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<front>
<journal-meta>
<journal-id journal-id-type="publisher-id">Front. Agron.</journal-id>
<journal-title>Frontiers in Agronomy</journal-title>
<abbrev-journal-title abbrev-type="pubmed">Front. Agron.</abbrev-journal-title>
<issn pub-type="epub">2673-3218</issn>
<publisher>
<publisher-name>Frontiers Media S.A.</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="doi">10.3389/fagro.2022.1004771</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Agronomy</subject>
<subj-group>
<subject>Mini Review</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>Prospects of rhizobial inoculant technology on Bambara groundnut crop production and growth</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Fwanyanga</surname>
<given-names>Felicitas M.</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/1933745"/>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Horn</surname>
<given-names>Lydia N.</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/321839"/>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Sibanda</surname>
<given-names>Timothy</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author" corresp="yes">
<name>
<surname>Reinhold-Hurek</surname>
<given-names>Barbara</given-names>
</name>
<xref ref-type="aff" rid="aff3">
<sup>3</sup>
</xref>
<xref ref-type="author-notes" rid="fn001">
<sup>*</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/370635"/>
</contrib>
</contrib-group>
<aff id="aff1">
<sup>1</sup>
<institution>Department of Biochemistry, Microbiology, and Biotechnology, University of Namibia</institution>, <addr-line>Windhoek</addr-line>, <country>Namibia</country>
</aff>
<aff id="aff2">
<sup>2</sup>
<institution>Zero Emissions Research Initiative, Multi-disciplinary Research Services, University of Namibia</institution>, <addr-line>Windhoek</addr-line>, <country>Namibia</country>
</aff>
<aff id="aff3">
<sup>3</sup>
<institution>CBIB Center for Biomolecular Interactions Bremen, Department of Microbe-Plant Interactions, Faculty of Biology and Chemistry, University of Bremen</institution>, <addr-line>Bremen</addr-line>, <country>Germany</country>
</aff>
<author-notes>
<fn fn-type="edited-by">
<p>Edited by: Ajit Singh, University of Nottingham Malaysia Campus, Malaysia</p>
</fn>
<fn fn-type="edited-by">
<p>Reviewed by: Mustapha Mohammed, University for Development Studies, Ghana;Abe Shegro Gerrano, Agricultural Research Council of South Africa (ARC-SA), South Africa</p>
</fn>
<fn fn-type="corresp" id="fn001">
<p>*Correspondence: Barbara Reinhold-Hurek, <email xlink:href="mailto:breinhold@uni-bremen.de">breinhold@uni-bremen.de</email>
</p>
</fn>
<fn fn-type="other" id="fn002">
<p>This article was submitted to Plant-Soil Interactions, a section of the journal Frontiers in Agronomy</p>
</fn>
</author-notes>
<pub-date pub-type="epub">
<day>29</day>
<month>09</month>
<year>2022</year>
</pub-date>
<pub-date pub-type="collection">
<year>2022</year>
</pub-date>
<volume>4</volume>
<elocation-id>1004771</elocation-id>
<history>
<date date-type="received">
<day>27</day>
<month>07</month>
<year>2022</year>
</date>
<date date-type="accepted">
<day>12</day>
<month>09</month>
<year>2022</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright &#xa9; 2022 Fwanyanga, Horn, Sibanda and Reinhold-Hurek</copyright-statement>
<copyright-year>2022</copyright-year>
<copyright-holder>Fwanyanga, Horn, Sibanda and Reinhold-Hurek</copyright-holder>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/">
<p>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.</p>
</license>
</permissions>
<abstract>
