babalola, 2018). Harnessing natural resources such as plant-associated microbiome (PAM) could be one of the most effective strategies to improve agricultural productivity and future food security in a more sustainable way. The PAM technology has a better potential to minimize environmental hazards and increase food quality and quantity while lessening resource inputs compared to the conventional farm practices. Additional plant-microbiome discoveries and technological improvements are emerging and embracing a shift in the paradigm toward next-generation microbial applications could lead to better food production systems (Nezhad et al., 2015). In situ plant-microbiome engineering, high throughput sequencing, and plant breeding will be integral to enhancing the understanding and development of efficient microbial inoculants. Evidence shows that more attention has been given to rhizosphere and root microbiota that play a key role in plant productivity (Goswami and Deka, 2020; Nuzzo et al., 2020; Sousa et al., 2020), while other plant sections such as leaf, stem, seeds, and flowers remains largely unexplored. Yet, they could be playing important roles in plant defense system and response against abiotic and biotic stress (Singh and Trivedi, 2017).

      Agronomic Management Practices and Interventions That Optimize PGPM Functionality

      Modern farming encourages the integration of bio-inoculants with other farm management practices and this has been shown to have complementary and synergistic effects in improving growth and yield quality characteristics in apple fruit farming (Mosa et al., 2018). The positive association between agronomic management practices and ecosystem functioning could be exploited to enhance soil fertility amelioration and plant productivity (Costanzo and Bàrberi, 2014). One possible approach is to increase the above-ground litter and below-ground root traits that host and provide energy to the PGPMs responsible for decomposition and nutrient recycling (Bakker et al., 2012). This approach encourages farmers to utilize agronomic practices that increase genetic, species, and habitat diversity within the field scale hence increasing farm's overall productivity and agroecosystem resilience (Moonen and Bàrberi, 2008; Mburu et al., 2016). Conserving a high diversity of indigenous microbial functional communities in the soil ensures continuous maintenance of critical soil functions amidst the changing climatic conditions. This could provide production-related insurance to the farmers on ecosystem productivity and stability upon any ecological perturbations (Yachi and Loreau, 1999; Shanafelt et al., 2015).

      Multiple cropping systems coupled with rotational practices is demonstrated to sequester more carbon to the soil (Hontoria et al., 2019). Obligate PGPMs, that would not survive without a plant host, utilize carbon as the sole energy source (Ventorino et al., 2012). Therefore, farmers should critically choose cropping systems that favor carbon sequestration in order to conserve the functioning of beneficial obligate microbial communities. However, for maximum benefits to be achieved in multiple cropping systems, choosing complementary plant genotypes known to host multiple beneficial PGPMs would be ideal. For instance, intercropping of cereals with legumes such as lentils, faba bean, and chickpea, which are considered (Faucon et al., 2017; Lazzaro et al., 2018). Cereal-legume intercropping system creates a microclimate that regulates heat stress, moisture, wind stress, weed and pest infestation (Lazzaro et al., 2018). The use of PGPMs can enhance the interspecific plant-microbial interactions in intercropping system (Figure 3). The addition of organic amendments such as vermicompost, manure, and biochar that are rich in PGPMs and nutrients would help to sustain high energy demanding soil processes and promotes microbial decomposition and nutrient recycling (Cobb et al., 2018; Nyamwange et al., 2018; Koskey et al., 2020). Non-chemical weeding and pest control methods promote the build-up of beneficial plant-soil biodiversity which are considered the main drivers of an ecosystem (Marzaioli et al., 2010). On the contrary, intensive cultivation, a common practice in smallholder agroecosystems, reduces soil biodiversity, organic matter, and increase CN ratio, therefore, reducing the overall microbial functionality (Ventorino et al., 2012). Therefore, a change in cultivation practices to more sustainable agroecological practices in smallholder systems would be inevitable if food security is to be realized.

      Plants are considered naturally as selective agents that continuously shape rhizospheric soil microbiome and rhizosphere engineering is slowly emerging as a new research field to potentially address crop production (Haldar and Sengupta, 2015). AMF are important ecosystem promoters and are recognized as key elements in low-input agroecosystems; however, their structural composition, diversity and performance are highly influenced by plant genotype (López-García et al., 2017). Certain plant taxonomic families are known to be poor AMF hosts while others such as legumes are known to be excellent AMF hosts. A few plant taxa are non-host. Currently, plants are selectively bred to produce root exudates that enhance rhizosphere plant-microbiome interactions and possibly promote agroecosystem sustainability and productivity (Bakker et al., 2012). To embrace this strategy and apply in smallholder agroecosystems, it will require farmers no infrastructural changes other than the selection of their preferred crop cultivars or species bred to enhance root exudation. However, more knowledge in this area should be generated to deepen the understanding of their mechanisms, pros and cons, cost-benefit analysis, and their applicability to resource-strained smallholder farmers. Enhancing farmers' knowledge of agroecosystem functionality would optimize soil fertility restoration successes, agroecosystem sustainability, and crop productivity.

      Development of Microbial Inocula for Smallholder Farmers

      Currently, there is a rising global market demand for microbial inoculants that can be used as biofertilizers or biostimulants in crop production (Lobo et al., 2019). Bioinoculants contain one or more PGPMs (bacteria, algae, or fungi) packaged in a carrier material. A carrier material refers to the delivery “vehicle” that is packaged to transfer the bioinoculum to the plant rhizosphere. It determines the form (either liquid or solid), shelf life, and the application or delivery methods of the microbial inoculant (Reddy and Saravanan, 2013). According to Soumare et al. (2020), a good microbial inoculum should be packaged in a carrier material that provides an optimum microenvironment (pH, water, and carbon content) for microorganisms, maintain longer shelf life and microbial viability without the need for a special storage facility. Besides, the carrier material should be cost-effective, readily available, eco-friendly, acquiescent to nutrient supplement, and not harmful to the user (Alori and Babalola, 2018). It is interesting to note that very few studies have focused on the selection and development of carrier material and their effect on bio-inoculum as most studies emphasize on the performance of microbial strains (Herrmann and Lesueur, 2013). Encapsulation of bioinoculants is a newly emerging technique that utilizes polymer beads to enclose one or more microbial species. This technique allows the incorporation of other organic bio-effectors such as humic acid and strigolactones, protects the microbial life from desiccation, and allows slow release of the components into the soil (Gouda et al., 2018). Despite its biotechnological potentials as bioinoculant carriers, nano- and micro-encapsulation methods have not been exploited commercially particularly by entities targeting smallholder systems (Herrmann and Lesueur, 2013). Therefore, with advancing technologies, more studies that could lead to the development of versatile carrier inoculants suitable for use in smallholder agroecosystems should be done.

      The fact that the majority of microbial inoculants in SSA are imported (Babalola and Glick, 2012) raises a question if they are tailored to match the varying smallholder farmers' agroecosystems, shelf-life needs, local storage, and soil conditions. A short inoculant shelf-life constraints inoculant supply chain and significantly reduces inoculant reliability, viability, and availability (Deaker et al., 2012). Inoculant viability determines the success of its use and continuous adoption by the farmers, who are in most cases production-oriented rather than agroecology conservationists. Therefore, effective bioinoculants should be able to competitively and successfully establish themselves in the soil within the shortest time possible amidst the presence of already established native microbes. Various studies have tried to unveil the fate of microbial inoculum and their effect on the native microbial communities upon their introduction into the soil (Sharma et al., 2012). For instance, Nuzzo et al. (2020) demonstrated that some PGPM formulations have no impact on plant growth but significantly affect the diversity and structure of native microbial communities. On the contrary, PGPM inoculation improved plant growth but had no influence on species diversity and richness of native microbes in the host plant roots (Piromyou et al., 2011). These inconsistencies are likely to be common in smallholder agroecosystems and, therefore, calls for selection and development of microbial strains that interact well with native microbial communities.

      Soil conditions such as pH, presence of organic matter, water availability, and other physicochemical properties affect the infectivity of microbial inoculants (Njeru et al., 2020; Saad et al., 2020). Some PGPM inoculants can confer resilience against such harsh local environmental conditions (Agami et al., 2016). This explains why microbial inoculants are recommended even in soils with less water and where most nutrients are immobile (Sindhu et al., 2020). In some instances, seed companies and researchers have solved this challenge by producing crop cultivars that customarily favor colonization of specific PGPMs under a wide range of soil conditions (Faye et al., 2020). Through this approach, Gitonga et al. (2021) investigated how organic and conventional smallholder farming systems and soybean cultivars (promiscuous vs. non-promiscuous) affect native Bradyrhizobium spp. diversity. Similarly, Sinong et al. (2021) found P-solubilizing microbial isolates that could be exploited to enhance the growth of two rice cultivars under low-input cultivation than conventional practices. The authors aimed at optimizing smallholder agroecosystem at the farm level that potentially harbor diverse soil microbiota that enhances crop productivity.

      In other cases, seed manufacturers have partnered with farmers to establish ‘custom seed inoculation’ where on farmer's request, seeds are inoculated with specific PGPMs by the manufacturer prior to packaging and delivery to the farmers for planting (Deaker et al., 2012). These two approaches can be easily replicated in smallholder agroecosystems, but more research and partnerships on bioprospecting for effective PGPMs compatible with various local crop cultivars should be initiated. Researchers should keep in mind the need for new PGPM inoculants adapted to the current and incoming stressful climatic conditions as the future performance of the inoculants currently in the market may not be guaranteed.

      Challenges of Widespread Utilization of PGPMs in Smallholder Agroecosystems

      Notwithstanding their importance in upscaling agriculture, the use of PGPM inoculants in smallholder settings is largely unaccountable (Oruru and Njeru, 2016) and more research should focus on quantifying their use, adoption, and their overall effect on soil, crops, and farmers' livelihood. Farmers are used to the application of ‘blanket’ solutions in solving their day-to-day field challenges and the adoption of particular techniques providing specific solutions in certain locations should be encouraged. Industrially, there is a challenge in the production of bioinoculants that could be used for a broad range of crops grown in geographically and climatically diverse territories (Santos et al., 2019). PGPMs, unlike the broad-spectrum agrochemicals, are highly selective in their use and only target specific plant hosts. Their viability is short and the cost of maintaining PGPMs during storage is very high especially in rural setups where electricity and modern storage facilities are limiting resources (Tabassum et al., 2017). Thus, the search for innovative microbial solutions based on farmers' needs should be done with geographical considerations, increasing episodes of climatic and environmental stresses.

      The risk of toxicity arising from inoculant contamination is high if proper quality control standards and storage measures are not taken into consideration. Raimi et al. (2019) reported 67% of the South African biofertilizers, analyzed through sequencing, showed high levels of toxins and contaminants affecting the quality of the inoculants, therefore, jeopardizing their potential benefits. The intentional movement of bioinoculants containing various exotic microbial species or strains to new agroecosystems is growing, but the possible negative ecological consequence of their introduction is poorly understood (Schwartz et al., 2006). This may lead to unintended negative invasion and the establishment of microbes in new agroecosystems. Non-sterile and contaminated inoculum can result in the emergence of phytopathogens that are parasitic to the native PGPMs and plants and can potentially cause significant crop losses. Controlling the cases of invasive species would be costly to the farmers and thus, the need for inoculation particularly with imported inoculants should first be carefully evaluated and where possible, the use of high-quality local indigenous species should be recommended. In some of the African countries where economic and technological policies have been put in place to support the use of biofertilizers, there is hardly any evidence of the successful implementation of the approaches. This failure is linked to financial misappropriation, policy management and lack of investment interest among the stakeholders (Abdullah and Samah, 2013). Additionally, unreliable climatic conditions, variation in soil factors and poor agronomic management practices need to be addressed especially in the SSA region where the impact of bio-inoculation would be profound if fully adopted (Ngetich et al., 2012).

