Role of Phosphorus and Inoculation with <i>Bradyrhizobium</i> in Enhancing Soybean Production

Mirriam, Akello; Mugwe, Jayne; Nasar, Jamal; Kisaka, Oscar; Ranjan, Shivani; Gitari, Harun

doi:https://doi.org/10.1155/2023/3231623

Advances in Agriculture

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Review Article | Open Access

Volume 2023 | Article ID 3231623 | https://doi.org/10.1155/2023/3231623

Role of Phosphorus and Inoculation with Bradyrhizobium in Enhancing Soybean Production

Akello Mirriam,¹Jayne Mugwe,¹Jamal Nasar,²Oscar Kisaka,³Shivani Ranjan,⁴and Harun Gitari¹

Academic Editor: Ijaz Ahmad

Received10 Aug 2022

Revised25 Mar 2023

Accepted15 Apr 2023

Published23 May 2023

Abstract

Soybean (Glycine max L. Merril) is among the key oil seed crops worldwide, providing several benefits from human consumption to the enhancement of soil productivity. In Uganda, legumes are cultivated on roughly 1.5 million ha, with soybean being produced on a lower production area of 150,000 ha compared to beans (925,000 ha) and groundnuts (253,000 ha). In terms of achievable yield, soybean emerges the highest at 1.2 t·ha⁻¹ as compared to beans (0.5 t·ha⁻¹) and groundnuts (0.7 t·ha⁻¹). Despite the smallest production coverage area, the crop’s feasible grain yield is projected at 4.6 t·ha⁻¹ under optimal environmental conditions. The major bottleneck to the crop’s production is the decreasing soil fertility, mainly caused by low nitrogen (N) but also phosphorus (P) levels in the soil. There is a high potential for supplying N from the atmosphere through biological N fixation (BNF), a natural process mediated by the symbiotic bacteria Bradyrhizobium japonicum, which requires optimum P levels for effective N fixation and increased yield. The current work reviews the present status of soybean production in Uganda, highlights its ecological requirements, importance, and constraints, and proposes the use of inoculation and P application to boost its production.

1. Introduction

Soybean, which belongs to the family Fabaceae, is the most important legume oil seed crop to many people globally and particularly in the tropics [1–3]. Integration of grain legumes into farming systems enhances soil fertility and increases household incomes [4–6]. Indeed, legume provides the cheapest source of protein for vegetarians by supplementing mineral and vitamin requirements [7, 8]. Soybean provides dietary proteins for not only human but also animal feed in the form of soy meal, which makes up approximately 98% of global livestock feed [6, 9]. In addition to being utilized as a source of biodiesel fuel, soybean accounts for nearly 30% of the global refined vegetable oil [10, 11].

In Uganda, Ronner and Giller [12] documented that legumes are grown on around 1.5 million hectares. Soybean, which is cultivated on 150,000 ha comes third in cultivated land after common beans (925,000 ha) and groundnuts (253,000 ha). Even though common beans occupy a hefty share with nearby a third of the cultivated land, soybean in its place displays the most favorable efficiency with a yield of 1.2 t·ha⁻¹ as related to 0.7 t·ha⁻¹ for ground nuts and 0.5 t·ha⁻¹ for beans [13]. In comparison, in Uganda, Mutegi and Zingore [14] estimated a 100% increase in soybean yield under integrated soil fertility management (ISFM) technologies. The transformation and modernization of the agricultural sector to increase productivity have been embraced by the Ugandan government, which in 2010 introduced the vegetable oil development project. The aim was to support soybean and other oilseed-producing farmers in terms of increasing yields and value chain development [15].

Despite its importance, soybean yield has remained low in sub-Saharan Africa (SSA). For instance, AASR [16] stated a low legume yield of less than 1 t·ha⁻¹ and Mutegi and Zingore [17] reported a stagnated average legume yield of about 0.7 t·ha⁻¹ contrary to the expected 3 t·ha⁻¹, which exacerbates food insecurity in SSA. The major cause of such low productivity is low soil fertility caused by insufficiencies in mostly N and P [18–22]. Low soil fertility is equally attributed to negative nutrient balances for these minerals resulting from low use of inorganic fertilizers, leaching, and continuous nutrient mining through crop harvests [23–26].

Declining soil fertility coupled with traditional varieties has a negative effect on soybean production [5, 15]. This is particularly so because farmers are less informed and less willing to adopt high-yielding varieties and ISFM production technologies like BNF. For instance, a 30% increase in soybean production has been reported globally with the embracing of new varieties and better crop management techniques [27]. In Uganda, a study by CRAFT [28] revealed that with inoculation, 4,100 farmers harvested 1450 t of soybean as compared to their previous harvest of 1,040 without inoculation. Therefore, integration of inoculated improved soybean varieties into most cropping systems in the tropics, Uganda inclusive, could help a great deal in increasing N fixation and boosting soybean economic returns.

2. General Information about Soybean Production

Globally, soybean has emerged as the most valued legume crop in relation to not only overall production but also international trade [2, 29]. The world’s leading soybean producers include Brazil, the USA, Argentina, India, and China, with 34, 31, 18, 11, and 9 million ha dedicated to soybean cultivation, respectively [30]. Akibode and Meredia [31]; noted that over 75% of the pulses harvested in Asia and SSA come from rain-fed production systems. Subsequently, this has resulted in a 0.4% negligible increase in crop yield in the last 10 years, from 800 to 850 kg·ha⁻¹ [13, 31]. Specifically, the on-farm soybean yield in SSA is 700 kg·ha⁻¹, a value that is nearly four times below the achievable yield of 3000 kg·ha⁻¹ recorded in station studies. This could be due to the different management efforts highly accrued to the research station fields as compared to the on-farm conditions. The low crop yields reported on smallholder farms have exacerbated poverty, food insecurity, and malnutrition in many parts of SSA [14].

Ohyama et al. [32] reported that soybean yield could increase up to 4.6 t·ha⁻¹ under prime environmental (climatic and soil) conditions. However, the USA and Japan have reported greater potential soybean yields of 10 and 8 t·ha⁻¹, respectively [32, 33]. Hence, soybean productivity potential could be maximized than we have thought if proper soil and crop management practices are used [34].

There has been a substantial upsurge in soybean production over the years. In Uganda, soybean production was done in less than 100 ha till the 1990s, when the area cultivated increased steadily (Figure 1). Nonetheless, the yield stagnated at around a ton per ha. In the last decade, the country’s soybean production has been faring well compared to some key African nations. For instance, her annual production is approximately 49000 t, compared to Egypt (3900 t), Kenya (2400 t), Rwanda (24000 t), Ethiopia (97000 t), and South Africa (1018000 t) (Table 1). Her mean yield is 1.01 t·ha⁻¹, a figure that is above that of Rwanda (0.5 t·ha⁻¹) and yet far below those of Egypt (3.2) and Ethiopia (2.2).

Soybean production is common in the Northern and Eastern regions of the country [35] (Figure 2). According to UBOS [35]; in the seasons of 2008/2009, northern Uganda produced 16,000 Mt of soybean, which was harvested from 26,000 ha. Western Uganda followed with 2000 Mt being produced from 2000 ha, whilst the Central region produced 200 Mt from an area of 1000 ha. Thereafter, the soybean production area remained stagnant, after a steep increase that was observed between 2000 and 2003 [12]. In 2008, Kasese among the six national evaluation locations recorded the uppermost mean grain yield of 2385 kg·ha⁻¹ while Hoima recorded the lowermost mean yield of 935 kg·ha⁻¹. In a similar study conducted by UBOS [36], the Lango subregion ranked as the largest producer with 73,969 t, followed by Busoga with 11,095 t, Acholi with 6,161 t, and lastly Bukedi with 5,603 t. The northern region had the highest soybean production area (26,195 ha), followed by eastern (7,279 ha), Western (2,220 ha), and Central (750 ha) [36].

(a)

(b)

Soybean production in Uganda has steadily been increasing, but due to the soybean leaf rust disease outbreak, its growth stagnated, hence devastating soybean production farmers throughout the country in the past years. The Soybean Breeding and Seed Systems Program, in partnership with the Ministry of Agriculture, Animal Industry, and Fisheries (MAAIF), Regional Universities Forum for Agricultural Development (RUFORUM), National Crops Resources Research Institute (NaCCRI), Alliance for a Green Revolution in Africa (AGRA), and soybean Africa immensely and successfully bred, released and recommended early maturing, better yielding, and rust-resistant soybean varieties from 2004 to 2013. Among the new varieties released were, Namsoy 4M and Maksoy 1N in 2004, Maksoy 2N in 2008, Maksoy 3N in 2010, whereas, Maksoy 5N and Maksoy 4N were released in 2013. There has been an increase in the adoption of these improved soybean varieties particularly in Uganda, for commercial production, resulting in an increase in soybean yield of up to about 2500 kg per hectare. This has provided a high source of income and an affordable protein source for Uganda’s poor rural population [37].

In SSA, the total land area under soybean production covers about 1.3%, while the world soybean production accounts for 0.6%. Whereas in the past four decades’ soybean average yield in SSA was very low (1.1 t·ha⁻¹) compared to the world average (2.4 t·ha⁻¹). For example, in 2016/2017, the mean soybean yields in South Africa, Nigeria, Zambia, and Uganda were 2.29, 0.96, 1.94, and 0.6 t·ha⁻¹, respectively [5].

Globally, two soybean traits make it largely popular due to its high oil (20%) and protein content (40%), which all emanate from processed seed. Soybean, among crops, has proven to be the highest legume oilseed in protein content per unit area. In fact, Uganda’s science-led interventions contributed to the steady rise in soybean production from as low as 158,000 ha in 2004 to a higher value of 180,000 ha in 2010 [35].