<p>After peanuts and cowpeas (<italic>Vigna unguiculata</italic>), the Bambara groundnut (<italic>Vigna subterranea</italic> (L.) Verdc) is the third most significant food legume in Africa. It is characteristically grown in marginal soils, is drought tolerant, and also has the potential for nitrogen fixation. Despite that, year-on-year Bambara groundnut yields are on a gradual decline due to a combination of abiotic and biotic stresses such as uneven annual rainfall and climate-induced changes in soil microbial community compositions, negatively impacting food security. Thus, the application of rhizobial inoculants at planting significantly improves yields in many leguminous crops. Moreover, symbiotic inoculants are well established in developed countries for improving nitrogen fixation and productivity in grain legumes. Sub-Saharan African countries, however, still under-utilise the above practice. In crop production, nitrogen (N) is the most frequently deficient nutrient since it stimulates root and shoots growth. Whereas nitrogen fertilisers can be used to supplement soil N levels, they are, however, also costly, at times inadequate, may not be timely in supply and may have deleterious environmental consequences. Hence, rhizobial inoculants are seen as a cheaper, easier, and safer method for improving N-fixation and crop productivity in grain legumes, as a result, smallholder farming systems are food secure. Thus, identifying the most efficient rhizobial strains for biofertiliser production for Bambara groundnut is of utmost importance to the farming communities.</p>
</abstract>
<kwd-group>
<kwd>Bambara groundnuts</kwd>
<kwd>food security</kwd>
<kwd>legumes (Fabaceae)</kwd>
<kwd>productivity</kwd>
<kwd>biofertiliser</kwd>
<kwd>rhizobia</kwd>
</kwd-group>
<counts>
<fig-count count="1"/>
<table-count count="0"/>
<equation-count count="0"/>
<ref-count count="66"/>
<page-count count="7"/>
<word-count count="3318"/>
</counts>
</article-meta>
</front>
<body>
<sec id="s1" sec-type="intro">
<title>Introduction</title>    <p>
<italic>Leguminosae</italic>, which has more than 770 genera and 19,500 species, is the third-largest land plant family (<xref ref-type="bibr" rid="B36">Liu et&#xa0;al., 2011</xref>; <xref ref-type="bibr" rid="B52">Ren, 2018</xref>). Additionally, behind cereals, leguminous are the second-most produced crops (<xref ref-type="bibr" rid="B6">Belete et&#xa0;al., 2019</xref>). There are many native legume species in Africa where the highest levels of global legume diversity are found (<xref ref-type="bibr" rid="B58">Sprent et&#xa0;al., 2010</xref>). According to <xref ref-type="bibr" rid="B39">Mfilinge et&#xa0;al. (2014)</xref>; <xref ref-type="bibr" rid="B8">B&#xfc;chi et&#xa0;al. (2015)</xref>; <xref ref-type="bibr" rid="B46">Phillips and Saunders (2016)</xref>, and other sources, legumes are grown as fodder, seed crops, as cover crops along cash crops or in conjunction with other crops. The capacity of legumes to fix atmospheric nitrogen has been credited with their ability to dominate many unfavourable and disturbed ecosystems by enabling the plants to flourish in nutrient-poor soils (<xref ref-type="bibr" rid="B4">Andrews and Andrews, 2017</xref>; <xref ref-type="bibr" rid="B28">Jaiswal and Dakora, 2019</xref>; <xref ref-type="bibr" rid="B62">Van Wyk, 2019</xref>).</p>
<p>The Bambara groundnut (<italic>Vigna subterranea</italic> (L.) Verdc) is one of the legumes that were historically grown for food in Africa. Despite being significant in several areas, including nutrition, medicine, and agronomical value, the crop is neglected and underutilised (<xref ref-type="bibr" rid="B43">Musa et&#xa0;al., 2016</xref>; <xref ref-type="bibr" rid="B10">Babalola et&#xa0;al., 2017</xref>; <xref ref-type="bibr" rid="B15">Gbaguidi et&#xa0;al., 2018</xref>; <xref ref-type="bibr" rid="B27">Ikenganyia et&#xa0;al., 2018</xref>; <xref ref-type="bibr" rid="B32">Khan et&#xa0;al., 2021</xref>). After the well-known groundnut (<italic>Arachis hypogea</italic>) and cowpea (<italic>Vigna unguiculata</italic>), it is the third-grain legume crop grown in the tropical lowlands of Africa (<xref ref-type="bibr" rid="B13">Egbe et&#xa0;al., 2013</xref>). The grains show a variety of colours (<xref ref-type="fig" rid="f1">