      Future Perspectives

      The increasing demand for safe food and better nutrition, advancing research technologies, and interest in sustainable agriculture has further renewed global interest on PGPM bioinoculants. For instance, by 2019, China registered more than 800 inoculant related patents while India surpassed 100 patents (Santos et al., 2019). Therefore, it is expected that, through advanced research innovations, more bioinoculants will be produced in the following years. The effects of climate change present a major challenge to industrial bioinoculant producers, and research on PGPMs that are more effective under a broader range of stressful conditions and induce plant tolerance would increase. The challenges on microbial shelf life, storage and viability losses should be addressed and new technologies of seed coating that deliver stable formulations able to withstand harsh storage conditions should be developed (Bargaz et al., 2018). Plant breeders, seed producers, and farmers could overcome these challenges through the initiation of “tailor-made” products that could address specific challenges. However, further scientific research and economic benefit analysis in this area should be done.

      More knowledge and deeper understanding are needed on how agronomic practices under changing climatic conditions affect the composition, abundance, and bio-functionality of PGPMs in delivering multiple agroecosystem services. Farmers need to know how PGPM communities are managed at spatial and temporal scale to promote synergies, effectiveness, and avoid trade-offs. Fostering proximity to smallholder farmers in redesigning agroecosystems and policy making should be prioritized. This can be achieved by involving them in-field research demonstrations, data collection, reporting, and policy recommendation drafting (IFAD and UNEP, 2013). These approaches will enhance farmers' knowledge and technological capacity in the use of bio-inoculants, therefore, ensuring a continuous adoption of techniques that take into account their local ecological conditions and knowledge.

      Conclusion

      The use of PGPMs as biostimulants, biofertilizers, or biocontrol agents by smallholder farmers has substantially grown owing to their impressive performance, economic benefits, and environmental safety associated with their use. They provide beneficial agroecosystem services such as soil nutrient amelioration, crop nutrient, and yield improvement, plant tolerance to biotic and abiotic stresses, biocontrol of pests and diseases, and water uptake. The adoption of PGPMs in smallholder agroecosystems is on the rise with the increasing number of patents and new inoculants being observed in developing countries. Multisectoral research on the use of PGPMs involving smallholder farmers is encouraged and its output should capture the aims of both the “productionist” and “agroecologist” paradigms. More knowledge on the effects of climate change and agronomic practices on the bio-functionality of PGPMs in delivering multiple agroecosystem services should be generated. Robust technologies are needed to enhance the PGPM production and most importantly to improve the effectiveness, stability, and reliability of the products under environmentally stressing conditions. Putting into consideration the collective experience, needs, and indigenous knowledge of smallholder farmers, PGPM inoculation could be a key pillar in addressing SDG 2 goal of ending hunger, promoting food security, and environmental sustainability.

      Author Contributions

      GK drafted the outline structure and prepared the manuscript with contributions from SM and RA. EN and JM provided technical guidelines and reviews during manuscript preparation. All authors approved the final draft of the manuscript for submission.

      Conflict of Interest

      The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

      The authors acknowledge the smallholder farmers from Tharaka Nithi County, Kenya and the Kenyatta University FLAIR research team (Nairobi) led by EN for their collaboration and in provision of supporting materials included in this manuscript.