2.1. Economic Importance of Soybean

Pulse crops are essential sources of not only nutrition and food but also energy that contribute around 30% of crop production globally [10, 11]. Soybean, as a grain legume, plays a key role in fixing atmospheric N [3, 38]. In addition, it is a crucial source of not only micronutrients but also macronutrients and vital secondary metabolites that are key components to promote health [39, 40]. It is also a critical source of dietary proteins and amino acids such as valine, methionine, cystine, tyrosine, theonine, isoleucine, tryptophan, phenylalanine, and lysine, which are critical components of the protoplasm and de-oxyribo nucleic acid [41].

Soybean is composed of about 42% proteins and 20% oils [42], in addition to fat-soluble vitamins, which are used to produce many products such as lecithin [43]. This could be a good alternative to quite expensive protein-rich foods like fish and chicken, particularly in developing nations [42]. In many parts of the SSA countries, it provides about 4% of the daily calorie intake, whilst, in Latin America and South Africa, it provides about 3% of the daily protein intake. Thus, soybean remains to be an important crop, especially for vegetarians [44].

Agricultural food legume crops such as soybean are very significant in developing nations since they are accountable for addressing both food and nutritional uncertainty [8, 31, 45]. They are very crucial for livestock and human nutrition [9, 46]. In reality, they serve as rotation crops, where they furnish cereal crops with N besides helping in reducing soil pathogens [3, 8, 34, 47–49]. Many legumes form synergy associations with bacteria that have the capability of fixing atmospheric N [6, 45, 50]. For example, in Brazil, the quantity of organic N formed in such relations of rhizobia and legumes is about 20 million tons per year, with soybeans, in precise, have been observed to fix around 300 kg N·ha⁻¹ [3, 6, 51].

According to Giller and Wilson [52] and Giller [53]; the BNF input in terms of total N uptake through symbiotic N fixation for soybean, pulses, groundnut, and sugar cane is 67, 55, 65, and 17%, respectively. The average percentage of crop N extracted from atmospheric N is almost 70% worldwide, so legume N fixation in agroecosystems is considered the most significant source of N in soils. Although it mostly fixes the N for its use, if the residues (above ground and roots) are incorporated back into the soil, it would reduce the N demand of the cereals in the rotation by 40% [48].

In many farming systems, food legumes such as soybeans often serve as a feed crop, obtaining higher price values than cereals, and they are progressively cultivated to complement the income of farmers [4, 54]. Thus, this is an economically important crop for trade both in international and local markets, with the largest exporters of soybean being the USA, Brazil, Argentina, and China [55]. In Uganda, soybean has been reported to contribute to about 1% of the gross domestic product majorly due to exports to the neighbouring countries between the years 2008 and 2009 [36]. For instance, Ssengedo et al. [56] observed an increase in export earnings of soybean in Uganda from USD 300,000 in 2006 to USD 1,163,000 in 2009, accounting for a 288% increase. In 2019, the country’s total soybean export volume was 1150 t against a total export value of USD 722,440. Thus, due to their economic importance, legume crops, and specifically soybeans have become central targets not only from the environmental and biotechnological point of view but also for agricultural research [3, 50, 57].

2.2. Constraints to Soybean Production

Many biotic and abiotic factors have inhibited soybean production, which includes low soil fertility status and minimal soil moisture content [5, 57]. The abiotic factors can further be categorized into edaphic and climatic factors [58].

2.2.1. Biotic Constraints

Many diseases affect the yield of soybean globally, such as red leaf blotch, leaf spot, anthracnose stem, fusarium wilt, charcoal rot, blight brown stem rot, stem blight phytophthora root rot, stem rot pod, and alfalfa mosaic, whereby the intensity varies depending on the location [59]. Specifically, in Uganda, the yield of this crop is severely affected by soybean leaf rust (Phakopsorapachyrihizi Syd) (Figure 3).

In recent times, soybean leaf rust has become the most destructive soybean foliar disease and can cause up to approximately 90% loss of yield [37] if not well controlled. This disease has become endemic in areas where soybean is grown, having been first identified in Uganda in 1996, showing symptoms that include yellowing of leaves and tan sporulating lesions [12]. Leaf rust remains a problem in soybean production. Nonetheless, with the introduction of new varieties such as Maksoy 1N, 2N, 3N, 4N, and 5N, which were introduced between 2004 and 2015, there has been increased resistance to soybean leaf rust, thus leading to increased yields [55]. Insect pests are also of economic importance in soybean production. These pests include pod-sucking and defoliating insects like aphids that suck the young succulent green part of the soybean plant and sucking bugs that suck the contents of pods and soft plant parts [60]. During storage, the grains are susceptible to attack by storage moths.

2.2.2. Abiotic Constraints

The average soybean yield (grain) in tropical Africa is relatively low at 1000 kg ha⁻¹ in comparison with 2500–3500 kg·ha⁻¹ attainable in developed nations [61]. This is largely ascribed to the lack of better varieties, which is a major determent of soybean production in African countries. In other areas, low grain yield is compounded by pod-shattering, especially in the dry savannah environment with high average temperatures and low average rainfall [44, 62], which further reduces yield [58, 63, 64].

Some farmers have failed to use rhizobia due to inaccessibility and ignorance, and there is a problem of fake seeds on the market and a lack of promiscuous soybean varieties [65]. A study by N₂Africa [66] indicated a total number of 17,297 farmers who adopted inoculation, comprising 11,245 women (65%) and 6,052 men (35%) (Table 2). In some African countries, farmers too lack interest in soybean production due to lower soybean grain demand and a lack of soybean processing equipment.

3. Biological Nitrogen Fixation

Sustainable agriculture in recent studies is increasingly gaining fame as a means to address the above-mentioned challenges. These are technologies that focus to increase the availability of N, enhancing legume productivity, and production systems that improve economic and ecological environmental conservation [6, 49, 67–71]. BNF is an alternative example that can supply N, reduce the high cost of N fertilizers, and subsequently limit the environmental footprint of N [72]. Oil seed legumes such as groundnut (Arachis hypogaea L.) and soybean are more efficient in fixing N, estimated globally at 6.3 times greater BNF when combined yearly (18.5 Tg·year⁻¹) compared with food legumes like common beans (0.58 Tg), chickpea (Cicer arietinum L.) (0.60 Tg), pea (Pisum sativum L.) (0.57 Tg), and other pulses (0.47 Tg) [73]. Therefore, soybean is very pertinent in BNF.

The process of changing inert N₂ to biologically utilizable NH₄ is termed biological N fixation, in which only bacteria (rhizobia) mediate the process in nature [74]. Through the process of forming nodules, legumes such as soybeans have gained the capability to absorb N₂ gas from the atmosphere. The legume plant provides the bacteria with photosynthesis energy in the form of C, and it reciprocates by fixing N₂ gas into an available form for plant uptake [53, 77].

By optimizing the symbiotic relationship of rhizobia with soybean, under optimal conditions such as limitless critical nutrients such as P and Mo, the legume can fix up to 300 kg N·ha⁻¹ [10, 11, 76, 77]. P and sometimes K are critical nutrients that mostly limit soybean production [52, 53]. The optimal efficiency of N fixation requires the presence of a satisfactory quantity of not only compatible but also effective rhizobia strains in the rhizosphere [52].

These root nodule-occupying rhizobia originate either from the commercial inoculants, for whom a total of 4,100 farmers in the year 2020 inoculated soybean and harvested 1,449,610 kg (1450 tonnes) of soybean from a total of 995 ha of land, or from the native rhizobia in the soil [28, 48]. With P being one of the essential elements that enhance the association, it requires that its supply be maintained at a certain optimum level for adequate yields to be attained, and this can be done only by periodically replenishing it through the use of mineral fertilizers [23, 78–80]. Besides P promoting rhizobia growth, it also encourages root nodulation, which consequentially enhances the BNF process [45, 81–83]. Findings by Dugje et al. [84] and Adjei-Nsiah et al. [85, 86] revealed that although P is very important in rhizobia inoculation of soybean, the increase in soybean yield is usually less compared to the crop’s feasible grain yield, which is projected at 3 t·ha⁻¹.

Nonetheless, the high cost of the fertilizers is a key drawback to their wide application by farmers [48], more so if the appropriate P application rate is not well known. The high cost of fertilizers and high soil degradation due to a lack of knowledge on the optimum application P rates continuously lead to low crop, yields exacerbating famine in some sub-Saharan countries, a problem that has become a jinx for researchers to fix [23]. Exploiting low-cost alternatives of N sources through heightening the normal biological N fixation (BNF) in legumes such as soybean may be a judicious substitute if the cost of farming is to be lowered. Optimal nutrient use efficiency and productivity will be improved, besides decreasing the related environmental penalties of the use of N fertilizers [23, 51, 87].

The number of native bacterial strains in the rhizosphere is often insufficient to induce substantial N-fixation [34]. Hence, inoculation of soybean legumes improves the process of fixation of N through BNF [48]. This is due to the increased development of root nodules, which houses the B. japonicum that enhances atmospheric N use by the plants [88].

Nitrogen is a main (macro) nutrient with momentous roles in the production of amino acids in legumes. It is also necessary for plant growth due to its key role in cell division [89]. It promotes vegetative growth and chlorophyll foliage. Specifically, it enhances photosynthesis and forms an important constituent of vitamins besides helping in the manufacture of carbohydrates, affecting both plant and plant energy reactions [90–92]. Soybean inoculation with particular Bradyrhizobium strains increases N uptake, dry biomass weight, and grain yield [48, 53, 92, 93]. This farming practice is gaining popularity among the SSA nations. For instance, in 2020, 4,100 farmers inoculated soybean in Uganda and harvested 1,450 t of soybean produced from 995 ha, compared to a previous low average yield of 1,040 t [28].