<bold>Figure&#xa0;1</bold>
</xref>). Bambara groundnuts variety are enjoyed by many people, especially in Africa, and are consumed in various forms, including dried, freshly cooked, and combined with other grains as food (<xref ref-type="bibr" rid="B30">Kanonge-Mafaune et&#xa0;al., 2018</xref>). In addition to other nutritional content, the grain of Bambara is made up of a high percentage of protein (20.6%), carbohydrate (56.5%), fat (6.6%), and fibre (6.3%) (<xref ref-type="bibr" rid="B23">Hillocks et&#xa0;al., 2012</xref>; <xref ref-type="bibr" rid="B41">Mubaiwa et&#xa0;al., 2017</xref>; <xref ref-type="bibr" rid="B25">Ibny et&#xa0;al., 2019</xref>). According to <xref ref-type="bibr" rid="B41">Mubaiwa et&#xa0;al. (2017)</xref>, the Bambara groundnut has a higher protein quality since its protein score recorded was 80% as opposed to 74% for soybean, 65% for groundnut, and 64% for cowpea. The lack of information regarding better seed systems, breeding, agronomic techniques, processing, and utilisation are amongst the factors restricting the utilisation of Bambara groundnut (<xref ref-type="bibr" rid="B42">Mubaiwa et&#xa0;al., 2018</xref>; <xref ref-type="bibr" rid="B59">Tan et&#xa0;al., 2020</xref>). It is well known that Bambara groundnut cultivation contributes to the preservation of soil fertility through the symbiotic fixation of nitrogen by root nodule-associated bacterial symbionts called rhizobia (<xref ref-type="bibr" rid="B31">Karunaratne et&#xa0;al., 2015</xref>). Despite its contribution to soil wellbeing, symbiotic nitrogen fixation is affected by some climatic conditions such as poor rainfall, prolonged drought, as well as high temperatures that affect rhizobium populations in the soil, and consequently reduce nodulation and yields of locally cultivated Bambara groundnuts (<xref ref-type="bibr" rid="B21">Gr&#xf6;nemeyer et&#xa0;al., 2014</xref>). As a countermeasure strategy, studies have indicated that coating Bambara groundnut seeds with rhizobial inoculants before planting tends to increase yields (<xref ref-type="bibr" rid="B23">Hillocks et&#xa0;al., 2012</xref>; <xref ref-type="bibr" rid="B25">Ibny et&#xa0;al., 2019</xref>). Motivated by the need for adaptation to climate change and to sustainably stabilise and improve yield of nutritious food in smallholder agriculture facing challenges to apply N fertiliser (<xref ref-type="bibr" rid="B47">Pulido-Su&#xe1;rez et&#xa0;al., 2021</xref>), this review discusses benefits of Bambara groundnut and potential of rhizobial inoculation in Bambara groundnut crop production, and urges on developing adapted inoculants. As a search strategy, we used the terms &#x2018;Bambara groundnut&#x2019;, &#x2018;rhizobia&#x2019;, &#x2018;biofertiliser/inoculants&#x2019; or &#x2018;Biological Nitrogen Fixation&#x2019;, to screen the relevant journals for recent articles from 2010 to 2022, with the exception of one article from 1997. The quality areas of selection bias, suitable data collection and analysis, and generalizability were used to evaluate each study&#x2019;s quality.</p>
<fig id="f1" position="float">
<label>Figure&#xa0;1</label>
<caption>
<p>Examples of Bambara grounduts. <bold>(A)</bold> Dehulled grains in various colours, here from cream to dark brown. <bold>(B)</bold> Freshly harvested Bambara groundnuts. <bold>(C)</bold> Symbiotic root nodules of field-grown Bambara groundnut.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fagro-04-1004771-g001.tif"/>