      References Abbey J. A. Percival D. Abbey L.ord, Asiedu S. K. Prithiviraj B. Schilder A. (2019). Biocontrol science and technology biofungicides as alternative to synthetic fungicide control of grey mould (Botrytis cinerea)-prospects and challenges. Biocontrol Sci. Technol. 29, 241262. 10.1080/09583157.2018.1548574 Abdel Latef A. A. H. Abu Alhmad M. F. Kordrostami M. Abo–Baker A. B. A. E. Zakir A. (2020). Inoculation with azospirillum lipoferum or azotobacter chroococcum reinforces maize growth by improving physiological activities under saline conditions. J. Plant Growth Regul. 39, 12931306. 10.1007/s00344-020-10065-9 Abdel-Rahman H. M. Salem A. A. Moustafa M. M. A. Hoda El-Garhy, A. S. (2017). A novice Achromobacter sp. EMCC1936 strain acts as a plant-growth-promoting agent. Acta Physiol. Plant. 39:61. 10.1007/s11738-017-2360-6 Abdullah F. A. Samah B. A. (2013). Factors impinging farmers' use of agriculture technology article in asian social science. Asian Soc. Sci. 9, 120124. 10.5539/ass.v9n3p120 Abo-Zaid G. A. Matar S. M. Abdelkhalek A. (2020). Induction of plant resistance against tobacco mosaic virus using the biocontrol agent streptomyces cellulosae isolate actino 48. Agronomy 10, 116. 10.3390/agronomy10111620 Adeyemi N. O. Atayese M. O. Olubode A. A. Akan M. E. (2019). Effect of commercial arbuscular mycorrhizal fungi inoculant on growth and yield of soybean under controlled and natural field conditions. J. Plant Nutr. 10.1080/01904167.2019.1685101 Agami R. Abd El Khalek Abd El Mola I. A A. R. Medani R. Abd El-Mola I. Taha R. (2016). Exogenous application with plant growth promoting rhizobacteria (PGPR) or proline induces stress tolerance in basil plants (Ocimum basilicum L.) exposed to water stress. Int. J. Environ. Agric. Res. 2, 7892. Available online at: https://www.researchgate.net/publication/308984083 Ahemad M. Kibret M. (2014). Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. J. King Saud Univ. Sci. 26, 120. 10.1016/j.jksus.2013.05.001 Ahmed E. Holmström S. J. M. (2014). Siderophores in environmental research: roles and applications. Microb. Biotechnol. 7, 196208. 10.1111/1751-7915.1211724576157 Aliyu I. A. Yusuf A. A. Atta A. (2019). Evaluation of indigenous rhizobial isolates in search for candidate strain for commercial production. Bayero J. Pure Appl. Sci. 11:33. 10.4314/bajopas.v11i1.5S Alori E. T. Babalola O. O. (2018). Microbial inoculants for improving crop quality and human health in Africa. Front. Microbiol. 9:2213. 10.3389/fmicb.2018.0221330283427 Altieri M. A. Funes-Monzote F. R. Petersen P. (2012). Agroecologically efficient agricultural systems for smallholder farmers: contributions to food sovereignty. Agron. for Sust. Dev. 32, 113. 10.1007/s13593-011-0065-6 Arthurs S. Heinz K. M. (2006). Biocontrol science and technology evaluation of the nematodes steinernema feltiae and thripinema nicklewoodi as biological control agents of western flower thrips frankliniella occidentalis infesting chrysanthemum. Biocontrol Sci. Technol. 16, 141155. 10.1080/09583150500258545 Aseri G. K. Jain N. Tarafdar J. C. (2009). Hydrolysis of organic phosphate forms by phosphatases and phytase producing fungi of arid and semi arid soils of India. Am. Euras. J. Agric. Environ. Sci. 5, 564570. Available online at: https://www.researchgate.net/publication/278679570 Avio L. Turrini A. Giovannetti M. Sbrana C. (2018). Designing the ideotype mycorrhizal symbionts for the production of healthy food. Front. Plant Sci. 9:1089. 10.3389/fpls.2018.0108930154803 Azizoglu U. (2019). Bacillus thuringiensis as a biofertilizer and biostimulator: a mini-review of the little-known plant growth-promoting properties of Bt. Curr. Microbiol. 76, 13791385. 10.1007/s00284-019-01705-931101973 Babalola O. O. Glick B. R. (2012). The use of microbial inoculants in African agriculture: current practice and future prospects. J. Food Agric. Environ. 10, 540549. https://www.researchgate.net/publication/260934217 Bado B. V. Sedogo M. Lompo F. Maman Laminou S. M. (2018). Biological nitrogen fixation by local and improved genotypes of cowpea in burkina faso (West Africa): total nitrogen accumulated can be used for quick estimation. Adv. Agric. 2018, 18. 10.1155/2018/9641923 Bakker M. G. Manter D. K. Sheflin A. M. Weir T. L. Vivanco J. M. (2012). Harnessing the rhizosphere microbiome through plant breeding and agricultural management. Plant Soil 360, 113. 10.1007/s11104-012-1361-x Barberi P. (2015). Functional biodiversity in organic systems: the way forward? Sust Agric Res. 4:26. 10.5539/sar.v4n3p26 Bargaz A. Lyamlouli K. Chtouki M. Zeroual Y. Dhiba D. (2018). Soil microbial resources for improving fertilizers efficiency in an integrated plant nutrient management system. Front. Microbiol. 9:1606. 10.3389/fmicb.2018.01606 Bationo A. Hartemink A. Lungu O. Naimi M. Okoth P. Smaling E. . (2012). “Knowing the African soils to improve fertilizer recommendations,” in Improving Soil Fertility Recommendations in Africa Using the Decision Support System for Agrotechnology Transfer (DSSAT), eds J. Kihara, D. Fatondji, J. Jones, G. Hoogenboom, R. Tabo, and A. Bationo (Dordrecht: Springer), 1942. 10.1007/978-94-007-2960-5_3 Bonner M. R. Alavanja M. C. R. (2017). Pesticides, human health, and food security. Food Energy Secur. 6, 8993. 10.1002/fes3.112 Browne P. Rice O. Miller S. H. Burke J. Dowling D. N. Morrissey J. P. . (2009). Superior inorganic phosphate solubilization is linked to phylogeny within the pseudomonas fluorescens complex. Appl. Soil Ecol. 43, 131138. 10.1016/j.apsoil.2009.06.010 Brussaard L. de Ruiter P. C. Brown G. G. (2007). Soil biodiversity for agricultural sustainability. Agric. Ecosyst. Environ. 121, 233244. 10.1016/j.agee.2006.12.013 Carlson R. Tugizimana F. Steenkamp P. A. Dubery I. A. Hassen A. I. Labuschagne N. (2020). Rhizobacteria-induced systemic resilience in Sorghum bicolor (L.) moench against Fusarium pseudograminearum crown rot under drought stress conditions. Biol. Control 151:104395. 10.1016/j.biocontrol.2020.104395 Celador-Lera L. Jiménez-Gómez A. Menéndez E. Rivas R. (2018). “Biofertilizers based on bacterial endophytes isolated from cereals: potential solution to enhance these crops,” in Role of Rhizospheric Microbes in Soil: Stress Management and Agricultural Sustainability, Vol. 1 (Singapore: Springer), 175203. 10.1007/978-981-10-8402-7_7 Chavoshi S. Nourmohamadi G. Madani H. Abad H. H. S. Fazel M. A. (2018). The effects of biofertilizers on physiological traits and biomass accumulation of red beans (Phaseolus vulgaris cv.Goli) under water stress. Iran. J. Plant Physiol. 8, 25552562. 10.22034/IJPP.2018.543427 Choudhary D. K. Varma A. (2017). “Nitrogenase (a Key Enzyme): Structure and Function,” in Rhizobium Biology and Biotechnology. Soil Biology, eds A. Hansen, D. Choudhary, P. Agrawal, and A. Varma (Cham: Springer), 293307. 10.1007/978-3-319-64982-5_14 Cobb A. B. Wilson G. W. T. Goad C. L. Grusak M. A. (2018). Influence of alternative soil amendments on mycorrhizal fungi and cowpea production. Heliyon 4:e00704. 10.1016/j.heliyon.2018.e0070430094374 Coniglio A. Mora V. Puente M. Cassán F. (2019). “Azospirillum as biofertilizer for sustainable agriculture: azospirillum brasilense AZ39 as a model of PGPR and field traceability,” in Microbiol Probiotics for Agricultural Systems, eds D. Zúñiga-Dávila, F. González-Andrés, and E. Ormeño-Orrillo (Cham: Springer), 4570. 10.1007/978-3-030-17597-9_4 Constantine K. L. Kansiime M. K. Mugambi I. Nunda W. Chacha D. Rware H. . (2020). Why don't smallholder farmers in Kenya use more biopesticides? Pest Manage. Sci. 76, 36153625. 10.1002/ps.589632400959 Costanzo A. Bàrberi P. (2014). Functional agrobiodiversity and agroecosystem services in sustainable wheat production. A review. Agron. Sust. Dev. 34, 327348. 10.1007/s13593-013-0178-1 Dakora F. D. Matiru V. N. Kanu A. S. (2015). Rhizosphere ecology of lumichrome and riboflavin, two bacterial signal molecules eliciting developmental changes in plants. Front. Plant Sci. 6:700. 10.3389/fpls.2015.0070026442016 Dawwam G. E. Elbeltagy A. Emara H. M. Abbas I. H. Hassan M. M. (2013). Beneficial effect of plant growth promoting bacteria isolated from the roots of potato plant. Ann. Agric. Sci. 58, 195201. 10.1016/j.aoas.2013.07.007 Deaker R. Hartley E. Gemell G. (2012). Conditions affecting shelf-life of inoculated legume seed. Agriculture 2, 3851. 10.3390/agriculture2010038 Ding B. Zhang X. Xu Y. An L. Liu X. Su Q. (2020). The bacterial potassium transporter gene MbtrkH improves K+ uptake in yeast and tobacco. PLoS ONE 15:e036246. 10.1371/journal.pone.023624632804956 Dissanayaka D. M. S. B. Plaxton W. C. Lambers H. Siebers M. Marambe B. Wasaki J. (2018). Molecular mechanisms underpinning phosphorus-use efficiency in rice. Plant Cell Environ. 41, 14831496. 10.1111/pce.1319129520969 Draghi W. O. María P. Del F. Barsch A. Albicoro F. J. Lozano M. J. . (2017). A metabolomic approach to characterize the acid-tolerance response in Sinorhizobium meliloti. Metabolomics. 1, 71. Egamberdiyeva D. (2007). The effect of plant growth promoting bacteria on growth and nutrient uptake of maize in two different soils. Appl. Soil Ecol. 36, 184189. 10.1016/j.apsoil.2007.02.005 Elagib N. A. Al-Saidi M. (2020). Balancing the benefits from the water–energy–land–food nexus through agroforestry in the Sahel. Sci. Total Environ. 742:140509. 10.1016/j.scitotenv.2020.14050933167296 Escalas A. Hale L. Voordeckers J. W. Yang Y. Firestone M. K. Alvarez-Cohen L. . (2019). Microbial functional diversity: from concepts to applications. Ecol. Evolut. 9, 1200012016. 10.1002/ece3.567031695904 Etesami H. Alikhani H. A. Hosseini H. M. (2015). Indole-3-acetic acid (IAA) production trait, a useful screening to select endophytic and rhizosphere competent bacteria for rice growth promoting agents. MethodsX. 2, 7278. 10.1016/j.mex.2015.02.00826150974 FAO (2018). Tracking Progress on Food and Agriculture-Related SDG Indicators A Report on the Indicators Under FAO Custodianship. Available online at: http://www.fao.org/sdg-progress-report/en/ Faucon M. P. Houben D. Lambers H. (2017). Plant functional traits: soil and ecosystem services. Trends Plant Sci. 22, 385394. 10.1016/j.tplants.2017.01.00528209328 Faye A. Stewart Z. P. Ndung'u-Magiroi K. Diouf M. Ndoye I. Diop T. . (2020). testing of commercial inoculants to enhance p uptake and grain yield of promiscuous soybean in Kenya. Sustainability 12:3803. 10.3390/su12093803 Fofana B. Sacande M. Blagna F. Dibloni T. O. Compaore E. Sanon K. B. . (2020). Boosting land restoration success in the great green wall through the use of symbiotic microorganisms for propagated tree seedlings. Int. J. Biol. Chem. Sci. 14, 110125. 10.4314/ijbcs.v14i1.10 Fukami J. Cerezini P. Hungria M. (2018a). Azospirillum: benefits that go far beyond biological nitrogen fixation. AMB Express 8:73. 10.1186/s13568-018-0608-129728787 Fukami J. Ollero F. J. de la Osa C. Megías M. Hungria M. (2018b). Co-inoculation of maize with azospirillum brasilense and rhizobium tropici as a strategy to mitigate salinity stress. Funct. Plant Biol. 45, 328. 10.1071/FP1716732290956 Gabasawa A. I. (2020). “Prospects for developing effective and competitive native strains of rhizobium inoculants in Nigeria,” in Current Microbiological Research in Africa, eds A. Abia and G. Lanza (Cham: Springer), 223256. 