The use of BNF knowledge comprising Rhizobium inoculants in legumes can be a feasible substitute for pricy fertilizers, principally when targeting improved legume production [3, 70, 94]. Shahid et al. [95] reported that if a low number of native rhizobia strains prevail, inoculation with well-suited and sufficient rhizobia with optimal P levels may be necessary and is a key component that farmers may use to maximize yields.

The value of rhizobia is not well recognized and understood by farmers [96, 97]. In Uganda, a study by Wortmann and Kaizzi [98] showed that most farmers seldom inoculate soybeans but instead cultivate nonpromiscuous varieties that rarely nodulate in the presence of native rhizobium strains. Moreover, biological N₂-fixation was low due to weak P availability. Soybean N-balances can be improved with inoculation, resulting in a 30–70% rise in yield [45, 99]. Wortmann and Kaizzi [98] and Rwakaikara-silver and Nkwiine [96] observed that although soybean plants were able to nodulate without the application of inoculation, there was still a yield improvement of about 600 kg·ha⁻¹ when inoculant and fertilizer were combined. With inoculation and P-fertilizer use, only 21 demonstrations and 221 adaption trials were set up by AFRST. In northern Uganda, a total of 1440 farmers harvested 496,882 kg of soybean, while in eastern Uganda, 2000 farmers harvested 30 tons of soybean [66].

A lot of N is needed for high-yielding soybean plants and an estimated 70% of the plant’s N is supplied through BNF [51, 96, 100]. Salvagiotti et al. [101] and Bhuiyan et al. [94] also noted that BNF supplied about 60% of the N needed by soybean plants. When introduced into a new place with soils that has inadequate rhizobia, soybeans respond most strongly to inoculation [100]. As cited by Abdul-Latif [101]; rhizobia inoculation resulted in increased nodulation subsequently increasing grain yield.

In another study, soybean trials were conducted for three consecutive years between 2009 and 2012 in Uganda, Kenya, Rwanda, Tanzania, and Malawi. The results indicated that without inoculation, planting soybeans with P fertilizer might increase soybean yields by approximately 100 percent relative to conventional farming practices with no inoculation added. There was a further increase in soybean yields by 70% with basal P application over yields without both P and inoculation. Several studies clearly showed that grain legume yields heightened further at the establishment stage when provided with small doses of N [91, 98, 102]. This is necessary before nodule production for meeting N demand. The influence of externally (organic or inorganic) supplied N on the efficiency of N legume fixation is restricted after complete nodulation [17].

4. Effects of Phosphorus (P) on Biological Nitrogen Fixation (BNF)

Globally, P is a critical element that lacks a related atmospheric gaseous component in its biogeochemical cycle [103–106]. Hence, this implies that besides its native source, which is the weathering of parent material, it can also be recycled from organic P compounds [107, 108].

In soybeans, P is at its greatest demand during production (seed and pod development stages), where over 60% of P ultimately ends up being translocated into these organs [109]. A study by DAFF [110] revealed that very high soil P levels reduce not only the seed protein but also oil content, and further noted that the crop yield optimally with available P (Olsen P) of about 30 kg P·ha⁻¹. Nevertheless, reports are indicating a negligible increase in soybean yield when the concentration of soil P is more than 20 mg·kg⁻¹ [111–113]. This calls for appropriate P-use efficiency in soybean farming.

Improving P utilization is important in lowering P fertilizer costs, thereby guaranteeing not only high yield but also optimal economic benefits at harvest [67, 103, 114–117]. Unfortunately, in tropical soils, P is generally limited [19, 103, 118, 119]. This is because of its high fixation coupled with its slow mobility, for it reacts chemically with oxides of Al as well as that of Fe or gets bound in organic form [77, 120, 121], rendering it inaccessible for plant uptake. Thus, rendering the efficient use of P is of high global importance since it is an essential and critical element [103].

Turan et al. [122] observed that approximately 80% of the soil P is fixed with calcium, magnesium, iron, and aluminium oxides; hence, its availability for plant root uptake varies greatly with P source, soil pH, and drainage. The optimal P obtainability to plants is customarily recorded at a pH range of 6-7 [123]. However, tropical soils are generally acidic, which exacerbates the situation of P fixation, and hence, crops show P shortages despite the total P content normally exceeding the plants’ requirements in those types of soils [120, 122, 124, 125].

Under acidic soil conditions, it is vital to increase P use efficacy though such practice can be difficult specifically because of its low mobility [122, 124, 128, 127]. Therefore, to boost P efficiency, it is advisable to utilize the existing soil resources to offset the P exploitation, principally through crop harvest [78, 128, 129]. Exemplary, in soybeans, P removal through harvest is estimated to be at 81% of the total P that is utilized in plant tissue [130, 131]. Phosphorus is highly required by plants, specifically during their initial growth stages [1]. This calls for appropriate P levels in soybean production and inoculation for higher BNF to enhance root nodulation that will fix appreciable amounts of N and hence attain high growth and grain yield. This will therefore lead to great economic returns for soybean.

On the other hand, the ultimate N source in agroecosystems is BNF, which is a process that encompasses a weighty amount of P [48, 94]. With the limited application of P, rhizobia activity and N fixation are decreased. Early development of lateral, fibrous, and stable roots is stirred by P, rendering it very important for nodule growth and N fixation [1, 94].

According to Abdul-Latif [102]; inadequate P supply limits root development, sugar translocation, and the photosynthesis process among other functions that are directly influenced by N fixation in legume plants. Supplementing P stimulates crop growth by snowballing BNF, hence improving the availability of macronutrients in legumes [48, 94]. Nyoki and Ndakidemi [132]; Akpalu et al. [133]; and Bhuiyan et al. [94] recounted that synergetic use of P and beneficial bacteria like Bradyrhizobiium in legume plants improved growth, nodulation, and consequently grain yield as compared to the isolated use of any of the two. Phosphorus supplementation and Bradyrhizobium inoculation heightened the absorption of P, N, and K into the several organs of the entire soybean plant [132, 133].

Phosphorus is among the essential nutrients and is of great importance in BNF in legumes. A lot of energy is needed to facilitate this symbiotic process, which has a high demand for P [83, 134] to enhance metabolism [134–136]. Many reports indicated a strong P sink concentration in nodules, usually exceeding that of shoots and roots [110, 111, 137]. Nitrogen-fixing plants require more P as compared with N-supplied plants [132, 138]. Therefore, the application of P could boost its uptake and utilization in the establishment, growth, initiation of nodule formation, and nodule primordia increase, improving yield, quality of the crop, and function of nodules [75, 135], rhizobial strain’s growth [137, 139], and host plant growth [137, 140]. Studies by Jones et al. [140] and Sa and Israel [111] proved that P increases the number of root nodules, and their weights, as well as enhances the pod yield. However, Jacobsen [142] and Graham and Rosas [143] revealed that the application of P increases N fixation by stimulating the growth of the host plant.

Application of P fertilizer together with inoculants of rhizobium affected not only the nodulation but also the N fixation of legume [94, 144]. Similar patterns were also noted by Hoque and Haq [145] on treating various legumes with P and rhizobium, which noticed a rise in the growth and nodulation. It is widely accepted, however, that the soybean response to the application of phosphatic fertilizer is dependent on crop, climate, and management practices [34].

In crop development, P plays key roles such as boosting energy storage and its transfer, flowering, root growth stimulation, nodule production, seed formation, and N₂ fixation [146]. Subsequently, the application of P can also upsurge the legumes’ leaf surface area, promote root elongation and grain size; the concentration of N in biomass and grain, and the number of nodules [147, 148]. The process of N₂ fixation in legumes is susceptible to P insufficiency, leading to reduced nodule mass [94].

Nodules are an effective P sink, where its concentration in nodules typically exceeds that of shoots and roots [111, 137, 140, 149]. Thus, treating P-deficient soils with inorganic phosphatic fertilizer results in an increased number of nodules [148, 150, 151]. Nevertheless, Bremer and Mulvaney [152] observed increased dry matter and grain yield with the P use at the rate of 45 kg·ha⁻¹ with no effect on N₂ fixation, suggesting that the host legume was more receptive than the rhizobia to P application. Therefore, P management under P-deficient soils is critical for achieving high soybean yields. Soil factors such as low P levels, on the other hand, aggravate pod abortion, thereby decreasing soybean yield [149]. Soybean crop response to P has also been observed by Mallarino and Reuben [153] to be based on soil available P. Further, in another study, it was noted that P application is unlikely to boost yield above 12 mg·kg⁻¹ at soil P concentration [154].

Phosphorus plays the most significant role among the important nutrients in the BNF process in legumes like soybean posing a great concern for nutrient availability [155]. The demand for symbiotic N fixation is high since the process expends high energy [134, 136], and the metabolism of energy production depends intensely on P availability [135, 136]. Cassman et al. [138] noted that N fixation was more enhanced in soybean plants with P application than with N supplied. The P application is very important in the development and growth of nodules [75, 151]. Jacobsen [142] and Graham and Rosas [143] noted, however, that P fertilization improves symbiotic N fixation by encouraging the growth of host plants rather than directly affecting the growth and functioning of nodules.

5. Effects of Inoculation on Soybean P Uptake and Yield

The number of native bacterial strains in the rhizosphere is often insufficient to induce substantial N-fixation [34]. Hence, inoculation of soybean legumes improves the process of fixation of N through BNF [48]. This is due to the increased development of root nodules, which houses the B. japonicum that enhances atmospheric N use by the plants [88].