</fig>
</sec>
<sec id="s2">
<title>Origin and distribution of Bambara groundnut</title>
<p>Bambara groundnut, which is a native African legume, has been grown for generations in sub-Saharan Africa, primarily in semi-arid areas (<xref ref-type="bibr" rid="B26">Ikenganyia et&#xa0;al., 2017</xref>; <xref ref-type="bibr" rid="B60">Temegne et&#xa0;al., 2018</xref>). According to <xref ref-type="bibr" rid="B44">Nass&#xe9; et&#xa0;al. (2019)</xref>; <xref ref-type="bibr" rid="B38">Mayes et&#xa0;al. (2019)</xref> and <xref ref-type="bibr" rid="B32">Khan et&#xa0;al. (2021)</xref>, Bambara groundnut was initially discovered in West Africa and appears to have moved southwards throughout sub-Saharan Africa. Literature has suggested that the Bambara groundnut originated in an area named &#x201c;BAM-BARA&#x201d;, which is home to an agriculturist tribe that resided largely in the state of Bambara near Timbukutu in the west African region of central Mali (<xref ref-type="bibr" rid="B59">Tan et&#xa0;al., 2020</xref>), hence the name Bambara groundnut. Currently, the Bambara groundnut is grown extensively in most of West to southern Africa, Central Africa, Indonesia, Malaysia, India, Sri Lanka, Philippines, South Pacific, sections of northern Australia, Papua New Guinea, Central and South America (<xref ref-type="bibr" rid="B5">Aviara et&#xa0;al., 2013</xref>; <xref ref-type="bibr" rid="B31">Karunaratne et&#xa0;al., 2015</xref>).</p>
<p>Several semi-arid and sub-Sahara African countries, including Nigeria, Ghana, Cameroon, Togo, and Mali are now well-known for cultivating the crop. The primary growing regions for Bambara nuts in Southern Africa, are South Africa and Zimbabwe, while Southeast Asia, especially Thailand, Indonesia, and Malaysia, make up the secondary growing region (<xref ref-type="bibr" rid="B32">Khan et&#xa0;al., 2021</xref>). The world&#x2019;s annual production is estimated to be around 330 thousand tons, with the west African countries - Burkina Faso, Cameroon, Mali, Niger, Togo, and the Democratic Republic of the Congo being the major growing regions, with annual production at about 0.3 million tons and with Burkina Faso providing the most extensive yield at around 0.1 million tons per year (<xref ref-type="bibr" rid="B32">Khan et&#xa0;al., 2021</xref>). The lower yields in Sub-Saharan Africa emphasise the need for Bambara groundnut breeding to enrich varieties, as well as inoculant use to improve agronomic practices and enhance yields.</p>
</sec>
<sec id="s3">
<title>Biological nitrogen fixation</title>
<p>The primary nutrient that promotes plant root and shoots development is Nitrogen (N) (<xref ref-type="bibr" rid="B65">Yakubu et&#xa0;al., 2010</xref>). Despite its importance, N remains the most often inadequate nutrient for crop production in many parts of the world, especially in Africa and amongst resource-poor farmers. The ongoing use of N fertilisers to supplement N for plants demonstrates the necessity of this nutrient. <xref ref-type="bibr" rid="B47">Pulido-Su&#xe1;rez et&#xa0;al. (2021)</xref> and <xref ref-type="bibr" rid="B64">Wekesa et&#xa0;al. (2021)</xref> claim that the use of N fertilisers by resource-poor farmers is challenged by several factors such as cost, the possibility they may not be timely available in smallholder farming systems and may leach into surface and groundwater systems, especially when applied in sandy soils. To protect the environment from such unintended consequences, the greening revolution demands that economic, environmental, and renewable energy concerns employ biological alternatives (<xref ref-type="bibr" rid="B16">Gopalakrishnan et&#xa0;al., 2015</xref>). Hence, various research initiatives are being directed to the importance of biological nitrogen fixation (BNF), particularly by leguminous crops (<xref ref-type="bibr" rid="B50">Rao, 2014</xref>).</p>