10.1007/978-3-030-35296-7_9 Gamez R. Cardinale M. Montes M. Ramirez S. Schnell S. Rodriguez F. (2019). Screening, plant growth promotion and root colonization pattern of two rhizobacteria (pseudomonas fluorescens Ps006 and Bacillus amyloliquefaciens Bs006) on banana cv. Williams (Musa acuminata Colla). Microbiol. Res. 220, 1220. 10.1016/j.micres.2018.11.00630744815 Giller K. E. Kanampiu F. Hungria M. Vanlauwe B. (2019). The role of nitrogen fixation in African smallholder agriculture. Agric. Ecosyst. Environ. 285:106601. 10.1016/j.agee.2019.106601 Giovannini L. Palla M. Agnolucci M. Avio L. Sbrana C. Turrini A. . (2020). Arbuscular mycorrhizal fungi and associated microbiota as plant biostimulants: research strategies for the selection of the best performing inocula. Agronomy 10:106. 10.3390/agronomy10010106 Gitonga N. M. Njeru E. M. Cheruiyot R. Maingi J. M. (2021). Genetic and morphological diversity of indigenous bradyrhizobium nodulating soybean in organic and conventional family farming systems. Front. Sust. Food Syst. 4:606618. 10.3389/fsufs.2020.606618 Goswami M. Deka S. (2020). Plant growth-promoting rhizobacteria—alleviators of abiotic stresses in soil: a review. Pedosphere 30, 4061. 10.1016/S1002-0160(19)60839-8 Gouda S. Kerry R. G. Das G. Paramithiotis S. Shin H. S. Patra J. K. (2018). Revitalization of plant growth promoting rhizobacteria for sustainable development in agriculture. Microbil. Res. 206, 131140. 10.1016/j.micres.2017.08.01629146250 Grover M. Ali S. Z. Sandhya V. Rasul A. Venkateswarlu B. (2011). Role of microorganisms in adaptation of agriculture crops to abiotic stresses. World J. Microbiol. Biotechnol. 27, 12311240. 10.1007/s11274-010-0572-7 Guo D. J. Singh R. K. Singh P. Li D. P. Sharma A. Xing Y. X. . (2020). Complete genome sequence of enterobacter roggenkampii ED5, a nitrogen fixing plant growth promoting endophytic bacterium with biocontrol and stress tolerance properties, isolated from sugarcane root. Front. Microbiol. 11:580081. 10.3389/fmicb.2020.58008133072048 Guo Q. Li Y. Lou Y. Shi M. Jiang Y. Zhou J. . (2019). Bacillus amyloliquefaciens Ba13 induces plant systemic resistance and improves rhizosphere microecology against tomato yellow leaf curl virus disease. Appl. Soil Ecol. 137, 154166. 10.1016/j.apsoil.2019.01.015 Gupta V. V. S. R. Zhang B. Penton C. R. Yu J. Tiedje J. M. (2019). Diazotroph diversity and nitrogen fixation in summer active perennial grasses in a mediterranean region agricultural soil. Front. Mol. Biosci. 6:115. 10.3389/fmolb.2019.0011531750314 Gururani M. A. Upadhyaya C. P. Baskar V. Venkatesh J. Nookaraju A. Park S. W. (2013). Plant growth-promoting rhizobacteria enhance abiotic stress tolerance in solanum tuberosum through inducing changes in the expression of ROS-scavenging enzymes and improved photosynthetic performance. J. Plant Growth Regul. 32, 245258. 10.1007/s00344-012-9292-6 Haldar S. Sengupta S. (2015). Plant-microbe cross-talk in the rhizosphere: insight and biotechnological potential. Open Microbiol. J. 9, 17. 10.2174/187428580150901000125926899 Harrison R. D. Thierfelder C. Baudron F. Chinwada P. Midega C. Schaffner U. . (2019). Agro-ecological options for fall armyworm (Spodoptera frugiperda JE Smith)management: Providing low-cost, smallholder friendly solutions to an invasive pest. J. Environ. Manage. 243, 318330. 10.1016/j.jenvman.2019.05.01131102899 Hatting J. L. Moore S. D. Malan A. P. (2019). Microbial control of phytophagous invertebrate pests in South Africa: current status and future prospects. J. Invertebr. Pathol. 165, 5466. 10.1016/j.jip.2018.02.004 Heil M. Bostock R. M. (2002). Induced systemic resistance (ISR) against pathogens in the context of induced plant defences. Ann. Bot. 89, 503512. 10.1093/aob/mcf07612099523 Herrero M. Thornton P. K. Power B. Bogard J. R. Remans R. Fritz S. . (2017). Farming and the geography of nutrient production for human use: a transdisciplinary analysis. Lancet Planet. Health 1, e33e42. 10.1016/S2542-5196(17)30007-428670647 Herrmann L. Lesueur D. (2013). Challenges of formulation and quality of biofertilizers for successful inoculation. Appl. Microbiol. Biotechnol. 97, 88598873. 10.1007/s00253-013-5228-824037408 Hontoria C. García-González I. Quemada M. Roldán A. Alguacil M. M. (2019). The cover crop determines the AMF community composition in soil and in roots of maize after a ten-year continuous crop rotation. Sci. Total Environ. 660, 913922. 10.1016/j.scitotenv.2019.01.09530743976 Hungria M. Nogueira M. A. Araujo R. S. (2015). Soybean Seed Co-Inoculation with Bradyrhizobium spp. and Azospirillum brasilense: A New Biotechnological Tool to Improve Yield and Sustainability. American Journal of Plant Sciences. 6, 811817. 10.4236/ajps.2015.66087 IFAD UNEP (2013). Smallholders, Food Security and the Environment. Available online at: https://www.ifad.org/documents/38714170/39135645/smallholders_report.pdf/133e8903-0204-4e7d-a780-bca847933f2e Iriti M. Scarafoni A. Pierce S. Castorina G. Vitalini S. (2019). Soil application of effective microorganisms (EM) maintains leaf photosynthetic efficiency, increases seed yield and quality traits of bean (Phaseolus vulgaris L.) plants grown on different substrates. Int. J. Mol. Sci. 20:2327. 10.3390/ijms2009232731083418 Jaiswal D. K. Verma J. P. Prakash S. Meena V. S. Meena R. S. (2016). “Potassium as an important plant nutrient in sustainable agriculture: a state of the art,” in Potassium Solubilizing Microorganisms for Sustainable Agriculture, eds V. Meena, B. Maurya, J. Verma, and R. Meena (Springer), 2129. 10.1007/978-81-322-2776-2_2 Jiménez-Gómez A. Celador-Lera L. Fradejas-Bayón M. Rivas R. (2017). Plant probiotic bacteria enhance the quality of fruit and horticultural crops. AIMS Microbiol. 3, 483501. 10.3934/microbiol.2017.3.48331294172 Kalayu G. (2019). Phosphate solubilizing microorganisms: Promising approach as biofertilizers. Int. J. Agron. 2019:4917256. 10.1155/2019/4917256 Kaminsky L. M. Trexler R. V. Malik R. J. Hockett K. L. Bell T. H. (2019). The Inherent conflicts in developing soil microbial inoculants. Trends Biotechnol. 37, 140151. 10.1016/j.tibtech.2018.11.01130587413 Kannahi M. Senbagam N. (2014). Studies on siderophore production by microbial isolates obtained from rhizosphere soil and its antibacterial activity. J. Chem. Pharmaceut. Res. 6, 11421145. Available online at: http://jocpr.com/vol6-iss4-2014/JCPR-2014-6-4-1142-1145.pdf Kavoo-Mwangi A. M. Kahangi E. M. Ateka E. Onguso J. Mukhongo R. W. Mwangi E. K. . (2013). Growth effects of microorganisms based commercial products inoculated to tissue cultured banana cultivated in three different soils in Kenya. Appl. Soil Ecol. 64, 152162. 10.1016/j.apsoil.2012.12.002 Kawaka F. Dida M. M. Opala P. A. Ombori O. Maingi J. Osoro N. . (2014). Symbiotic Efficiency of Native Rhizobia Nodulating Common Bean (Phaseolus vulgaris L. ) in Soils of Western Kenya. Int. Sch. Res. Notices 2014, 18. 10.1155/2014/25849727355005 Kebede E. (2020). Grain legumes production and productivity in Ethiopian smallholder agricultural system, contribution to livelihoods and the way forward. Cogent Food Agric. 6:1722353. 10.1080/23311932.2020.1722353 Kermah M. Franke A. C. Adjei-Nsiah S. Ahiabor B. D. K. Abaidoo R. C. Giller K. E. (2018). N2-fixation and N contribution by grain legumes under different soil fertility status and cropping systems in the Guinea savanna of northern Ghana. Agric. Ecosyst. Environ. 261, 201210. 10.1016/j.agee.2017.08.02829970948 Khalid M. Hassani D. Bilal M. Asad F. Huang D. (2017). Influence of bio-fertilizer containing beneficial fungi and rhizospheric bacteria on health promoting compounds and antioxidant activity of Spinacia oleracea L. Botan. Stud. 58:35. 10.1186/s40529-017-0189-3 Kiss L. (2008). Intracellular mycoparasites in action: interactions between powdery mildew fungi and ampelomyces. Br. Mycol. Soc. Sympo. Ser. 27, 3752. 10.1016/S0275-0287(08)80045-8 Köhl J. Kolnaar R. Ravensberg W. J. (2019). Mode of action of microbial biological control agents against plant diseases: relevance beyond efficacy. Front. Plant Sci. 10:845. 10.3389/fpls.2019.0084531379891 Koskey G. Avio L. Lazzaro M. Pellegrini F. Sbrana C. Turrini A. . (2020). Smart use of microbial-rich vermicomposting to enhance tripartite plant-microbe-soil interactions. EGU Gen. Assemb. 2020, 12. 10.5194/egusphere-egu2020-3345 Koskey G. Mburu S. W. Kimiti J. M. Ombori O. Maingi J. M. Njeru E. M. (2018). Genetic characterization and diversity of rhizobium isolated from root nodules of mid-altitude climbing bean (Phaseolus vulgaris L.) varieties. Front. Microbiol. 9:968. 10.3389/fmicb.2018.0096829867872 Koskey G. Mburu S. W. Njeru E. M. Kimiti J. M. Ombori O. Maingi J. M. (2017). Potential of native rhizobia in enhancing nitrogen fixation and yields of climbing beans (Phaseolus vulgaris L.) in contrasting environments of eastern Kenya. Front. Plant Sci. 8:443. 10.3389/fpls.2017.0044328408912 Kristek S. Kristek A. Guberac V. Stanisavljevi,ć A. (2006). Effect of bacterium Pseudomonas fluorescens and low fungicide dose seed treatments on parasite fungus Aphanomyces cochlioides and sugar beet yield and. Plant Soil Environ. 52, 314320. 10.17221/3447-PSE Kuivanen K. S. Alvarez S. Michalscheck M. Adjei-Nsiah S. Descheemaeker K. Mellon-Bedi S. . (2016). Characterising the diversity of smallholder farming systems and their constraints and opportunities for innovation: a case study from the Northern Region, Ghana. NJAS Wagen. J. Life Sci. 78, 153166. 10.1016/j.njas.2016.04.003 Kumari P. Meena M. Gupta P. Dubey M. K. Nath G. Upadhyay R. S. (2018). Plant growth promoting rhizobacteria and their biopriming for growth promotion in mung bean (Vigna radiata (L.) R. Wilczek). Biocatal. Agric. Biotechnol. 16, 163171. 10.1016/j.bcab.2018.07.030 Kumawat K. C. Sharma P. Sirari A. Singh I. Gill B. S. Singh U. . (2019). Synergism of Pseudomonas aeruginosa (LSE-2) nodule endophyte with Bradyrhizobium sp. (LSBR-3) for improving plant growth, nutrient acquisition and soil health in soybean. World J. Microbiol. Biotechnol. 35:47. 10.1007/s11274-019-2622-030834977 Kushwaha P. Kashyap P. L. Kuppusamy P. Srivastava A. K. Tiwari R. K. (2020). Functional characterization of endophytic bacilli from pearl millet (Pennisetum glaucum) and their possible role in multiple stress tolerance. Plant Biosyst. 154, 503514. 10.1080/11263504.2019.1651773 Lazzaro M. Costanzo A. Bàrberi P. (2018). Single vs multiple agroecosystem services provided by common wheat cultivar mixtures: weed suppression, grain yield and quality. Field Crops Res. 221, 277297. 10.1016/j.fcr.2017.10.006 Li H.-B. Singh R. K. Singh P. Song Q.-Q. Xing Y.-X. Yang L.-T. . (2017). Genetic diversity of nitrogen-fixing and plant growth promoting pseudomonas species isolated from sugarcane rhizosphere. Front. Microbiol. 8:1268. 10.3389/fmicb.2017.0126828769881 Lin L. Xu X. (2013). Indole-3-acetic acid production by endophytic streptomyces sp. En-1 isolated from medicinal plants. Curr. Microbiol. 67, 209217. 10.1007/s00284-013-0348-z23512121 Liu X. Cao A. Yan D. Ouyang C. Wang Q. Li Y. (2019). Overview of mechanisms and uses of biopesticides. Int. J. Pest Manage. 24, 18. 