Nitrogen is a main (macro) nutrient with momentous roles in the production of amino acids in legumes. It is also necessary for plant growth due to its key role in cell division [89]. It promotes vegetative growth and chlorophyll foliage. Specifically, it enhances photosynthesis and forms an important constituent of vitamins besides helping in the manufacture of carbohydrates, affecting both plant and plant energy reactions [90–92]. Soybean inoculation with particular Bradyrhizobium strains increases the N uptake, dry biomass weight, and grain yield [48, 53, 93]. This farming practice is gaining popularity among the SSA nations. For instance, in 2020, 4,100 farmers inoculated soybean in Uganda and harvested 1,450 t of soybean produced from 995 ha, compared to a previous low average yield of 1,040 t [28].

Synergetic inoculation with rhizobium and application of P significantly improved p uptake in soybeans (Figure 4). Consequently, this affects growth, nodule formation, and yield in soybean production [45, 48, 93, 95, 156]. In Uganda, while applying P at a rate of 15 kg·ha⁻¹ in soybeans, Otieno et al. [45] and Kaizzi et al. [144] that observed it resulted in significant yield gains and profitability (Figure 5). Explicitly, under P application and inoculation, treatments that received 15 kg P·ha⁻¹ recorded the highest yield of 1.2 t·ha⁻¹, which was 30% higher than control. This translated to a net income of US$ 414.93. In a separate study by Wortmann et al. [157]; yield upsurge was only eminent with the use of triple superphosphate mineral fertilizer (TSP) but not with an organic P supplied using Busumbu rock phosphate (9% P), as observed by Ronner and Giller [12]. Moreso, from a study carried out in Palisa Uganda, by Ebanyat [23]; soybean yields only showed a moderate response to the use of 30 kg P·ha⁻¹.

The value of rhizobia is not well recognized and understood by farmers [96, 97]. In Uganda, a study by Wortmann and Kaizzi [98] revealed that most farmers seldom inoculate soybeans but instead cultivate nonpromiscuous varieties that rarely nodulate in the presence of native rhizobium strains. Moreover, biological N₂-fixation was low due to weak P availability. Soybean N-balances can be improved with inoculation, resulting in a 30–70% rise in yield [45, 99]. Wortmann and Kaizzi [98] and Rwakaikara-silver and Nkwiine [96] observed that even though soybean plants were able to nodulate deprived of the inoculation, there was a yield enhancement of roughly 600 kg·ha⁻¹ when fertilizer and inoculant were combined. With inoculation and P-fertilizer use, only 21 demonstrations and 221 adaption trials were set up by AFRST. In northern Uganda, a total of 1440 farmers harvested 496,882 kg of soybean, while in eastern Uganda, 2000 farmers harvested 30 tons of soybean [66].

A lot of N is required for high-yielding soybean, with a projected 70% of the plant’s N being provided through BNF [51, 96, 100]. Bhuiyan et al. [94] and Salvagiotti et al. [101] also noted that BNF provided around 60% of the N required by soybean plants. Once introduced in a new area where the soils have insufficient rhizobia, soybeans respond well to inoculation (Abdul-Latif [102]). As noted by Van Kessel and Hartley [100]; rhizobia inoculation resulted in improved nodulation, consequently increasing grain yield.

In another study, soybean trials were conducted for three consecutive years between 2009 and 2012 in Uganda, Kenya, Rwanda, Tanzania, and Malawi. The results indicated that without inoculation, planting soybeans with P fertilizer might increase soybean yields by approximately 100 percent relative to conventional farming practices with no inoculation added. There was a further increase in soybean yields by 70% with basal P application over yields without both P and inoculation. Several studies clearly showed that grain legume yields heightened further at the establishment stage when provided with small doses of N [94, 98, 102]. This is necessary before nodule production for meeting N demand. The influence of externally (organic or inorganic) supplied N on the efficiency of N legume fixation is restricted after complete nodulation [14].

6. Conclusion and Recommendations

The review has demonstrated the greatest economic and industrial potential for soybean production in Uganda. This provides a leeway impetus for its increased production, especially in regions among others, the northern part exhibiting good climatic conditions with high production potential. The chief limiting factor in soybean production in the study area is declining soil fertility which stems from P and N as the most critical and limiting nutrients. Due to the nature of tropical soils, which are highly weathered and acidic, P is usually fixed in the soil making it inaccessible for crop uptake and use. N is also lost from the soil pool through many pathways such as leaching, denitrification, evapotranspiration, and crop harvest among others, and this leads to the negative N nutrient balance in the soil ecosystem.

Biological N fixation using a compatible strain, Bradyrhizobium japonicum, is an environmentally friendly and affordable measure of engaging the bacteria in the rhizosphere to enhance the BNF process through root nodulation. Root nodulation can positively influence soybean growth and yield due to an enhanced N₂ fixation by the bacteria and P applied, which facilitates faster root establishment. Therefore, with inoculation, soybean N-balances can be enhanced, leading to an increment in grain yield. Synergetic inoculation with rhizobium and application of P significantly influence growth, nodule formation, and yield in soybean production. Specifically, the study revealed a yield of over 1 t·ha⁻¹ with P and inoculation against a value of below 0.7 t·ha⁻¹ without the inputs. Unfortunately, farmers are not well informed about the prominence of rhizobia in fixing atmospheric N in the soil for legumes like soybean, which would be a cheaper option than the expensive inorganic N fertilizer. This calls for more farmer sensitization on the benefits of BNF with the use of optimum P.

Data Availability

No data were used to support this study.

Conflicts of Interest

The authors declare that they have no conflicts of interest. The work reported in this study was carried out by Mirriam, a Master’s degree student, who was funded by the East African Council in 2019.