<p>BNF is a fascinating biological phenomenon that involves the interaction between soil microorganisms, in particular bacteria, and higher plants (<xref ref-type="bibr" rid="B55">Santos et&#xa0;al., 2019</xref>). When the bacteria are in a symbiotic relationship, the BNF process is mediated by bacteria and the product is readily available to plants (<xref ref-type="bibr" rid="B54">Santi et&#xa0;al., 2013</xref>). During this process atmospheric N<sub>2</sub> is reduced to ammonia by the action of the enzyme nitrogenase (<xref ref-type="bibr" rid="B35">Liu et&#xa0;al., 2016</xref>). BNF occurs in the rhizosphere of non-leguminous plants and, in the root nodules of leguminous plants in the soil (<xref ref-type="bibr" rid="B1">Ahemad and Kibret, 2014</xref>). Rhizobia in the root nodule obtain carbon sources and thus energy from the higher plant and use them to reduce usable N (ammonium) which is then directly supplied to the plant to produce biomass and food (<xref ref-type="bibr" rid="B48">Puozaa et&#xa0;al., 2017</xref>; <xref ref-type="bibr" rid="B37">Mahmud et&#xa0;al., 2020</xref>). According to <xref ref-type="bibr" rid="B29">Jaiswal et&#xa0;al. (2021)</xref>, legume-rhizobia symbiosis is responsible for between one-third and one-half of the total N added to agricultural land. Similar to this, <xref ref-type="bibr" rid="B30">Kanonge-Mafaune et&#xa0;al. (2018)</xref> claimed that under ideal conditions, grain legumes may fix up to 200&#xa0;kg of N ha<sup>&#x2212;1</sup>, considerably lowering the need for inorganic N fertilisers. <xref ref-type="bibr" rid="B25">Ibny et&#xa0;al. (2019)</xref> and <xref ref-type="bibr" rid="B47">Pulido-Su&#xe1;rez et&#xa0;al. (2021)</xref> also argue that the nitrogen fixed by legumes can be as high as the amounts of nitrogen fertilisers used in conventional farming practices. This is congruent with <xref ref-type="bibr" rid="B13">Egbe et&#xa0;al. (2013)</xref> arguing that nearly half of the amount of nitrogen (N) used in inorganic N fertilisers is through symbiotic nitrogen fixation, according to estimates. According to some estimations, Bambara groundnuts may fix up to 28.42&#xa0;kg N/ha in the Sudano-Sahelian zone of Nigeria (<xref ref-type="bibr" rid="B65">Yakubu et&#xa0;al., 2010</xref>). According to <xref ref-type="bibr" rid="B66">Yusif et&#xa0;al. (2016)</xref>, fixation by rhizobia recruited from the soil alone provided additional nitrogen of 61.1 mg plant<sup>-1</sup>, but soil and inoculated rhizobia (HISTICK) together gave an additional nitrogen input of 124.7 mg plant<sup>-1</sup> in groundnut in Nigeria. While the above estimates differ in magnitude, the overall observation is that BNF significantly contributes to soil N build-up, making it a reliable substitute for inorganic fertiliser application.</p>
<p>
<xref ref-type="supplementary-material" rid="SM1">
<bold>Table S1</bold>
</xref> presents some of the benefit increases of legume yields or nitrogen inputs with different inoculants. The highest N increases have been recorded by <xref ref-type="bibr" rid="B11">Denton et&#xa0;al. (2017)</xref> in Faba bean and Lupin. Furthermore, several reports have as well indicated increased grain yield with increased N content in the soil. The highest grain yield improvements have been recorded in cowpea which was inoculated with <italic>Bradyrhizobium</italic> strains BR 3267 and BR 3262 (EMBRAPA BRAZIL). From the review, it is evident that Bambara groundnut has been ignored by research given that there are few reports on inoculant use on Bambara groundnut. However, the information emanating from research findings on other legume crops is giving support to inoculant technology and its benefit to the plants.</p>