10.1080/09670874.2019.1664789 Lobo C. B. Juárez Tomás M. S. Viruel E. Ferrero M. A. Lucca M. E. (2019). Development of low-cost formulations of plant growth-promoting bacteria to be used as inoculants in beneficial agricultural technologies. Microbiol. Res. 219, 1225. 10.1016/j.micres.2018.10.01230642462 López-García Á. Varela-Cervero S. Vasar M. Öpik M. Barea J. M. Azcón-Aguilar C. (2017). Plant traits determine the phylogenetic structure of arbuscular mycorrhizal fungal communities. Mol. Ecol. 26, 69486959. 10.1111/mec.1440329110362 Mabrouk Y. Hemissi I. Salem I. Ben M. S. Saidi M. Belhadj O. (2018). “Potential of rhizobia in improving nitrogen fixation and yields of legumes,” in Symbiosis, ed E. C. Rigobelo (London: InTech), 107119. 10.5772/intechopen.73495 Malik A. Mor V. S. Tokas J. Punia H. Malik S. Malik K. . (2020). “Biostimulant-treated seedlings under sustainable agriculture: a global perspective facing climate change. Agronomy 11:14. 10.3390/agronomy11010014 Marzaioli R. D'Ascoli R. De Pascale R. F. A. R. (2010). Soil quality in a Mediterranean area of Southern Italy as related to different land use types. Appl. Soil Ecol. 44, 205212. 10.1016/j.apsoil.2009.12.007 Masso C. Mukhongo R. W. Thuita M. Abaidoo R. Ulzen J. Kariuki G. . (2016). “Biological inoculants for sustainable intensification of agriculture in Sub-Saharan Africa smallholder farming systems,” in Climate Change and Multi-Dimensional Sustainability in African Agriculture, eds R. Lal, D. Kraybill, D. Hansen, B. Singh, T. Mosogoya, and L. Eik (Cham: Springer), 639658. 10.1007/978-3-319-41238-2_33 Mburu S. W. Koskey G. Kimiti J. M. Ombori O. Maingi J. M. Njeru E. M. (2016). Agrobiodiversity conservation enhances food security in subsistence-based farming systems of Eastern kenya. Agric. Food Secur. 5:19. 10.1186/s40066-016-0068-2 Mburu S. W. Koskey G. Njeru E. M. Ombori O. Maingi J. M. Kimiti J. M. (2020). Differential response of promiscuous soybean to local diversity of indigenous and commercial bradyrhizobium inoculation under contrasting agroclimatic sones. Int. J. Plant Product. 10.1007/s42106-020-00117-1 McDonald B. A. Stukenbrock E. H. (2016). Rapid emergence of pathogens in agro-ecosystems: global threats to agricultural sustainability and food security. Philos. Trans. Royal Soc. B Biol. Sci. 371, 20160026. 10.1098/rstb.2016.002628080995 McGuire A. V. Northfield T. D. (2020). Tropical occurrence and agricultural importance of beauveria bassiana and metarhizium anisopliae. Front. Sust. Food Syst. 4:6. 10.3389/fsufs.2020.00006 McNeely D. Chanyi R. M. Dooley J. S. Moore J. E. Koval S. F. (2017). Biocontrol of Burkholderia cepacia complex bacteria and bacterial phytopathogens by Bdellovibrio bacteriovorus. Can. J. Microbiol. 63, 350358. 10.1139/cjm-2016-061228177793 Melo A. L. de A. Soccol V. T. Soccol C. R. (2016). Bacillus thuringiensis: mechanism of action, resistance, and new applications: a review. Crit. Rev. Biotechnol. 36, 317326. 10.3109/07388551.2014.96079325264571 Menge E. M. Njeru E. M. Koskey G. Maingi J. (2018). Rhizobial inoculation methods affect the nodulation and plant growth traits of host plant genotypes: a case study of common bean Phaseolus vulgaris L. germplasms cultivated by smallholder farmers in Eastern Kenya. Adv. Agric. Sci. 6, 7794. Available online at: https://www.researchgate.net/publication/328886447 Mhango W. G. Snapp S. Kanyama-Phiri Y. (2017). Biological nitrogen fixation and yield of pigeonpea and groundnut: quantifying response on smallholder farms in northern Malawi. Afr. J. Agric. Res. 12, 13851394. 10.5897/AJAR2017.12232 Mishra B. K. Lal G. Sharma Y. K. Kant K. Saxena S. N. Dubey P. N. (2019). Effect of microbial inoculants on cumin (Cuminum cyminum Linn.) growth and yield. Int. J. Seed Spices 53, 5356. Available online at: http://isss.ind.in/userfiles/file/2019~new/Untitled-9.pdf Misra M. Sachan A. Sachan S. G. (2020). “Current aspects and applications of biofertilizers for sustainable agriculture,” in Plant Microbiomes for Sustainable Agriculture (Cham: Springer), 445473. 10.1007/978-3-030-38453-1_15 Moonen A. C. Bàrberi P. (2008). Functional biodiversity: an agroecosystem approach. Agric. Ecosyst. Environ. 127, 721. 10.1016/j.agee.2008.02.013 Mosa W. F. A. E.-G. Paszt L. S. Frac M. Trzciński P. Treder W. Klamkowski K. (2018). The role of biofertilizers in improving vegetative growth, yield and fruit quality of apple. Hortic. Sci. 45, 173180. 10.17221/101/2017-HORTSCI Mukhongo R. W. Tumuhairwe J. B. Ebanyat P. AbdelGadir A. A. H. Thuita M. Masso C. (2017). Combined application of biofertilizers and inorganic nutrients improves sweet potato yields. Front. Plant Sci. 8:219. 10.3389/fpls.2017.0021928348569 Mukhongo R. W. Tumuhairwe J. B. Ebanyat P. AbdelGadir A. H. Thuita M. Masso C. (2016). Production and use of arbuscular mycorrhizal fungi inoculum in sub-Saharan Africa: challenges and ways of improving. Int. J. Soil Sci. 11, 108122. 10.3923/ijss.2016.108.122 Mus F. Alleman A. B. Pence N. Seefeldt L. C. Peters J. W. (2018). Exploring the alternatives of biological nitrogen fixation. Metallomics 10, 523538. 10.1039/C8MT00038G29629463 Musyoka D. M. Njeru E. M. Nyamwange M. M. Maingi J. M. (2020). Arbuscular mycorrhizal fungi and bradyrhizobium co-inoculation enhances nitrogen fixation and growth of green grams (Vigna radiata L.) under water stress. J. Plant Nutr. 43, 10361047. 10.1080/01904167.2020.1711940 Nezhad H. M. Shafiabadi J. Hussain M. A. Nezhad M. H. (2015). Microbial resources to safeguard future food security. Adv. Food Technol. Nutr. Sci. 1, 813. 10.17140/AFTNSOJ-SE-1-102 Ngetich F. K. Shisanya C. A. Mugwe J. Mucheru-Muna M. Mugendi D. (2012). “The potential of organic and inorganic nutrient sources in sub-saharan african crop farming systems,” in Soil Fertility Improvement and Integrated Nutrient Management - A Global Perspective, ed J. K. Whalen (InTech), 135159. Available online at: www.intechopen.com Nicolopoulou-Stamati P. Maipas S. Kotampasi C. Stamatis P. Hens L. (2016). Chemical pesticides and human health: the urgent need for a new concept in agriculture. Front. Public Health 4:148. 10.3389/fpubh.2016.0014827486573 Niu D.-D. Wang C.-J. Guo Y.-H. Jiang C.-H. Zhang W.-Z. Wang Y.-P. . (2012). The plant growth-promoting rhizobacterium Bacillus cereus AR156 induces resistance in tomato with induction and priming of defence response. Biocont. Sci. Technol. 22, 9911004. 10.1080/09583157.2012.706595 Njeru E. M. Bocci G. Avio L. Sbrana C. Turrini A. Giovannetti M. . (2017). Functional identity has a stronger effect than diversity on mycorrhizal symbiosis and productivity of field grown organic tomato. Euro. J. Agron. 86, 111. 10.1016/j.eja.2017.02.007 Njeru E. M. Muthini M. Muindi M. M. Ombori O. Nchore S. B. Runo S. . (2020). “Exploiting arbuscular mycorrhizal fungi-rhizobia-legume symbiosis to increase smallholder farmers' crop production and resilience under a changing climate,” in Climate Impacts on Agricultural and Natural Resource Sustainability in Africa, eds B. Singh, A. Safalaoh, N. Amuri, L. Eik, B. Sitaula, and R. Lal (Cham: Springer), 471488. 10.1007/978-3-030-37537-9_27 Novo L. A. B. Castro P. M. L. Alvarenga P. da Silva E. F. (2018). “Plant growth-promoting rhizobacteria-assisted phytoremediation of mine soils,” in Bio-Geotechnologies for Mine Site Rehabilitation, eds M.N.V. Prasad, P.J. de Campos Favas, and S.K. Maiti (Amsterdam: Elsevier Inc.), 281295. 10.1016/B978-0-12-812986-9.00016-6 Nuzzo A. Satpute A. Albrecht U. Strauss S. L. (2020). Impact of soil microbial amendments on tomato rhizosphere microbiome and plant growth in field soil. Microbiol. Ecol. 80, 398409. 10.1007/s00248-020-01497-732144464 Nyambo D. G. Luhanga E. T. Yonah Z. Q. (2019). A review of characterization approaches for smallholder farmers: towards predictive farm typologies. Sci. World J. 2019:6121467. 10.1155/2019/612146731239834 Nyamwange M. M. Njeru E. M. Mucheru-Muna M. Ngetich F. (2018). Soil management practices affect arbuscular mycorrhizal fungi propagules, root colonization and growth of rainfed maize. AIMS Agric. Food 3, 120134. 10.3934/agrfood.2018.2.120 Odame H. (1997). Biofertilizer in Kenya: Research, production and extension dilemmas. Biotechnol. Dev. Mon. 30, 2023. Available online at: http://www.biotech-monitor.nl/3009.htm Orrell P. Bennett A. E. (2013). How can we exploit above-belowground interactions to assist in addressing the challenges of food security? Front. Plant Sci. 4:432. 10.3389/fpls.2013.0043224198821 Oruru M. B. Njeru E. M. (2016). Upscaling arbuscular mycorrhizal symbiosis and related agroecosystems services in smallholder farming systems. BioMed Res. Int. 2016, 112. 10.1155/2016/437624026942194 Ouma E. W. Asango A. M. Maingi J. Njeru E. M. (2016). Elucidating the potential of native rhizobial isolates to improve biological nitrogen fixation and growth of common bean and soybean in smallholder farming systems of Kenya. Int. J. Agronomy. 2016:4569241. 10.1155/2016/4569241 Panwar V. Aggarwal A. Singh G. Saharan M. S. Verma A. Sharma I. . (2014). Efficacy of foliar spray of Trichoderma isolates against Fusarium graminearum causing head blight of wheat. J. Wheat Res. 6, 5963. Available online at: http://epubs.icar.org.in/ejournal/index.php/JWR Parani K. Saha B. K. (2012). Prospects of using phosphate solubilizing pseudomonas as bio fertilizer. Eur. J. Biol. Sci. 4, 4044. 10.5829/idosi.ejbs.2012.4.2.63117 Park J. M. Radhakrishnan R. Kang S. M. Lee I. J. (2015). IAA producing Enterobacter sp. I-3 as a potent bio-herbicide candidate for weed control: a special reference with lettuce growth inhibition. Ind. J. Microbiol. 55, 207212. 10.1007/s12088-015-0515-y25805908 Park Y. G. Mun B. G. Kang S. M. Hussain A. Shahzad R. Seo C. W. . (2017). Bacillus aryabhattai SRB02 tolerates oxidative and nitrosative stress and promotes the growth of soybean by modulating the production of phytohormones. PLoS ONE 12:e0173203. 10.1371/journal.pone.017320328282395 Pellegrino E. Turrini A. Gamper H. A. Caf,à G. Bonari E. Young J. P. W. . (2012). Establishment, persistence and effectiveness of arbuscular mycorrhizal fungal inoculants in the field revealed using molecular genetic tracing and measurement of yield components. New Phytol. 194, 810822. 10.1111/j.1469-8137.2012.04090.x22380845 Pérez-Escamilla R. (2017). Food security and the 2015–2030 sustainable development goals: from human to planetary health. Curr. Dev. Nutr. 1:e000513. 10.3945/cdn.117.00051329955711 Piromyou P. Buranabanyat B. Tantasawat P. Tittabutr P. Boonkerd N. Teaumroong N. (2011). Effect of plant growth promoting rhizobacteria (PGPR) inoculation on microbial community structure in rhizosphere of forage corn cultivated in Thailand. Euro. J. Soil Biol. 47, 4454. 10.1016/j.ejsobi.2010.11.004 Preininger C. Sauer U. Bejarano A. Berninger T. (2018). Concepts and applications of foliar spray for microbial inoculants. Appl. Microbiol. Biotechnol. 102, 72657282. 10.1007/s00253-018-9173-429961100 Premachandra D. Hudek L. Enez A. Ballard R. Barnett S. Franco C. M. M. . (2020). Assessment of the capacity of beneficial bacterial inoculants to enhance canola (brassica napus l.) growth under low water activity. Agronomy 10:1449. 10.3390/agronomy10091449 Raaijmakers J. M. Vlami M. de Souza J. T. (2002). Antibiotic production by bacterial biocontrol agents. Antonie Leeuwenhoek. 81, 537547. 