References

M. Khanam, M. S. Islam, M. H. Ali, I. F. Chowdhury, and S. M. Masum, “Performance of soybean under different levels of phosphorus and potassium,” Bangladesh Agronomy Journal, vol. 19, no. 1, pp. 99–108, 2016.
View at: Publisher Site | Google Scholar
M. M. Rahman, M. M. Hossain, M. P. Anwar, and A. S. Juraimi, “Plant density influence on yield and nutritional quality of soybean seed,” Asian Journal of Plant Sciences, vol. 10, no. 2, pp. 125–132, 2011.
View at: Publisher Site | Google Scholar
J. Jena, S. Maitra, A. Hossain et al., “Role of legumes in cropping system for soil ecosystem improvement,” Ecosystem Services: Types, Management and Benefits, Nova Science Publishers, Inc, Suite N Hauppauge, NY, USA, 2022.
View at: Google Scholar
W. Mhango, “Nitrogen budgets in legume based cropping systems in northern Malawi,” Dissertation Abstracts International, vol. 72, no. 3, 2011.
View at: Google Scholar
E. Joachim, Soybean Production in Uganda. Determinants, Problems and Improvements, GRIN Verlag publishers, Munich, Germany, 2021.
W. dos Santos Sousa, R. P. Soratto, D. S. Peixoto et al., “Effects of Rhizobium inoculum compared with mineral nitrogen fertilizer on nodulation and seed yield of common bean. A meta-analysis,” Agronomy for Sustainable Development, vol. 42, no. 3, p. 52, 2022.
View at: Publisher Site | Google Scholar
K. Joshi, M. Asokan, K. Datta, and P. Kumar, “Socioeconomic constraints to legumes production in rice-wheat cropping systems of India,” Legumes in rice and Wheat Cropping Systems of the Indo-Gangetic Plain - Constraints and Opportunities, International Crops Research Institute for the Semi-Arid Tropics, Patancheru, AP, India, pp. 176–184, 2000.
View at: Google Scholar
M. A. Haile, N. N. Karanja, S. O. Nyawade et al., “Lupin and Lima beans diminish Potatoes’ N and P uptake, uptake efficiency and use efficiency,” Potato Research, 2023.
View at: Publisher Site | Google Scholar
P. Goldsmith, Economics of Soybean Production, Marketing and Utilization, University of Illinois, Champaign, IL, United States, 2008.
P. H. Graham and C. P. Vance, “Legumes: importance and constraints to greater use,” Plant Physiology, vol. 131, no. 3, pp. 872–877, 2003.
View at: Publisher Site | Google Scholar
A. Bulent, M. Abdullah, and M. Fereidouni, “Soybeans processing for biodiesel production,” Soybean - Applications and Technology, Intechopen, London, UK, 2011.
View at: Google Scholar
E. Ronner and E. K. Giller, Background Information on Agronomy, Farming Systems and Ongoing Projects on Grain Legumes in Uganda, Gates Open Research, Seattle, WA, USA, 2013.
Fao, “FAOSTAT- food and agriculture organization of the united nations,” FAO, Rome, Italy, 2022.
View at: Google Scholar
J. Mutegi and S. Zingore, Closing Crop Yield Gaps in Sub-saharan Africa through Integrated Soil Fertility Management, IPNI-Sub-Saharan Africa Program, Nairobi, Kenya, 2013.
D. Debnath and S. C. Babu, “Prospects for sustainable intensification of soybean production in sub-Saharan Africa,” African Journal of Agricultural and Resource Economics, vol. 15, no. 4, pp. 365–371, 2020.
View at: Publisher Site | Google Scholar
Aasr- Africa Agriculture Status Report, Focus on Staple Crops Nairobi Kenya Alliance for a Green Revolution in Africa, AGRA, Kigali, Rwanda, 2013.
J. Mutegi and S. Zingore, “Closing crop yield gaps in Sub‐Saharan Africa through integrated soil fertility management,” International Plant Nutrition Institute ISFM Policy Highlights, Norcross, GA, USA, 2013.
View at: Google Scholar
P. A. Sanchez, Properties and Management of Soils in the Tropics, Cambridge University Press, Cambridge, England, vol. 124, no. 3, 1997.
M. A. Otieno, H. I. Gitari, B. Danga, and A. N. Karuma, “Soil properties and fertility management with respect to Capsicum (Capsicum annuum L.) production in Nairobi Peri-urban Counties,” Journal of Soil Science and Plant Nutrition, vol. 22, no. 1, pp. 374–392, 2021.
View at: Publisher Site | Google Scholar
R. Mwadalu, B. Mochoge, M. Mwangi, and H. Gitari, “Heightening sorghum nitrogen uptake while maintaining optimal soil nutrient levels through mineral fertiliser application,” Journal of Applied Life Sciences and Environment, vol. 54, no. 4, pp. 458–472, 2022.
View at: Publisher Site | Google Scholar
R. Mwadalu, B. Mochoge, M. Mwangi, S. Maitra, and H. Gitari, “Response of Gadam sorghum (Sorghum bicolor) to farmyard manure and inorganic fertilizer application,” International Journal of Agriculture Environment & Biotechnology, vol. 15, no. 1, pp. 51–60, 2022.
View at: Publisher Site | Google Scholar
E. R. Mwakidoshi, H. I. Gitari, E. M. Muindi, A. Wamukota, M. F. Seleiman, and S. Maitra, “Smallholder farmers’ knowledge on the use of bioslurry as a soil fertility amendment input for potato production in Kenya,” Land Degradation & Development, 2023.
View at: Publisher Site | Google Scholar
P. Ebanyat, “A road to food: efficacy of nutrient management options targeted to heterogeneous soils capes in the Teso farming system, Uganda,” Environmental Microbiology, vol. 47, pp. 278–282, 2009.
View at: Google Scholar
M. Oscar Kisaka, C. Shisanya, L. Cournac, J. Raphael Manlay, H. Gitari, and J. Muriuki, “Integrating no-tillage with agroforestry augments soil quality indicators in Kenya’s dry-land agroecosystems,” Soil and Tillage Research, vol. 227, Article ID 105586, 2023.
View at: Publisher Site | Google Scholar
H. I. Gitari, C. K. K. Gachene, N. N. Karanja, S. Kamau, S. Nyawade, and E. Schulte-Geldermann, “Potato-legume intercropping on a sloping terrain and its effects on soil physico-chemical properties,” Plant and Soil, vol. 438, no. 1-2, pp. 447–460, 2019.
View at: Publisher Site | Google Scholar
I. O. Ochieng’, H. I. Gitari, B. Mochoge, E. Rezaei-Chiyaneh, and J. P. Gweyi-Onyango, “Optimizing maize yield, nitrogen efficacy and grain protein content under different N forms and rates,” Journal of Soil Science and Plant Nutrition, vol. 21, no. 3, pp. 1867–1880, 2021.
View at: Publisher Site | Google Scholar
G. Barrows, S. Sexton, and D. Zilberman, “Agricultural biotechnology: the promise and prospects of genetically modified crops,” The Journal of Economic Perspectives, vol. 28, no. 1, pp. 99–120, 2014.
View at: Publisher Site | Google Scholar
Craft-Climate Resilient Agribusiness for Tomorrow, “Over 4,100 Ugandan farmers reap higher soybean yields,” 2020, https://snv.org.
View at: Google Scholar
M. K. Abbasi, M. Manzoor, and M. M. Tahir, “Efficiency of Rhizobium inoculation and P fertilization in enhancing nodulation, seed yield, and phosphorus use efficiency by field grown soybean under hilly region of Rawalakot Azad Jammu and Kashmir, Pakistan,” Journal of Plant Nutrition, vol. 33, no. 7, pp. 1080–1102, 2010.
View at: Publisher Site | Google Scholar
Latifundist, “TOP 10 soybean producing countries in 2019,” 2019, https://latifundist.com.
View at: Google Scholar
S. Akibode and M. Maredia, Global and Regional Trends in Production, Trade and Consumption of Food Legume Crops, Department of Agricultural, Food and Resource Economics Michigan State University, East Lansing, MI, USA, 2011.
T. Ohyama, R. Minagawa, S. Ishikawa et al., Soybean seed production and nitrogen nutrition, vol. 6, pp. 116–143, 2012.
View at: Publisher Site
C. C. Zoundji, P. Houngnandan, H. M. Amidou, A. F. Kouleo, and F. Toukourou, “Inoculation and phosphorus application effects on Soybean (Glycine max (L.) Merrill). Productivity growth in farmers’ fields in Benin,” The journal of Animal and plant Sciences, vol. 25, no. 5, pp. 1384–1392, 2015.
View at: Google Scholar
T. Fairhurst, Ed., Handbook for Integrated Soil Fertility Management, Africa Soil Health Consortium, Nairobi, Kenya, 2012.
Ubos–Uganda Bureau of Statistics, “Uganda census of agriculture 2008/2009,” Tech. Rep., UBOS, Kampala, Uganda, 2010, Volume IV: Crop Area and Production Report.
View at: Google Scholar
Ubos–Uganda Bureau of Statistics, “Where are the farmers in Uganda? Spatial Distribution of farmers by important characteristics,” In Collaboration with Ministry of Agriculture, Animal Industry and Fisheries, Uganda Bureau of Statistics, Kabanyoro, Uganda, 2013.
View at: Google Scholar
P. Tukamuhabwa and T. Obua, Soybean Production Guide in Uganda, Makerere University Agricultural Research Institute, Kabanyoro, Uganda, 2015.
M. Ali and S. Kumar, “Major technology advances in Pulses,” Journal for Food Legume, vol. 23, pp. 169–185, 2009.
View at: Google Scholar
M. J. Messina, “Legumes and soybeans: overview of their nutritional profiles and health effects,” The American Journal of Clinical Nutrition, vol. 70, no. 3, pp. 439–450, 1999.
View at: Publisher Site | Google Scholar
P. J. White and P. H. Brown, “Plant nutrition for sustainable development and global health,” Annals of Botany, vol. 105, no. 7, pp. 1073–1080, 2010.
View at: Publisher Site | Google Scholar
H. S. Laswai, J. J. Mpagalile, V. C. K. Silayo, and W. R. Ballegu, “Use of soybeans in food formulation in Tanzania,” Proceedings of the First National Soybean Stakeholders Workshop, Sokoine University of Agriculture, Morogoro, Tanzania, pp. 52–59, 2005.
View at: Google Scholar
A. H. M. N. Anwar, A. K. Podder, M. A. Hasem, P. Bala, and M. , A. Islam, “Effect of Bradyrhizobium inoculants on the growth and yield of soybean varieties PB-1 and G-2,” Journal of Soil Nature, vol. 4, no. 1, pp. 39–48, 2010.