</sec>
<sec id="s4">
<title>The rhizobial symbionts</title>
<p>According to <xref ref-type="bibr" rid="B61">Tsukanova et&#xa0;al. (2017)</xref>, rhizobia are soil-borne bacteria that are part of the <italic>Proteobacteria</italic> families &#x3b1;, &#xdf;, and &#x3b4; with the ability to develop nodules on the roots, and occasionally the stems of host plants, which are mostly legumes (<xref ref-type="bibr" rid="B1">Ahemad and Kibret, 2014</xref>; <xref ref-type="bibr" rid="B49">Raissa et&#xa0;al., 2020</xref>). The alpha-proteobacteria harbour most bacterial genera of nodule-forming microsymbionts; for example, the major genera are <italic>Rhizobium</italic>, <italic>Bradyrhizobium</italic>, <italic>Azorhizobium</italic>, <italic>Mesorhizobium</italic>, <italic>Ensifer (Sinorhizobium), Neorhizobium, Pararhizobium</italic>, and <italic>Allorhizobium</italic>, collectively referred to as &#x201c;rhizobia&#x201d; (<xref ref-type="bibr" rid="B29">Jaiswal et&#xa0;al., 2021</xref>), which can form symbiotic associations with a variety of legumes.</p>
<p>Except for a few studies that have demonstrated that species of the genus <italic>Bradyrhizobium</italic> nodulate Bambara groundnut, there is little information available on the biodiversity of rhizobia nodulating Bambara groundnut in African soils (<xref ref-type="bibr" rid="B25">Ibny et&#xa0;al., 2019</xref>). According to <xref ref-type="bibr" rid="B28">Jaiswal and Dakora (2019)</xref>, <italic>Bradyrhizobium</italic> is regarded as one of the most cosmopolitan and diverse bacterial groups responsible for nodulation in a variety of host legumes including Bambara groundnut in Africa. However, it is important to remember that the distribution patterns of rhizobial species vary depending on the geographic region (<xref ref-type="bibr" rid="B26">Ikenganyia et&#xa0;al., 2017</xref>). Hence, they might be other rhizobial symbionts associated with Bambara groundnut which have not been explored. Despite the need for increased food legume production, it has been reported that the diversity and distribution of the African nodulating indigenous legumes that form symbioses with bradyrhizobia and other rhizobia are not well understood. Nonetheless, research has revealed that bradyrhizobia nodulates several African dietary legumes (<xref ref-type="bibr" rid="B25">Ibny et&#xa0;al., 2019</xref>; <xref ref-type="bibr" rid="B2">Ajayi et&#xa0;al., 2020</xref>; <xref ref-type="bibr" rid="B12">Dlamini et&#xa0;al., 2021</xref>). This could be explained by the distinctive edaphoclimatic conditions of the continent&#x2019;s diverse habitats (<xref ref-type="bibr" rid="B28">Jaiswal and Dakora, 2019</xref>). To find rhizobia that can efficiently nodulate and promote the growth of significant yet underutilised crop species like Bambara groundnut, it is crucial to constantly investigate new geographic regions. Further research to facilitate identifying of numerous unique bradyrhizobia residing in African soils are required, to better understand the biogeography of <italic>Bradyrhizobium</italic> strains and their potential for inoculant production. Examples of some of the rhizobia that have been isolated from different legume crops and more specifically on Bambara groundnut are presented in <xref ref-type="supplementary-material" rid="SM1">
<bold>Table S2</bold>