10.1023/A:102050142083112448749 Raimi A. Adeleke R. Roopnarain A. (2017). Soil fertility challenges and Biofertiliser as a viable alternative for increasing smallholder farmer crop productivity in sub-Saharan Africa. Cogent Food Agric. 3:1400933. 10.1080/23311932.2017.1400933 Raimi A. Ezeokoli O. Adeleke R. (2019). High-throughput sequence analysis of bacterial communities in commercial biofertiliser products marketed in South Africa: an independent snapshot quality assessment. 3 Biotech 9:108. 10.1007/s13205-019-1643-630863692 Rashid M. I. Mujawar L. H. Shahzad T. Almeelbi T. Ismail I. M. I. Oves M. (2016). Bacteria and fungi can contribute to nutrients bioavailability and aggregate formation in degraded soils. Microbiol. Res. 183, 2641. 10.1016/j.micres.2015.11.00726805616 Reddy C. A. Saravanan R. S. (2013). Polymicrobial multi-functional approach for enhancement of crop productivity. Adv. Appl. Microbiol. 82, 53113. 10.1016/B978-0-12-407679-2.00003-X23415153 Rivera J. D. Lemus R. W. Gipson M. L. Gipson R. G. (2015). Effects of polymicrobial bioinoculant on yield, quality and in situ digestibility of sorghum sudangrass in south mississippi cover crops. Agrotechnology 5:1. 10.4172/2168-9881.1000136 Rouphael Y. Colla G. (2020). Editorial: biostimulants in agriculture. Front. Plant Sci. 11:40. 10.3389/fpls.2020.00040 Rowe H. Brown C. Claassen V. P. (2007). Comparisons of mycorrhizal responsiveness with field soil and commercial inoculum for six native montane species and bromus tectorum. Restor. Ecol. 15, 4452. 10.1111/j.1526-100X.2006.00188.x Saad M. M. Eida A. A. Hirt H. (2020). Tailoring plant-associated microbial inoculants in agriculture: a roadmap for successful application. J. Exp. Bot. 71, 38783901. 10.1093/jxb/eraa11132157287 Salem A. A. (2016). Potential acting of a novice Achromobacter xylosoxidans strain as a plant growth-promoting factor. Ann. Agric. Sci. 54, 6376. 10.21608/assjm.2016.103911 Sanchis V. (2011). From microbial sprays to insect-resistant transgenic plants: History of the biospesticide Bacillus thuringiensis: A review. Agron. Sust. Dev. 31, 217231. 10.1051/agro/2010027 Sandhya V. Ali S. Z. Grover M. Reddy G. Venkateswarlu B. (2010). Effect of plant growth promoting Pseudomonas spp. on compatible solutes, antioxidant status and plant growth of maize under drought stress. Plant Growth Regul. 62, 2130. 10.1007/s10725-010-9479-4 Sangeeth K. P. Bhai R. S. Srinivasan V. (2012). Paenibacillus glucanolyticus, a promising potassium solubilizing bacterium isolated from black pepper (Piper nigrum L.) rhizosphere. J. Spices Aromat Crops 21, 118124. Available online at: www.indianspicesociety.in/josac/index.php/josac Santos M. S. Nogueira M. A. Hungria M. (2019). Microbial inoculants: reviewing the past, discussing the present and previewing an outstanding future for the use of beneficial bacteria in agriculture. AMB Express 9, 113. 10.1186/s13568-019-0932-031865554 Saravanakumar D. Samiyappan R. (2007). ACC deaminase from pseudomonas fluorescens mediated saline resistance in groundnut (Arachis hypogea) plants. J. Appl. Microbiol. 102, 12831292. 10.1111/j.1365-2672.2006.03179.x17448163 Sarwar M. (2015). Biopesticides: an effective and environmental friendly insect-pests inhibitor line of action. Int. J. Eng. Adv. Res. Technol. 1, 1015. Available online at: http://www.academia.edu/download/49520237/IJEART01108.pdf Saxena A. K. Pal K. K. Tilak K. V. B. R. (2000). “Bacterial biocontrol agents and their role in plant disease management,” in Biocontrol Potential and its Exploitation in Sustainable Agriculture, eds R.K. Upadhyay, K.G. Mukerji, and B.P. Chamola (Boston MA: Springer), 2537. 10.1007/978-1-4615-4209-4_3 Schütz L. Gattinger A. Meier M. Müller A. Boller T. Mäder P. . (2018). Improving crop yield and nutrient use efficiency via biofertilization—a global meta-analysis. Front. Plant Sci. 8:2204. 10.3389/fpls.2017.0220429375594 Schwartz M. W. Hoeksema J. D. Gehring C. A. Johnson N. C. Klironomos J. N. Abbott L. K. . (2006). The promise and the potential consequences of the global transport of mycorrhizal fungal inoculum. Ecol. Lett. 9, 501515. 10.1111/j.1461-0248.2006.00910.x16643296 Selvi K. Paul J. Vijaya V. Saraswathi K. (2017). Analyzing the efficacy of phosphate solubilizing microorganisms by enrichment culture techniques. Biochem. Mol. Biol. J. 3:1. 10.21767/2471-8084.100029 Seraj M. F. Rahman T. Lawrie A. C. Reichman S. M. (2020). Assessing the plant growth promoting and arsenic tolerance potential of Bradyrhizobium japonicum CB1809. Environ. Manage. 66, 930939. 10.1007/s00267-020-01351-z32918111 Shanafelt D. W. Dieckmann U. Jonas M. Franklin O. Loreau M. Perrings C. (2015). Biodiversity, productivity, and the spatial insurance hypothesis revisited. J. Theor. Biol. 380, 426435. 10.1016/j.jtbi.2015.06.01726100182 Sharma S. Gupta R. Dugar G. Srivastava A. K. (2012). “Impact of application of biofertilizers on soil structure and resident microbial community structure and function,” in Bacteria in Agrobiology: Plant Probiotics, ed D. Maheshwari (Berlin: Springer), 6577. 10.1007/978-3-642-27515-9_4 Sharma S. B. Sayyed R. Z. Trivedi M. H. Gobi T. A. (2013). Phosphate solubilizing microbes: Sustainable approach for managing phosphorus deficiency in agricultural soils. SpringerPlus. 2:587. 10.1186/2193-1801-2-58725674415 Sileshi G. W. Teketay D. Gebrekirstos A. Hadgu K. (2020). “Sustainability of faidherbia albida-based agroforestry in crop production and maintaining soil health,” in Agroforestry for Degraded Landscapes, eds J.C. Dagar, S.R. Gupta, and D. Teketay (Singapore: Springer), 349369. 10.1007/978-981-15-6807-7_12 Sindhu S. Dahiya A. Gera R. Sindhu S. S. (2020). Mitigation of abiotic stress in legume-nodulating rhizobia for sustainable crop production. Agric. Res. 9, 444459. 10.1007/s40003-020-00474-3 Singh B. K. Trivedi P. (2017). Microbiome and the future for food and nutrient security. Microbiol. Biotechnol. 10, 5053. 10.1111/1751-7915.1259228074557 Singh S. K. Pathak R. Pancholy A. (2017). Role of Root Nodule Bacteria in Improving Soil Fertility and Growth Attributes of Leguminous Plants Under Arid and Semiarid Environments. Cham: Springer. 10.1007/978-3-319-64982-5_4 Sinong G. F. Yasuda M. Nara Y. Lee C. G. Dastogeer K. M. G. Tabuchi H. . (2021). Distinct root microbial communities in nature farming rice harbor bacterial strains with plant growth-promoting traits. Front. Sust. Food Syst. 4:629942. 10.3389/fsufs.2020.629942 Song Y. Liu J. Chen F. (2020). Azotobacter chroococcum inoculation can improve plant growth and resistance of maize to armyworm, MYTHIMNA separata even under reduced nitrogen fertilizer application. Pest Manage. Sci. 76, 41314140. 10.1002/ps.596932706174 Soumare A. Boubekri K. Lyamlouli K. Hafidi M. Ouhdouch Y. Kouisni L. (2020). From isolation of phosphate solubilizing microbes to their formulation and use as biofertilizers: status and needs. Front. Bioeng. Biotechnol. 7:425. 10.3389/fbioe.2019.0042531998701 Sousa R. M. S. Mendes L. W. Antunes J. E. L. Oliveira L. M. de S. Sousa A. M. de, C. B. . (2020). Diversity and structure of bacterial community in rhizosphere of lima bean. Appl. Soil Ecol. 102:103490. 10.1016/j.apsoil.2019.103490 Stamenković S. Beškoski V. Karabegović I. Lazić M. Nikolić N. (2018). Microbial fertilizers: A comprehensive review of current findings and future perspectives. Span. J. Agric. Res. 16:2192. 10.5424/sjar/2018161-12117 Sun X. G. Tang M. (2013). Effect of arbuscular mycorrhizal fungi inoculation on root traits and root volatile organic compound emissions of Sorghum bicolor. South Afr. J. Bot. 88, 373379. 10.1016/j.sajb.2013.09.007 Swain H. Adak T. Mukherjee A. K. Mukherjee P. K. Bhattacharyya P. Behera S. . (2018). Novel Trichoderma strains isolated from tree barks as potential biocontrol agents and biofertilizers for direct seeded rice. Microbiol. Res. 214, 8390. 10.1016/j.micres.2018.05.01530031485 Tabassum B. Khan A. Tariq M. Ramzan M. Iqbal Khan M. S. Shahid N. . (2017). Bottlenecks in commercialisation and future prospects of PGPR. Appl. Soil Ecol. 121, 102117. 10.1016/j.apsoil.2017.09.030 Tapsoba P. K. Aoudji A. K. N. Kabore M. Kestemont M. P. Legay C. Achigan-Dako E. G. (2020). Sociotechnical context and agroecological transition for smallholder farms in benin and Burkina Faso. Agronomy 10, 134. 10.3390/agronomy10091447 Tewari S. Shrivas V. L. Hariprasad P. Sharma S. (2019). “Harnessing endophytes as biocontrol agents,” in Plant Health Under Biotic Stress (Sigapore: Springer), 189218. 10.1007/978-981-13-6040-4_10 Thakur D. Kaushal R. Shyam V. (2014). Phosphate solubilising microorganisms: role in phosphorus nutrition of crop plants-A review. Agric. Rev. 35:159. 10.5958/0976-0741.2014.00903.9 Velázquez-Hernández M. L. Baizabal-Aguirre V. M. Cruz-Vázquez F. Trejo-Contreras M. J. Fuentes-Ramírez L. E. Bravo-Patiño A. . (2011). Gluconacetobacter diazotrophicus levansucrase is involved in tolerance to NaCl, sucrose and desiccation, and in biofilm formation. Arch. Microbiol. 193, 137149. 10.1007/s00203-010-0651-z21103984 Velivelli S. L. S. Sessitsch A. Prestwich B. D. (2014). The role of microbial inoculants in integrated crop management systems. Potato Res. 57, 291309. 10.1007/s11540-014-9278-9 Ventorino V. De Marco A. Pepe O. Virzo A. Santo D. Moschetti G. (2012). “Impact of innovative agricultural practices of carbon sequestration on soil microbial community,” in Carbon Sequestration in Agricultural Soils, ed A. Piccolo (Berlin: Springer), 145177. 10.1007/978-3-642-23385-2_6 Wahid F. Fahad S. Danish S. Adnan M. Yue Z. Saud S. . (2020). Sustainable management with mycorrhizae and phosphate solubilizing bacteria for enhanced phosphorus uptake in calcareous soils. Agriculture 10, 114. 10.3390/agriculture10080334 Wang L. Zhang L. Liu Z. Zhao D. Liu X. Zhang B. . (2013). “A minimal nitrogen fixation gene cluster from Paenibacillus sp. WLY78 enables expression of active nitrogenase in Escherichia coli. PLoS Genet. 9, 110. 10.1371/annotation/1e9bcb70-265a-4383-abf4-3466d144d56e24146630 Wei C. Y. Lin L. Luo L. J. Xing Y. X. Hu C. J. Yang L. T. . (2014). Endophytic nitrogen-fixing Klebsiella variicola strain DX120E promotes sugarcane growth. Biol. Fertil. Soils 50, 657666. 10.1007/s00374-013-0878-3 Wu S. C. Cao Z. H. Li Z. G. Cheung K. C. Wong M. H. (2005). Effects of biofertilizer containing N-fixer, P and K solubilizers and AM fungi on maize growth: a greenhouse trial. Geoderma 125, 155166. 10.1016/j.geoderma.2004.07.003 Yachi S. Loreau M. (1999). Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis. Proc. Natl. Acad. Sci. 96, 14631468. 10.1073/pnas.96.4.14639990046 Yeager C. M. Northup D. E. Grow C. C. Barns S. M. Kuske C. R. (2005). Changes in nitrogen-fixing and ammonia-oxidizing bacterial communities in soil of a mixed conifer forest after wildfire. Appl. Environ. Microbiol. 71, 27132722. 10.1128/AEM.71.5.2713-2722.200515870363 Zhang F. Yuan J. Yang X. Cui Y. Chen L. Ran W. . (2013). Putative Trichoderma harzianum mutant promotes cucumber growth by enhanced production of indole acetic acid and plant colonization. Plant Soil 368, 433444. 10.1007/s11104-012-1519-6 Zhou D. Wang X. Chen G. Sun S. Yang Y. Zhu Z. . (2018). The major fusarium species causing maize ear and kernel rot and their toxigenicity in Chongqing, China. Toxins 10:90. 10.3390/toxins10020090