View at: Google Scholar
T. Hymowitz, R. J. Singh, and K. P. Kollipara, “The genomes of the Glycine,” Plant Breeding Reviews, pp. 289–311, 1998.
View at: Google Scholar
Usda–United States Department of Agriculture, Ongoing Verification of Product Formulation and Labelling Targeting the Eight Most Common (“Big 8”) Food Allergens, Food Safety and Inspection Service, Washington, DC, USA, 2018.
M. A. Otieno, H. I. Gitari, B. Danga, A. N. Karuma, S. Maitra, and H. I. Gitari, “Aggrandizing soybean yield, phosphorus use efficiency and economic returns under phosphatic fertilizer application and inoculation with Bradyrhizobium,” Journal of Soil Science and Plant Nutrition, vol. 22, no. 1, pp. 374–392, 2022.
View at: Publisher Site | Google Scholar
I. Zarei, Y. Sohrabi, G. R. Heidari, A. Jalilian, and K. Mohammadi, “Effects of biofertilizers on grain yield and protein content of two soybean (Glycine max L.) cultivars,” African Journal of Biotechnology, vol. 11, no. 27, pp. 7028–7037, 2012.
View at: Publisher Site | Google Scholar
S. Nyawade, H. I. Gitari, N. N. Karanja et al., “Enhancing climate resilience of rain-fed potato through legume intercropping and silicon application,” Frontiers in Sustainable Food Systems, vol. 4, Article ID 566345, 2020.
View at: Publisher Site | Google Scholar
M. Unkovic, D. Herridge, M. Peoples et al., Measuring Plant-Associated Nitrogen Fixation in Agricultural Systems Measuring Plant-Associated Nitrogen Fixation in Agricultural Systems, Clarus Design Pty Ltd, Canbera, Australia, 2 edition, 2008.
M. A. Raza, H. Gul, J. Wang et al., “Land productivity and water use efficiency of maize-soybean strip intercropping systems in semi-arid areas: a case study in Punjab Province, Pakistan,” Journal of Cleaner Production, vol. 308, Article ID 127282, 2021.
View at: Publisher Site | Google Scholar
K. Lindström, M. Murwira, A. Willems, and N. Altier, “The biodiversity of beneficial microbe-host mutualism: the case of rhizobia,” Research in Microbiology, vol. 161, no. 6, pp. 453–463, 2010.
View at: Publisher Site | Google Scholar
F. D. Herridge, B. M. Peoples, and M. R. Boddey, “Global inputs of Biological nitrogen fixation in Agricultural systems,” Plant and Soil, vol. 311, 2008.
View at: Publisher Site | Google Scholar
E. K. Giller and K. J. Wilson, Nitrogen Fixation in Tropical Cropping System, C.A.B. International, Wallingford, England, 1991.
K. E. Giller, Nitrogen Fixation in Tropical Cropping Systems, Cabi Series, CABI Publishing series, Wallingford, England, 2 edition, 2001.
S. Nedumaran, P. Abinaya, P. Jyosthnaa, B. Shraavya, R. Parthasarathy, and B. Cynthia, Grain Legumes Production, Consumption and Trade Trends in Developing Countries, International Crops Research Institute for the Semi-Arid Tropics, Telangana, India, 2015.
P. Tukamuhabwa and H. K. Oloka, Soybean Research and Development in Uganda: A Case of Paradigm Shift in an African University, Makerere University Agricultural Research Institute, Kabanyoro, Uganda, 2016.
M. Ssengendo, J. Mayende, and R. Mubiru, “Soybean fact sheet: export potential of the soybean sub-sector in Uganda,” A Survey Carried out by Participants of the COMESA Training done by International Trade Center (ITC) to Assess the Export Potential of Soybean Industry, Uganda Export Promotion Board, Kampala, Uganda, 2010.
View at: Google Scholar
R. P. Singh, N. Shankar, and P. K. Jaiwal, Nitrogen Nutrition and Sustainable Plant Productivity, Stadium press, LLC, Houston, TX, USA, 2012.
C. K. Ssekabembe, Introduction to Agronomy, Principles and Practices, Fountain publishers, Kampala, Uganda, 2010.
W. Allen, Soybean Cyst Nematode Management Guide, University of Missouri Division of Plant Sciences, Columbia, MO, USA, vol. 573, 2012.
E. A. Heinrichs and R. Muniappan, Integrated Pest Management for Tropical Crops: Soyabeans, CABI Publishing series, Wallingford, England, 2018.
S. Irwin and D. Good, The 2014 U.S. Average Soybean Yield: Headed for a New Record? Farmdoc Daily, Department of Agricultural and Consumer Economics, University of Illinois at Urbana-Champaign, Champaign, IL, USA, 2014.
M. F. Seleiman, M. T. Aslam, B. A. Alhammad et al., “Salinity stress in wheat: effects, mechanisms and management strategies,” Phyton-International Journal of Experimental Botany, vol. 91, no. 4, pp. 667–694, 2021.
View at: Publisher Site | Google Scholar
P. R. Rubaihayo, P. Tukamuhabwa, K. Dashiell, and E. Adipala, “Inheritance of resistance to pod shattering in soybean,” African Crop Science Journal, vol. 8, no. 3, 2000.
View at: Publisher Site | Google Scholar
R. Goher, H. M. Alkharabsheh, M. F. Seleiman et al., “Impacts of heat shock on productivity and quality of Triticum aestivum L. at different growth stages,” Notulae Botanicae Horti Agrobotanici Cluj-Napoca, vol. 51, no. 1, Article ID 13090, 2023.
View at: Publisher Site | Google Scholar
Mak, “MUAP-makerere university annual report,” 2013, https://pdd.mak.ac.ug.
View at: Google Scholar
N₂Africa, “Putting nitrogen fixation to work for smallholder farmers in Africa,” 2019, https://www.n2africa.org.
R. P. Soratto, M. J. Perdoná, R. J. Parecido, R. N. Pinotti, and H. I. Gitari, “Turning biennial into biannual harvest: long-term assessment of Arabica coffee–macadamia intercropping and irrigation synergism by biological and economic indices,” Food and Energy Security, vol. 11, no. 2, 2022.
View at: Publisher Site | Google Scholar
J. Nasar, G. Y. Wang, F. J. Zhou et al., “Nitrogen fertilization coupled with foliar application of iron and molybdenum improves shade tolerance of soybean under maize soybean intercropping,” Frontiers of Plant Science, vol. 13, Article ID 1014640, 2022a.
View at: Publisher Site | Google Scholar
J. Nasar, G. Y. Wang, S. Ahmad et al., “Nitrogen fertilization coupled with iron foliar application improves the photosynthetic characteristics, photosynthetic nitrogen use efficiency, and the related enzymes of maize crops under different planting patterns,” Frontiers of Plant Science, vol. 13, Article ID 988055, 2022b.
View at: Publisher Site | Google Scholar
M. A. Raza, H. S. Yasin, H. Gul et al., “Maize/soybean strip intercropping produces higher crop yields and saves water under semi-arid conditions,” Frontiers of Plant Science, vol. 13, Article ID 1006720, 2022.
View at: Publisher Site | Google Scholar
S. P. Paudyal and V. N. P. Gupta, “Substitution of chemical fertilizer nitrogen through Rhizobium inoculation technology,” Our Nature, vol. 16, no. 1, pp. 43–47, 2018.
View at: Publisher Site | Google Scholar
H. Shibata, J. N. Galloway, A. M. Leach et al., “Nitrogen footprints: Regional realities and options to reduce nitrogen loss to the environment,” Ambio, vol. 46, no. 2, pp. 129–142, 2017.
View at: Publisher Site | Google Scholar
D. L. N. Rao and D. Balachandar, “Nitrogen inputs from biological nitrogen fixation in Indian agriculture,” The Indian Nitrogen Assessment: Sources of Reactive Nitrogen, Environmental and Climate Effects, Management Options, and Policies, Elsevier, Amsterdam, The Netherlands, pp. 117–132, 2017.
View at: Publisher Site | Google Scholar
A. Coskan and K. Dog, “Symbiotic nitrogen fixation in soybean,” Soybean Physiology and Biochemistry, 2011.
View at: Publisher Site | Google Scholar
S. H. Waluyo, T. A. Lie, and L. Mannetje, “Effect of phosphate on nodule primordia of soybean (Glycine max Merrill) in acid soils in rhizotron experiment,” Indonesian Journal of Agricultural Science, vol. 5, no. 2, pp. 37–44, 2016.
View at: Publisher Site | Google Scholar
J. M. Grossman, M. E. Schipanski, T. Sooksanguan, S. Seehaver, and L. E. Drinkwater, “Diversity of rhizobia in soybean [Glycine max (Vinton)] nodules varies under organic and conventional management,” Applied Soil Ecology, vol. 50, 2011.
View at: Publisher Site | Google Scholar
M. W. Hill, B. G. Hopkins, V. D. Jolley, and B. L. Webb, “Phosphorus mobility through soil increased with organic acid-bonded phosphorus fertilizer (Carbond® P),” Journal of Plant Nutrition, vol. 38, no. 9, pp. 1416–1426, 2015.
View at: Publisher Site | Google Scholar
J. N. Mugo, N. N. Karanja, C. K. Gachene, K. Dittert, H. I. Gitari, and E. Schulte-Geldermann, “Response of potato crop to selected nutrients in Central and Eastern highlands of Kenya,” Cogent Food & Agriculture, vol. 7, no. 1, Article ID 1898762, 2021.
View at: Publisher Site | Google Scholar
G. W. Sileshi, B. Jama, B. Vanlauwe et al., “Nutrient use efficiency and crop yield response to the combined application of cattle manure and inorganic fertilizer in sub-Saharan Africa,” Nutrient Cycling in Agroecosystems, vol. 113, no. 2, pp. 181–199, 2019.
View at: Publisher Site | Google Scholar
S. Heydarzadeh, C. Arena, E. Vitale et al., “Impact of different fertilizer sources under supplementary irrigation and rain-fed conditions on eco-physiological responses and yield characteristics of dragon's head (Lallemantia iberica),” Plants, vol. 12, no. 8, p. 1693, 2023.
View at: Publisher Site | Google Scholar
N. Sanging, R. Abaidoo, K. Dashiell, R. Carsky, and A. Okogun, “Persistence and effectiveness of rhizobia nodulating promiscuous soybeans in moist savanna zones of Nigeria,” Applied Soil Ecology, vol. 3, pp. 215–224, 1996.