      Funding. This work was supported by The Future Leaders–African Independent Researchers (FLAIR) Fellowship Programme, which is a partnership between the African Academy of Sciences and the Royal Society funded by the UK Government's Global Challenges Research Fund (Grant No. FLR/R1/190944). The Scuola Superiore Sant'Anna, Pisa, Italy and the Deutscher Akademischer Austauschdienst (DAAD) funded the Ph.D., scholarships of GK and SM, respectively.

      ‘Oh, my dear Thomas, you haven’t heard the terrible news then?’ she said. ‘I thought you would be sure to have seen it placarded somewhere. Alice went straight to her room, and I haven’t seen her since, though I repeatedly knocked at the door, which she has locked on the inside, and I’m sure it’s most unnatural of her not to let her own mother comfort her. It all happened in a moment: I have always said those great motor-cars shouldn’t be allowed to career about the streets, especially when they are all paved with cobbles as they are at Easton Haven, which are{331} so slippery when it’s wet. He slipped, and it went over him in a moment.’ My thanks were few and awkward, for there still hung to the missive a basting thread, and it was as warm as a nestling bird. I bent low--everybody was emotional in those days--kissed the fragrant thing, thrust it into my bosom, and blushed worse than Camille. "What, the Corner House victim? Is that really a fact?" "My dear child, I don't look upon it in that light at all. The child gave our picturesque friend a certain distinction--'My husband is dead, and this is my only child,' and all that sort of thing. It pays in society." leave them on the steps of a foundling asylum in order to insure [See larger version] Interoffice guff says you're planning definite moves on your own, J. O., and against some opposition. Is the Colonel so poor or so grasping—or what? Albert could not speak, for he felt as if his brains and teeth were rattling about inside his head. The rest of[Pg 188] the family hunched together by the door, the boys gaping idiotically, the girls in tears. "Now you're married." The host was called in, and unlocked a drawer in which they were deposited. The galleyman, with visible reluctance, arrayed himself in the garments, and he was observed to shudder more than once during the investiture of the dead man's apparel. HoME香京julia种子在线播放 ENTER NUMBET 0016www.kokty.com.cn
      www.kinduct.com.cn
      www.fhpriu.com.cn
      www.gfltech.com.cn
      hzmsj.com.cn
      hzxfsj.com.cn
      www.fsduoxin.com.cn
      shxmpt.com.cn
      uxbwpb.com.cn
      www.spylkj.net.cn
      处女被大鸡巴操 强奸乱伦小说图片 俄罗斯美女爱爱图 调教强奸学生 亚洲女的穴 夜来香图片大全 美女性强奸电影 手机版色中阁 男性人体艺术素描图 16p成人 欧美性爱360 电影区 亚洲电影 欧美电影 经典三级 偷拍自拍 动漫电影 乱伦电影 变态另类 全部电 类似狠狠鲁的网站 黑吊操白逼图片 韩国黄片种子下载 操逼逼逼逼逼 人妻 小说 p 偷拍10幼女自慰 极品淫水很多 黄色做i爱 日本女人人体电影快播看 大福国小 我爱肏屄美女 mmcrwcom 欧美多人性交图片 肥臀乱伦老头舔阴帝 d09a4343000019c5 西欧人体艺术b xxoo激情短片 未成年人的 插泰国人夭图片 第770弾み1 24p 日本美女性 交动态 eee色播 yantasythunder 操无毛少女屄 亚洲图片你懂的女人 鸡巴插姨娘 特级黄 色大片播 左耳影音先锋 冢本友希全集 日本人体艺术绿色 我爱被舔逼 内射 幼 美阴图 喷水妹子高潮迭起 和后妈 操逼 美女吞鸡巴 鸭个自慰 中国女裸名单 操逼肥臀出水换妻 色站裸体义术 中国行上的漏毛美女叫什么 亚洲妹性交图 欧美美女人裸体人艺照 成人色妹妹直播 WWW_JXCT_COM r日本女人性淫乱 大胆人艺体艺图片 女同接吻av 碰碰哥免费自拍打炮 艳舞写真duppid1 88电影街拍视频 日本自拍做爱qvod 实拍美女性爱组图 少女高清av 浙江真实乱伦迅雷 台湾luanlunxiaoshuo 洛克王国宠物排行榜 皇瑟电影yy频道大全 红孩儿连连看 阴毛摄影 大胆美女写真人体艺术摄影 和风骚三个媳妇在家做爱 性爱办公室高清 18p2p木耳 大波撸影音 大鸡巴插嫩穴小说 一剧不超两个黑人 阿姨诱惑我快播 幼香阁千叶县小学生 少女妇女被狗强奸 曰人体妹妹 十二岁性感幼女 超级乱伦qvod 97爱蜜桃ccc336 日本淫妇阴液 av海量资源999 凤凰影视成仁 辰溪四中艳照门照片 先锋模特裸体展示影片 成人片免费看 自拍百度云 肥白老妇女 女爱人体图片 妈妈一女穴 星野美夏 日本少女dachidu 妹子私处人体图片 yinmindahuitang 舔无毛逼影片快播 田莹疑的裸体照片 三级电影影音先锋02222 妻子被外国老头操 观月雏乃泥鳅 韩国成人偷拍自拍图片 强奸5一9岁幼女小说 汤姆影院av图片 妹妹人艺体图 美女大驱 和女友做爱图片自拍p 绫川まどか在线先锋 那么嫩的逼很少见了 小女孩做爱 处女好逼连连看图图 性感美女在家做爱 近距离抽插骚逼逼 黑屌肏金毛屄 日韩av美少女 看喝尿尿小姐日逼色色色网图片 欧美肛交新视频 美女吃逼逼 av30线上免费 伊人在线三级经典 新视觉影院t6090影院 最新淫色电影网址 天龙影院远古手机版 搞老太影院 插进美女的大屁股里 私人影院加盟费用 www258dd 求一部电影里面有一个二猛哥 深肛交 日本萌妹子人体艺术写真图片 插入屄眼 美女的木奶 中文字幕黄色网址影视先锋 九号女神裸 和骚人妻偷情 和潘晓婷做爱 国模大尺度蜜桃 欧美大逼50p 西西人体成人 李宗瑞继母做爱原图物处理 nianhuawang 男鸡巴的视屏 � 97免费色伦电影 好色网成人 大姨子先锋 淫荡巨乳美女教师妈妈 性nuexiaoshuo WWW36YYYCOM 长春继续给力进屋就操小女儿套干破内射对白淫荡 农夫激情社区 日韩无码bt 欧美美女手掰嫩穴图片 日本援交偷拍自拍 入侵者日本在线播放 亚洲白虎偷拍自拍 常州高见泽日屄 寂寞少妇自卫视频 人体露逼图片 多毛外国老太 变态乱轮手机在线 淫荡妈妈和儿子操逼 伦理片大奶少女 看片神器最新登入地址sqvheqi345com账号群 麻美学姐无头 圣诞老人射小妞和强奸小妞动话片 亚洲AV女老师 先锋影音欧美成人资源 33344iucoom zV天堂电影网 宾馆美女打炮视频 色五月丁香五月magnet 嫂子淫乱小说 张歆艺的老公 吃奶男人视频在线播放 欧美色图男女乱伦 avtt2014ccvom 性插色欲香影院 青青草撸死你青青草 99热久久第一时间 激情套图卡通动漫 幼女裸聊做爱口交 日本女人被强奸乱伦 草榴社区快播 2kkk正在播放兽骑 啊不要人家小穴都湿了 www猎奇影视 A片www245vvcomwwwchnrwhmhzcn 搜索宜春院av wwwsee78co 逼奶鸡巴插 好吊日AV在线视频19gancom 熟女伦乱图片小说 日本免费av无码片在线开苞 鲁大妈撸到爆 裸聊官网 德国熟女xxx 新不夜城论坛首页手机 女虐男网址 男女做爱视频华为网盘 激情午夜天亚洲色图 内裤哥mangent 吉沢明歩制服丝袜WWWHHH710COM 屌逼在线试看 人体艺体阿娇艳照 推荐一个可以免费看片的网站如果被QQ拦截请复制链接在其它浏览器打开xxxyyy5comintr2a2cb551573a2b2e 欧美360精品粉红鲍鱼 教师调教第一页 聚美屋精品图 中韩淫乱群交 俄罗斯撸撸片 把鸡巴插进小姨子的阴道 干干AV成人网 aolasoohpnbcn www84ytom 高清大量潮喷www27dyycom 宝贝开心成人 freefronvideos人母 嫩穴成人网gggg29com 逼着舅妈给我口交肛交彩漫画 欧美色色aV88wwwgangguanscom 老太太操逼自拍视频 777亚洲手机在线播放 有没有夫妻3p小说 色列漫画淫女 午间色站导航 欧美成人处女色大图 童颜巨乳亚洲综合 桃色性欲草 色眯眯射逼 无码中文字幕塞外青楼这是一个 狂日美女老师人妻 爱碰网官网 亚洲图片雅蠛蝶 快播35怎么搜片 2000XXXX电影 新谷露性家庭影院 深深候dvd播放 幼齿用英语怎么说 不雅伦理无需播放器 国外淫荡图片 国外网站幼幼嫩网址 成年人就去色色视频快播 我鲁日日鲁老老老我爱 caoshaonvbi 人体艺术avav 性感性色导航 韩国黄色哥来嫖网站 成人网站美逼 淫荡熟妇自拍 欧美色惰图片 北京空姐透明照 狼堡免费av视频 www776eom 亚洲无码av欧美天堂网男人天堂 欧美激情爆操 a片kk266co 色尼姑成人极速在线视频 国语家庭系列 蒋雯雯 越南伦理 色CC伦理影院手机版 99jbbcom 大鸡巴舅妈 国产偷拍自拍淫荡对话视频 少妇春梦射精 开心激动网 自拍偷牌成人 色桃隐 撸狗网性交视频 淫荡的三位老师 伦理电影wwwqiuxia6commqiuxia6com 怡春院分站 丝袜超短裙露脸迅雷下载 色制服电影院 97超碰好吊色男人 yy6080理论在线宅男日韩福利大全 大嫂丝袜 500人群交手机在线 5sav 偷拍熟女吧 口述我和妹妹的欲望 50p电脑版 wwwavtttcon 3p3com 伦理无码片在线看 欧美成人电影图片岛国性爱伦理电影 先锋影音AV成人欧美 我爱好色 淫电影网 WWW19MMCOM 玛丽罗斯3d同人动画h在线看 动漫女孩裸体 超级丝袜美腿乱伦 1919gogo欣赏 大色逼淫色 www就是撸 激情文学网好骚 A级黄片免费 xedd5com 国内的b是黑的 快播美国成年人片黄 av高跟丝袜视频 上原保奈美巨乳女教师在线观看 校园春色都市激情fefegancom 偷窥自拍XXOO 搜索看马操美女 人本女优视频 日日吧淫淫 人妻巨乳影院 美国女子性爱学校 大肥屁股重口味 啪啪啪啊啊啊不要 操碰 japanfreevideoshome国产 亚州淫荡老熟女人体 伦奸毛片免费在线看 天天影视se 樱桃做爱视频 亚卅av在线视频 x奸小说下载 亚洲色图图片在线 217av天堂网 东方在线撸撸-百度 幼幼丝袜集 灰姑娘的姐姐 青青草在线视频观看对华 86papa路con 亚洲1AV 综合图片2区亚洲 美国美女大逼电影 010插插av成人网站 www色comwww821kxwcom 播乐子成人网免费视频在线观看 大炮撸在线影院 ,www4KkKcom 野花鲁最近30部 wwwCC213wapwww2233ww2download 三客优最新地址 母亲让儿子爽的无码视频 全国黄色片子 欧美色图美国十次 超碰在线直播 性感妖娆操 亚洲肉感熟女色图 a片A毛片管看视频 8vaa褋芯屑 333kk 川岛和津实视频 在线母子乱伦对白 妹妹肥逼五月 亚洲美女自拍 老婆在我面前小说 韩国空姐堪比情趣内衣 干小姐综合 淫妻色五月 添骚穴 WM62COM 23456影视播放器 成人午夜剧场 尼姑福利网 AV区亚洲AV欧美AV512qucomwwwc5508com 经典欧美骚妇 震动棒露出 日韩丝袜美臀巨乳在线 av无限吧看 就去干少妇 色艺无间正面是哪集 校园春色我和老师做爱 漫画夜色 天海丽白色吊带 黄色淫荡性虐小说 午夜高清播放器 文20岁女性荫道口图片 热国产热无码热有码 2015小明发布看看算你色 百度云播影视 美女肏屄屄乱轮小说 家族舔阴AV影片 邪恶在线av有码 父女之交 关于处女破处的三级片 极品护士91在线 欧美虐待女人视频的网站 享受老太太的丝袜 aaazhibuo 8dfvodcom成人 真实自拍足交 群交男女猛插逼 妓女爱爱动态 lin35com是什么网站 abp159 亚洲色图偷拍自拍乱伦熟女抠逼自慰 朝国三级篇 淫三国幻想 免费的av小电影网站 日本阿v视频免费按摩师 av750c0m 黄色片操一下 巨乳少女车震在线观看 操逼 免费 囗述情感一乱伦岳母和女婿 WWW_FAMITSU_COM 偷拍中国少妇在公车被操视频 花也真衣论理电影 大鸡鸡插p洞 新片欧美十八岁美少 进击的巨人神thunderftp 西方美女15p 深圳哪里易找到老女人玩视频 在线成人有声小说 365rrr 女尿图片 我和淫荡的小姨做爱 � 做爱技术体照 淫妇性爱 大学生私拍b 第四射狠狠射小说 色中色成人av社区 和小姨子乱伦肛交 wwwppp62com 俄罗斯巨乳人体艺术 骚逼阿娇 汤芳人体图片大胆 大胆人体艺术bb私处 性感大胸骚货 哪个网站幼女的片多 日本美女本子把 色 五月天 婷婷 快播 美女 美穴艺术 色百合电影导航 大鸡巴用力 孙悟空操美少女战士 狠狠撸美女手掰穴图片 古代女子与兽类交 沙耶香套图 激情成人网区 暴风影音av播放 动漫女孩怎么插第3个 mmmpp44 黑木麻衣无码ed2k 淫荡学姐少妇 乱伦操少女屄 高中性爱故事 骚妹妹爱爱图网 韩国模特剪长发 大鸡巴把我逼日了 中国张柏芝做爱片中国张柏芝做爱片中国张柏芝做爱片中国张柏芝做爱片中国张柏芝做爱片 大胆女人下体艺术图片 789sss 影音先锋在线国内情侣野外性事自拍普通话对白 群撸图库 闪现君打阿乐 ady 小说 插入表妹嫩穴小说 推荐成人资源 网络播放器 成人台 149大胆人体艺术 大屌图片 骚美女成人av 春暖花开春色性吧 女亭婷五月 我上了同桌的姐姐 恋夜秀场主播自慰视频 yzppp 屄茎 操屄女图 美女鲍鱼大特写 淫乱的日本人妻山口玲子 偷拍射精图 性感美女人体艺木图片 种马小说完本 免费电影院 骑士福利导航导航网站 骚老婆足交 国产性爱一级电影 欧美免费成人花花性都 欧美大肥妞性爱视频 家庭乱伦网站快播 偷拍自拍国产毛片 金发美女也用大吊来开包 缔D杏那 yentiyishu人体艺术ytys WWWUUKKMCOM 女人露奶 � 苍井空露逼 老荡妇高跟丝袜足交 偷偷和女友的朋友做爱迅雷 做爱七十二尺 朱丹人体合成 麻腾由纪妃 帅哥撸播种子图 鸡巴插逼动态图片 羙国十次啦中文 WWW137AVCOM 神斗片欧美版华语 有气质女人人休艺术 由美老师放屁电影 欧美女人肉肏图片 白虎种子快播 国产自拍90后女孩 美女在床上疯狂嫩b 饭岛爱最后之作 幼幼强奸摸奶 色97成人动漫 两性性爱打鸡巴插逼 新视觉影院4080青苹果影院 嗯好爽插死我了 阴口艺术照 李宗瑞电影qvod38 爆操舅母 亚洲色图七七影院 被大鸡巴操菊花 怡红院肿么了 成人极品影院删除 欧美性爱大图色图强奸乱 欧美女子与狗随便性交 苍井空的bt种子无码 熟女乱伦长篇小说 大色虫 兽交幼女影音先锋播放 44aad be0ca93900121f9b 先锋天耗ばさ无码 欧毛毛女三级黄色片图 干女人黑木耳照 日本美女少妇嫩逼人体艺术 sesechangchang 色屄屄网 久久撸app下载 色图色噜 美女鸡巴大奶 好吊日在线视频在线观看 透明丝袜脚偷拍自拍 中山怡红院菜单 wcwwwcom下载 骑嫂子 亚洲大色妣 成人故事365ahnet 丝袜家庭教mp4 幼交肛交 妹妹撸撸大妈 日本毛爽 caoprom超碰在email 关于中国古代偷窥的黄片 第一会所老熟女下载 wwwhuangsecome 狼人干综合新地址HD播放 变态儿子强奸乱伦图 强奸电影名字 2wwwer37com 日本毛片基地一亚洲AVmzddcxcn 暗黑圣经仙桃影院 37tpcocn 持月真由xfplay 好吊日在线视频三级网 我爱背入李丽珍 电影师傅床戏在线观看 96插妹妹sexsex88com 豪放家庭在线播放 桃花宝典极夜著豆瓜网 安卓系统播放神器 美美网丝袜诱惑 人人干全免费视频xulawyercn av无插件一本道 全国色五月 操逼电影小说网 good在线wwwyuyuelvcom www18avmmd 撸波波影视无插件 伊人幼女成人电影 会看射的图片 小明插看看 全裸美女扒开粉嫩b 国人自拍性交网站 萝莉白丝足交本子 七草ちとせ巨乳视频 摇摇晃晃的成人电影 兰桂坊成社人区小说www68kqcom 舔阴论坛 久撸客一撸客色国内外成人激情在线 明星门 欧美大胆嫩肉穴爽大片 www牛逼插 性吧星云 少妇性奴的屁眼 人体艺术大胆mscbaidu1imgcn 最新久久色色成人版 l女同在线 小泽玛利亚高潮图片搜索 女性裸b图 肛交bt种子 最热门有声小说 人间添春色 春色猜谜字 樱井莉亚钢管舞视频 小泽玛利亚直美6p 能用的h网 还能看的h网 bl动漫h网 开心五月激 东京热401 男色女色第四色酒色网 怎么下载黄色小说 黄色小说小栽 和谐图城 乐乐影院 色哥导航 特色导航 依依社区 爱窝窝在线 色狼谷成人 91porn 包要你射电影 色色3A丝袜 丝袜妹妹淫网 爱色导航(荐) 好男人激情影院 坏哥哥 第七色 色久久 人格分裂 急先锋 撸撸射中文网 第一会所综合社区 91影院老师机 东方成人激情 怼莪影院吹潮 老鸭窝伊人无码不卡无码一本道 av女柳晶电影 91天生爱风流作品 深爱激情小说私房婷婷网 擼奶av 567pao 里番3d一家人野外 上原在线电影 水岛津实透明丝袜 1314酒色 网旧网俺也去 0855影院 在线无码私人影院 搜索 国产自拍 神马dy888午夜伦理达达兔 农民工黄晓婷 日韩裸体黑丝御姐 屈臣氏的燕窝面膜怎么样つぼみ晶エリーの早漏チ○ポ强化合宿 老熟女人性视频 影音先锋 三上悠亚ol 妹妹影院福利片 hhhhhhhhsxo 午夜天堂热的国产 强奸剧场 全裸香蕉视频无码 亚欧伦理视频 秋霞为什么给封了 日本在线视频空天使 日韩成人aⅴ在线 日本日屌日屄导航视频 在线福利视频 日本推油无码av magnet 在线免费视频 樱井梨吮东 日本一本道在线无码DVD 日本性感诱惑美女做爱阴道流水视频 日本一级av 汤姆avtom在线视频 台湾佬中文娱乐线20 阿v播播下载 橙色影院 奴隶少女护士cg视频 汤姆在线影院无码 偷拍宾馆 业面紧急生级访问 色和尚有线 厕所偷拍一族 av女l 公交色狼优酷视频 裸体视频AV 人与兽肉肉网 董美香ol 花井美纱链接 magnet 西瓜影音 亚洲 自拍 日韩女优欧美激情偷拍自拍 亚洲成年人免费视频 荷兰免费成人电影 深喉呕吐XXⅩX 操石榴在线视频 天天色成人免费视频 314hu四虎 涩久免费视频在线观看 成人电影迅雷下载 能看见整个奶子的香蕉影院 水菜丽百度影音 gwaz079百度云 噜死你们资源站 主播走光视频合集迅雷下载 thumbzilla jappen 精品Av 古川伊织star598在线 假面女皇vip在线视频播放 国产自拍迷情校园 啪啪啪公寓漫画 日本阿AV 黄色手机电影 欧美在线Av影院 华裔电击女神91在线 亚洲欧美专区 1日本1000部免费视频 开放90后 波多野结衣 东方 影院av 页面升级紧急访问每天正常更新 4438Xchengeren 老炮色 a k福利电影 色欲影视色天天视频 高老庄aV 259LUXU-683 magnet 手机在线电影 国产区 欧美激情人人操网 国产 偷拍 直播 日韩 国内外激情在线视频网给 站长统计一本道人妻 光棍影院被封 紫竹铃取汁 ftp 狂插空姐嫩 xfplay 丈夫面前 穿靴子伪街 XXOO视频在线免费 大香蕉道久在线播放 电棒漏电嗨过头 充气娃能看下毛和洞吗 夫妻牲交 福利云点墦 yukun瑟妃 疯狂交换女友 国产自拍26页 腐女资源 百度云 日本DVD高清无码视频 偷拍,自拍AV伦理电影 A片小视频福利站。 大奶肥婆自拍偷拍图片 交配伊甸园 超碰在线视频自拍偷拍国产 小热巴91大神 rctd 045 类似于A片 超美大奶大学生美女直播被男友操 男友问 你的衣服怎么脱掉的 亚洲女与黑人群交视频一 在线黄涩 木内美保步兵番号 鸡巴插入欧美美女的b舒服 激情在线国产自拍日韩欧美 国语福利小视频在线观看 作爱小视颍 潮喷合集丝袜无码mp4 做爱的无码高清视频 牛牛精品 伊aⅤ在线观看 savk12 哥哥搞在线播放 在线电一本道影 一级谍片 250pp亚洲情艺中心,88 欧美一本道九色在线一 wwwseavbacom色av吧 cos美女在线 欧美17,18ⅹⅹⅹ视频 自拍嫩逼 小电影在线观看网站 筱田优 贼 水电工 5358x视频 日本69式视频有码 b雪福利导航 韩国女主播19tvclub在线 操逼清晰视频 丝袜美女国产视频网址导航 水菜丽颜射房间 台湾妹中文娱乐网 风吟岛视频 口交 伦理 日本熟妇色五十路免费视频 A级片互舔 川村真矢Av在线观看 亚洲日韩av 色和尚国产自拍 sea8 mp4 aV天堂2018手机在线 免费版国产偷拍a在线播放 狠狠 婷婷 丁香 小视频福利在线观看平台 思妍白衣小仙女被邻居强上 萝莉自拍有水 4484新视觉 永久发布页 977成人影视在线观看 小清新影院在线观 小鸟酱后丝后入百度云 旋风魅影四级 香蕉影院小黄片免费看 性爱直播磁力链接 小骚逼第一色影院 性交流的视频 小雪小视频bd 小视频TV禁看视频 迷奸AV在线看 nba直播 任你在干线 汤姆影院在线视频国产 624u在线播放 成人 一级a做爰片就在线看狐狸视频 小香蕉AV视频 www182、com 腿模简小育 学生做爱视频 秘密搜查官 快播 成人福利网午夜 一级黄色夫妻录像片 直接看的gav久久播放器 国产自拍400首页 sm老爹影院 谁知道隔壁老王网址在线 综合网 123西瓜影音 米奇丁香 人人澡人人漠大学生 色久悠 夜色视频你今天寂寞了吗? 菲菲影视城美国 被抄的影院 变态另类 欧美 成人 国产偷拍自拍在线小说 不用下载安装就能看的吃男人鸡巴视频 插屄视频 大贯杏里播放 wwwhhh50 233若菜奈央 伦理片天海翼秘密搜查官 大香蕉在线万色屋视频 那种漫画小说你懂的 祥仔电影合集一区 那里可以看澳门皇冠酒店a片 色自啪 亚洲aV电影天堂 谷露影院ar toupaizaixian sexbj。com 毕业生 zaixian mianfei 朝桐光视频 成人短视频在线直接观看 陈美霖 沈阳音乐学院 导航女 www26yjjcom 1大尺度视频 开平虐女视频 菅野雪松协和影视在线视频 华人play在线视频bbb 鸡吧操屄视频 多啪啪免费视频 悠草影院 金兰策划网 (969) 橘佑金短视频 国内一极刺激自拍片 日本制服番号大全magnet 成人动漫母系 电脑怎么清理内存 黄色福利1000 dy88午夜 偷拍中学生洗澡磁力链接 花椒相机福利美女视频 站长推荐磁力下载 mp4 三洞轮流插视频 玉兔miki热舞视频 夜生活小视频 爆乳人妖小视频 国内网红主播自拍福利迅雷下载 不用app的裸裸体美女操逼视频 变态SM影片在线观看 草溜影院元气吧 - 百度 - 百度 波推全套视频 国产双飞集合ftp 日本在线AV网 笔国毛片 神马影院女主播是我的邻居 影音资源 激情乱伦电影 799pao 亚洲第一色第一影院 av视频大香蕉 老梁故事汇希斯莱杰 水中人体磁力链接 下载 大香蕉黄片免费看 济南谭崔 避开屏蔽的岛a片 草破福利 要看大鸡巴操小骚逼的人的视频 黑丝少妇影音先锋 欧美巨乳熟女磁力链接 美国黄网站色大全 伦蕉在线久播 极品女厕沟 激情五月bd韩国电影 混血美女自摸和男友激情啪啪自拍诱人呻吟福利视频 人人摸人人妻做人人看 44kknn 娸娸原网 伊人欧美 恋夜影院视频列表安卓青青 57k影院 如果电话亭 avi 插爆骚女精品自拍 青青草在线免费视频1769TV 令人惹火的邻家美眉 影音先锋 真人妹子被捅动态图 男人女人做完爱视频15 表姐合租两人共处一室晚上她竟爬上了我的床 性爱教学视频 北条麻妃bd在线播放版 国产老师和师生 magnet wwwcctv1024 女神自慰 ftp 女同性恋做激情视频 欧美大胆露阴视频 欧美无码影视 好女色在线观看 后入肥臀18p 百度影视屏福利 厕所超碰视频 强奸mp magnet 欧美妹aⅴ免费线上看 2016年妞干网视频 5手机在线福利 超在线最视频 800av:cOm magnet 欧美性爱免播放器在线播放 91大款肥汤的性感美乳90后邻家美眉趴着窗台后入啪啪 秋霞日本毛片网站 cheng ren 在线视频 上原亚衣肛门无码解禁影音先锋 美脚家庭教师在线播放 尤酷伦理片 熟女性生活视频在线观看 欧美av在线播放喷潮 194avav 凤凰AV成人 - 百度 kbb9999 AV片AV在线AV无码 爱爱视频高清免费观看 黄色男女操b视频 观看 18AV清纯视频在线播放平台 成人性爱视频久久操 女性真人生殖系统双性人视频 下身插入b射精视频 明星潜规测视频 mp4 免賛a片直播绪 国内 自己 偷拍 在线 国内真实偷拍 手机在线 国产主播户外勾在线 三桥杏奈高清无码迅雷下载 2五福电影院凸凹频频 男主拿鱼打女主,高宝宝 色哥午夜影院 川村まや痴汉 草溜影院费全过程免费 淫小弟影院在线视频 laohantuiche 啪啪啪喷潮XXOO视频 青娱乐成人国产 蓝沢润 一本道 亚洲青涩中文欧美 神马影院线理论 米娅卡莉法的av 在线福利65535 欧美粉色在线 欧美性受群交视频1在线播放 极品喷奶熟妇在线播放 变态另类无码福利影院92 天津小姐被偷拍 磁力下载 台湾三级电髟全部 丝袜美腿偷拍自拍 偷拍女生性行为图 妻子的乱伦 白虎少妇 肏婶骚屄 外国大妈会阴照片 美少女操屄图片 妹妹自慰11p 操老熟女的b 361美女人体 360电影院樱桃 爱色妹妹亚洲色图 性交卖淫姿势高清图片一级 欧美一黑对二白 大色网无毛一线天 射小妹网站 寂寞穴 西西人体模特苍井空 操的大白逼吧 骚穴让我操 拉好友干女朋友3p