View at: Publisher Site | Google Scholar
G. O’Hara, “Nutritional constraints on root nodule bacteria affecting symbiotic nitrogen fixation: a review,” Australian Journal of Experimental Agriculture, vol. 41, no. 3, pp. 417–433, 2001.
View at: Publisher Site | Google Scholar
S. Danso, “Biological nitrogen fixation in tropical agrosystems: twenty years of biological nitrogen fixation research in Africa,” Biological Nitrogen Fixation and Sustainability of Tropical Agriculture, IITA, Ibadan, Nigeria, 1992.
View at: Google Scholar
I. Dugje, L. Omoigui, F. Ekeleme, R. Bandyopadhyay, P. L. Kumar, and A. Kamara, Farmers’ Guide to Soybean Production in Northern Nigeria, International Institute of Tropical Agriculture, Ibadan, Nigeria, 2009.
S. Adjei-Nsiah, B. U. Alabi, J. K. Ahiakpa, and F. Kanampiu, “Response of grain legumes to phosphorus application in the Guinea savanna agroecological zones of Ghana,” Agronomy Journal, vol. 110, no. 3, pp. 1089–1096, 2018.
View at: Publisher Site | Google Scholar
S. Adjei-Nsiah, J. Kumah, E. Owusu-Bennoah, and F. Kanampiu, “Influence of P sources and rhizobium inoculation on growth and yield of soybean genotypes on ferric Lixisols of Northern Guinea savanna zone of Ghana,” Communications in Soil Science and Plant Analysis, vol. 50, no. 7, pp. 853–868, 2019.
View at: Publisher Site | Google Scholar
M. Jawad Hassan, M. Ali Raza, S. Ur Rehman et al., “Effect of cadmium toxicity on growth, oxidative damage, antioxidant defense system and cadmium accumulation in two sorghum cultivars,” Plants, vol. 9, no. 11, p. 1575, 2020.
View at: Publisher Site | Google Scholar
S. Tamiru, M. P. Lalit, and A. Tsige, “Effects of inoculation by Bradyrhizobium japonicum strains on nodulation, nitrogen fixation, and yield of soybean (Glycine max (L) merill) varieties on nitisols of bako western Ethiopia,” International Scholarly Research Notices, vol. 2012, Article ID 261475, 8 pages, 2012.
View at: Publisher Site | Google Scholar
R. Uchida, “Essential nutrients for plant growth: nutrient functions and deficiency symptoms,” Plant Nutrient Management in Hawaii’s Soils, University of Hawaii, Honolulu, HI, USA, 2000.
View at: Google Scholar
S. Sara, M. Morad, and C. M. Reza, “Effects of seed inoculation by Rhizobium strains on Chlorophyll content and protein percentage in common bean cultivars (Phaseolus vulgaris L.),” International Journal of Biosciences, vol. 3, no. 3, pp. 1–8, 2013.
View at: Publisher Site | Google Scholar
J. Nasar, W. Khan, M. Z. Khan et al., “Photosynthetic activities and photosynthetic nitrogen use efficiency of maize crop under different planting patterns and nitrogen fertilization,” Journal of Soil Science and Plant Nutrition, vol. 21, no. 3, pp. 2274–2284, 2021.
View at: Publisher Site | Google Scholar
J. Nasar, C. J. Zhao, R. Khan et al., “Maize-soybean intercropping at optimal N fertilization increases the N uptake, N yield and N use efficiency of maize crop by regulating the N assimilatory enzymes,” Frontiers of Plant Science, vol. 13, Article ID 1077948, 2022.
View at: Publisher Site | Google Scholar
A. Javaid and N. Mahmood, “Growth, nodulation, and yield response of soybean to biofertilizers and organic manures,” Plant Journal of Botany, vol. 42, no. 2, pp. 863–871, 2010.
View at: Google Scholar
M. M. H. Bhuiyan, M. M. Rahman, F. Afroze, G. N. C. Sutradhar, and M. S. I. Bhuiyan, “Effect of phosphorus, molybdenum and Rhizobium inoculation on growth and nodulation of mungbean. Scientific Officer, RARS, Hathazari, Chittagong,” Journal of Soil Nature, vol. 2, no. 2, pp. 25–30, 2008.
View at: Google Scholar
M. Q. Shahid, M. F. Saleem, H. Z. Khan, and S. A. Anjum, “Performance of soybean (Glycine max L.) under different phosphorus levels and inoculation.in Pakistan,” Journal of Agricultural Sciences, vol. 46, no. 4, pp. 237–241, 2009.
View at: Google Scholar
M. C. Rwakaikara-Silver and C. Nkwiine, “A review of work on rhizosphere microbiota in Uganda,” African Journal of Ecology, vol. 45, no. s2, pp. 20–26, 2007.
View at: Publisher Site | Google Scholar
E. V. Tairo and P. A. Ndakidemi, “Macronutrient Uptake in soybean as affected by Bradyrhizobium japonicum inoculation and phosphorus (P) supplements,” American Journal of Plant Sciences, vol. 5, no. 4, pp. 488–496, 2014.
View at: Publisher Site | Google Scholar
C. S. Wortmann and C. K. Kaizzi, “Nutrient balances and expected effects of alternative practices in farming systems of Uganda,” Agriculture, Ecosystems & Environment, vol. 71, no. 1-3, pp. 115–129, 1998.
View at: Publisher Site | Google Scholar
C. Nkwiine and M. C. Rwakaikara-Silver, “Status of research on soil microsymbionts in Uganda,” African Journal of Ecology, vol. 45, no. 2, pp. 27–35, 2007.
View at: Publisher Site | Google Scholar
C. Van Kessel and C. Hartley, “Agricultural management of grain legumes: has it led to an increase in nitrogen fixation,” Field Crops Research, vol. 65, no. 2-3, pp. 165–181, 2000.
View at: Publisher Site | Google Scholar
F. Salvagiotti, K. G. Cassman, J. E. Specht, D. T. Walters, A. Weiss, and A. Dobermann, “Nitrogen uptake, fixation and response to fertilizer N in soybeans: a review,” Field Crops Research, vol. 108, pp. 1–13, 2008.
View at: Publisher Site | Google Scholar
A.-A. Abdul-Latif, Contribution of Rhizobium and Phosphorus Fertilizer to Biological Nitrogen Fixation and Grain Yield of Soybean in the Tolon District, Faculty of Agriculture, Kwame Nkrumah University of Science and Technology, Kumasi, Ghana, 2013.
H. I. Gitari, N. Shadrack, S. Kamau, N. N. Karanja, C. K. K. Gachene, and E. Schulte-Geldermann, “Agronomic assessment of phosphorus efficacy for potato (Solanum tuberosum L) under legume intercrops,” Journal of Plant Nutrition, vol. 43, no. 6, pp. 864–878, 2020.
View at: Publisher Site | Google Scholar
R. Mikkelsen, “Sources of Phosphorus for plants: past, present, and future,” Better Crops with Plant Food, International Plant Nutrition Institute (IPNI), Peachtree Corners, GA, USA, 2019.
View at: Publisher Site | Google Scholar
R. P. Cheptoek, H. I. Gitari, B. Mochoge et al., “Maize productivity, economic returns and phosphorus use efficiency as influenced by lime, Minjingu Rock Phosphate and NPK inorganic fertilizer,” International Journal of Bioresource Science, vol. 8, pp. 47–60, 2021.
View at: Publisher Site | Google Scholar
P. J. A. Withers, “Closing the phosphorus cycle,” Nature Sustainability, vol. 2, no. 11, pp. 1001-1002, 2019.
View at: Publisher Site | Google Scholar
C. Lemming, A. Oberson, J. Magid et al., “Residual phosphorus availability after long-term soil application of organic Waste,” Agriculture, Ecosystems & Environment, vol. 270–271, 2019.
View at: Publisher Site | Google Scholar
A. Rahimi, H. Gitari, G. Lyons, S. Heydarzadeh, M. Tuncturk, and R. Tuncturk, “Effects of vermicompost, compost and animal manure on vegetative growth, physiological and antioxidant activity characteristics of Thymus vulgaris L. Under water stress,” Uzuncu Yil University Journal of Agricultural Sciences, vol. 33, no. 1, pp. 40–53, 2023.
View at: Publisher Site | Google Scholar
N. R. Usherwood, Nutrient Management for Top-Profit Soybeans, 1998, https://www.ppi-ppic.org.
Daff-Department of Agriculture Forestry and Fisheries, “Soybeans production guideline, RSA, DPP,” 2010, https://www.agriculture.gov.au/.
View at: Google Scholar
T. M. Sa and D. W. Israel, “Energy status and functioning of phosphorus deficient soybean nodules,” Plant Physiology, vol. 97, no. 3, pp. 928–935, 1991.
View at: Publisher Site | Google Scholar
R. Borges and A. P. Mallarino, “Broadcast and deep-band placement of phosphorus and potassium for soybean managed with ridge tillage,” Soil Science Society of America Journal, vol. 67, no. 6, pp. 1920–1927, 2003.
View at: Publisher Site | Google Scholar
J. R. Webb, A. P. Mallarino, and A. M. Blackmer, “Effects of residual and annually applied phosphorus on soil test values and yields of corn and soybean,” Journal of Production Agriculture, vol. 5, no. 1, pp. 148–152, 1992.
View at: Publisher Site | Google Scholar
M. Hernandez and F. Cuevas, “The effect of inoculating with Arbuscular mycorrhiza and Brady rhizobium strains on soybean (Glycine max (L.) Merrill) crop development,” Cultivos Tropicales, vol. 24, no. 2, pp. 19–21, 2003.
View at: Google Scholar
R. J. Parecido, R. P. Soratto, M. J. Perdoná et al., “Limestone increased coffee yield and profitability more than phosphogypsum or their combination,” Agronomy Journal, vol. 113, no. 4, pp. 3586–3599, 2021.
View at: Publisher Site | Google Scholar
E. J. Veneklaas, H. Lambers, J. Bragg et al., “Opportunities for improving phosphorus-use efficiency in crop plants,” New Phytologist, vol. 195, no. 2, pp. 306–320, 2012.
View at: Publisher Site | Google Scholar
M. A. Sarwar, M. Tahir, A. Tanveer, and M. Yaseen, “Evaluating role of plant growth promoting rhizobacteria for improving phosphorus use efficiency and productivity in sunflower (Helianthus annuus),” International Journal of Agriculture and Biology, vol. 18, pp. 881–888, 2016.
View at: Publisher Site | Google Scholar
S. O. Nyawade, C. K. K. Gachene, N. N. Karanja, H. I. Gitari, E. Schulte-Geldermann, and M. Parker, “Controlling soil erosion in smallholder potato farming systems using legume intercrops,” Geoderma Regional, vol. 17, Article ID 00225, 2019.
View at: Publisher Site | Google Scholar
H. I. Gitari, N. N. Karanja, C. K. K. Gachene, S. Kamau, K. Sharma, and E. Schulte-Geldermann, “Nitrogen and phosphorous uptake by potato (Solanum tuberosum L.) and their use efficiency under potato-legume intercropping systems,” Field Crops Research, vol. 222, pp. 78–84, 2018.
View at: Publisher Site | Google Scholar
I. G. Harun, E. M. Benson, and O. D. Benjamin, “Effect of lime and goat manure on soil acidity and maize (Zea mays) growth parameters at Kavutiri, Embu County – Central Kenya,” Journal of Soil Science and Environmental Management, vol. 6, no. 10, pp. 275–283, 2015.
View at: Publisher Site | Google Scholar
S. Faridvand, E. Rezaei-Chiyaneh, M. Battaglia, H. Gitari, M. A. Raza, and K. H. M. Siddique, “Application of bio and chemical fertilizers improves yield, and essential oil quantity and quality of Moldavian balm (Dracocephalum moldavica L.) intercropped with mung bean (Vigna radiata L.),” Food and Energy Security, vol. 11, no. 2, 2021.
View at: Publisher Site | Google Scholar
M. Turan, N. Ataoglu, and F. Sahin, “Evaluation of the capacity of phosphate solubilizing bacteria and fungi on different forms of phosphorus in liquid culture,” Journal of Sustainable Agriculture, vol. 28, no. 3, pp. 99–108, 2006.
View at: Publisher Site | Google Scholar
P. Anthony, G. Malzer, M. Zhang, and S. Sparrow, “Soil nitrogen and phosphorus behavior in a long‐term fertilization experiment,” Agronomy Journal, vol. 104, no. 5, pp. 1223–1237, 2012.
View at: Publisher Site | Google Scholar
C. Li, T. W. Kuyper, W. Van der Werf et al., “Testing for complementarity in phosphorus resource use by mixtures of crop species,” Plant and Soil, vol. 439, no. 1-2, pp. 163–177, 2019.
View at: Publisher Site | Google Scholar
P. J. White, T. S. George, P. J. Gregory, A. G. Bengough, P. D. Hallett, and B. M. McKenzie, “Matching roots to their environment,” Annals of Botany, vol. 112, no. 2, pp. 207–222, 2013.
View at: Publisher Site | Google Scholar
P. Hinsinger, E. Betencourt, L. Bernard et al., “P for two, sharing a scarce resource: soil phosphorus acquisition in the rhizosphere of intercropped species,” Plant Physiology, vol. 156, no. 3, pp. 1078–1086, 2011.
View at: Publisher Site | Google Scholar
C. S. Wortmann, A. O. Esilaba, K. C. Kaizzi, C. Kibunja, K. W. Ndungu-Magiroi, and N. Maman, Fertilizer Use Issues for Smallholder Agriculture in Tropical Africa, Intechopen, London, UK, 2019.
C. J. Rosen, K. A. Kelling, J. C. Stark, and G. A. Porter, “Optimizing phosphorus fertilizer management in potato production,” American Journal of Potato Research, vol. 91, no. 2, pp. 145–160, 2014.
View at: Publisher Site | Google Scholar
G. M. Pierzynski, R. W. McDowell, and J. T. Sims, “Chemistry, cycling, and potential movement of inorganic phosphorus in soils,” Phosphorus: Agriculture and the Environment, ASA, CSSA, and SSSA, Madison, WI, USA, pp. 53–86, 2005.
View at: Google Scholar
A. Dobermann, K. G. Cassman, C. Mamaril, and J. E. Sheehy, “Management of phosphorus, potassium, and sulfur in intensive, irrigated lowland rice,” Field Crops Research, vol. 56, no. 1-2, pp. 113–138, 1998.
View at: Publisher Site | Google Scholar
A. Adeli, K. R. Sistani, D. E. Rowe, and H. Tewolde, “Manure management: broiler litter effects on soybean production and soil N and P,” Agronomy Journal, vol. 97, no. 1, pp. 314–321, 2005.
View at: Publisher Site | Google Scholar
D. Nyoki and A. P. Ndakidemi, “Effects of Bradyrhizobium japonicum and phosphorus supplementation on the productivity of legumes,” International Journal of Physical and Social Sciences, vol. 3, no. 7, pp. 884–910, 2014.
View at: Google Scholar
M. Akpalu, “Phosphorus application and rhizobia inoculation on growth and yield of soybean (Glycine max L. Merrill),” American Journal of Experimental Agriculture, vol. 4, no. 6, pp. 674–685, 2014.
View at: Publisher Site | Google Scholar
J. Schulze, G. Temple, S. J. Temple, H. Beschow, and C. P. Vance, “Nitrogen fixation by white lupin under phosphorus deficiency,” Annals of Botany, vol. 98, no. 4, pp. 731–740, 2006.
View at: Publisher Site | Google Scholar
D. W. Israel, “Investigation of the role of phosphorus in symbiotic dinitrogen fixation,” Plant Physiology, vol. 84, no. 3, pp. 835–840, 1987.
View at: Publisher Site | Google Scholar
W. C. Plaxton, “Plant response to stress: biochemical adaptations to phosphate deficiency,” Encyclopedia of Plant and Crop Science, Marcel Dekker, New York, NY, USA, pp. 976–980, 2004.
View at: Google Scholar
J. J. Drevon and U. A. Hartwig, “Phosphorus deficiency increases the argon-induced decline of nodule nitrogenase activity in soybean and alfalfa,” Plants, vol. 201, pp. 463–469, 1997.
View at: Publisher Site | Google Scholar
K. G. Cassman, A. S. Whitney, and R. L. Fox, “Phosphorus requirements of soybean and cowpea as affected by mode of N nutrition,” Agronomy Journal, vol. 73, no. 1, pp. 17–22, 1981b.
View at: Publisher Site | Google Scholar
K. Leung and P. J. Bottomley, “Influence of phosphate on the growth and nodulation characteristics of Rhizobium trifolii,” Applied and Environmental Microbiology, vol. 53, no. 9, pp. 2098–2105, 1987.
View at: Publisher Site | Google Scholar
D. N. Munns, J. S. Hohenberg, T. L. Righetti, and D. J. Lauter, “Soil acidity tolerance of symbiotic and nitrogen‐fertilized soybeans ¹,” Agronomy Journal, vol. 73, no. 3, pp. 407–410, 1981.
View at: Publisher Site | Google Scholar
G. D. Jones, J. A. Lutz, and T. J. Smith, “Effects of phosphorus and potassium on soybean nodules and seed yield ¹,” Agronomy Journal, vol. 69, no. 6, pp. 1003–1006, 1977.
View at: Publisher Site | Google Scholar
I. Jakobsen, “The role of phosphorus in nitrogen fixation by young pea plants (Pisum sativum),” Physiologia Plantarum, vol. 64, no. 2, pp. 190–196, 1985.
View at: Publisher Site | Google Scholar
P. H. Graham and J. C. Rosas, “Phosphorus fertilization and symbiotic nitrogen fixation in common bean,” Agronomy Journal, vol. 71, no. 6, pp. 925-926, 1979.
View at: Publisher Site | Google Scholar
K. C. Kaizzi, J. Byalebeka, O. Semalulu et al., “Optimizing smallholder returns to fertilizer use: bean, soybean and groundnut,” Field Crops Research, vol. 127, pp. 109–119, 2012.
View at: Publisher Site | Google Scholar
M. Hoque and M. F. Haq, Rhizobial Inoculation and Fertilization of Lentil in Bangladesh, FAO, Rome, Italy, 1994.
M. Marschner, “Marschner’s Mineral Nutrition of Higher Plants,” Academic Press, Cambridge, p. 649, 3rd edition, 2012.
View at: Google Scholar
T. R. Sinclair and V. Vadez, “Physiological traits for crop yield improvement in low N and P environments,” Plant and Soil, vol. 245, pp. 1–15, 2002.
View at: Publisher Site | Google Scholar
M. Yahiya, A. Futma, and A. Fatma, “Influence of phosphorus on nitrogen fixation in chickpea cultivars,” Journal of Plant Nutrition, vol. 18, no. 4, pp. 719–727, 1995.
View at: Publisher Site | Google Scholar
U. F. Chiezey, “Pod abortion and grain yield of soybean (Glycine max (L) Merrill) as influenced by nitrogen and phosphorous nutrition in the Northern Guinea Savanna zone of Nigeria,” Tropical Oilseeds Journal, pp. 61–10, 2001.
View at: Google Scholar
G. E. Tsevetkova and G. I. Georgiev, “Effect of phosphorus nutrition on the nodulation, nitrogen fixation and nutrient use efficiency of Bradyrhizobium japonicum. Soybean (Glycine Max L. Merr.) symbiosis,” Bulgerian Journal of Plant Physiology, vol. 3, pp. 331–335, 2003.
View at: Google Scholar
K. G. Cassman, D. N. Munns, and D. P. Beck, “Phosphorus nutrition of Rhizobium japonicum: strain differences in phosphate storage and utilization,” Soil Science Society of America Journal, vol. 45, no. 3, pp. 517–520, 1981.
View at: Publisher Site | Google Scholar
J. M. Bremner and C. S. Mulvaney, “Nitrogen-total,” Methods of soil analysis Part 2 Chemical and Microbiological Properties, American Society of Agronomy, Soil Science Society of America,, Madison, Wisconsin, pp. 595–624, 1982.
View at: Google Scholar
A. P. Mallarino and D. Rueben, Phosphorous and Potassium Fertilization and Placement Methods for Corn-Soybean Rotations Managed with No-Till and Chisel plough tillage, Iowa State University, Ames, IA , USA, 2005.
R. B. Ferguson, C. A. Shapiro, A. R. Dobermann, and C. S. Wortmann, “Fertilizer recommendation for soybeans,” Neb Guide G859, vol. 6, 2006.
View at: Google Scholar
G. Santachiara, F. Salvagiotti, and J. L. Rotundo, “Nutritional and environmental effects on biological nitrogen fixation in soybean: a meta-analysis,” Field Crops Research, vol. 240, pp. 106–115, 2019.
View at: Publisher Site | Google Scholar
F. K. Kumaga and K. Ofori, “Response of soybean (Glycine max (L.) merrill) to Bradyrhizobia inoculation and phosphorus application,” International Journal of Agriculture and Biology, vol. 6, no. 2, pp. 324–327, 2004.
View at: Publisher Site | Google Scholar
C. Wortmann, B. D. Mcintyre, and C. K. Kaizzi, “Annual soil improving legumes: agronomic effectiveness, nutrient uptake, nitrogen fixation and water use,” Field Crops Research, vol. 68, no. 1, pp. 75–83, 2000.
View at: Publisher Site | Google Scholar

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