</xref>. Amongst at least 10 species of <italic>Bradyrhizobium</italic> spp. isolated from nodules or nodulating Bambara groundnut in the laboratory, there are several that were Namibian isolates recently described as novel species, such as <italic>B. subterraneum</italic> (<xref ref-type="bibr" rid="B19">Gr&#xf6;nemeyer et&#xa0;al., 2015a</xref>), <italic>B. kavangense</italic> (<xref ref-type="bibr" rid="B17">Gr&#xf6;nemeyer et&#xa0;al., 2015b</xref>), <italic>B. namibiense</italic> (<xref ref-type="bibr" rid="B18">Gr&#xf6;nemeyer et&#xa0;al., 2017</xref>), or <italic>B. vignae</italic> (<xref ref-type="bibr" rid="B20">Gr&#xf6;nemeyer et&#xa0;al., 2016</xref>). Thus, this host plant appears to be quite promiscuous towards <italic>Bradyrhizobium</italic> spp., suggesting that inoculants that are well-adapted to varieties and environmental conditions may have to be developed for maximum benefit of yields.</p>
<sec id="s4_1">
<title>Mechanisms of nitrogen fixation by rhizobia</title>
<p>Nitrogen fixation happens through three different processes, including root hair penetration and infection thread formation, or rhizobia can infect their legume hosts and induce root or stem nodule formation (<xref ref-type="bibr" rid="B36">Liu et&#xa0;al., 2011</xref>). In some plants such as peanuts, where the infection process does not involve root hairs, the rhizobia can also enter the host through wounds or lateral root emergence (also known as &#x201c;crack&#x201d; entry) (<xref ref-type="bibr" rid="B7">Boogerd and Van Rossum, 1997</xref>; <xref ref-type="bibr" rid="B52">Ren, 2018</xref>); or penetration of root primordia found on the stem of some plants such as in <italic>Sesbania</italic> can result in entry (<xref ref-type="bibr" rid="B14">Froussart et&#xa0;al., 2016</xref>). But based on the information at hand, it appears that most species of legumes have their roots infected by rhizobia through root hair infection (<xref ref-type="bibr" rid="B45">Perrine-Walker et&#xa0;al., 2014</xref>; <xref ref-type="bibr" rid="B63">Wang et&#xa0;al., 2018</xref>
<italic>)</italic>. According to <xref ref-type="bibr" rid="B33">Lindstr&#xf6;m and Mousavi (2020)</xref>, the <italic>nod</italic>, <italic>nif</italic> and <italic>fix</italic> genes dominantly regulate symbiotic nitrogen fixation in rhizobia. Additionally, other sets of genes in the bacteria regulate various aspects of the nodulation process (<xref ref-type="bibr" rid="B24">Hong et&#xa0;al., 2012</xref>). The &#x201c;<italic>nif</italic>&#x201d; genes which encode the nitrogen-fixing enzyme nitrogenase subunits and additional proteins required for nitrogenase synthesis, regulation, and function, and the &#x201c;<italic>nod</italic>&#x201d; genes, which encode proteins for Nod factor synthesis that induce various symbiotic responses on legume roots, are the main symbiosis genes being studied (<xref ref-type="bibr" rid="B16">Gopalakrishnan et&#xa0;al., 2015</xref>). According to <xref ref-type="bibr" rid="B34">Li et&#xa0;al. (2017)</xref>, particular <italic>nod</italic> genes have been demonstrated to be important determinants of legume host specificity. Furthermore, <xref ref-type="bibr" rid="B4">Andrews and Andrews (2017)</xref> noted that because rhizobium strains are specialised, one rhizobium strain may infect some species of legumes but not others. The <italic>nif</italic> and <italic>nod</italic> genes, with the exception of <italic>Bradyrhizobium</italic>, are frequently carried on plasmids or symbiotic islands. These genes can be transferred (lateral transfer) between several bacterial species within a genus but seldom across genera (<xref ref-type="bibr" rid="B56">Shin et&#xa0;al., 2016</xref>).</p>
<p>The exchange of signals that enables mutual recognition and the activation of a signalling cascade is the first step in symbiotic interactions (<xref ref-type="bibr" rid="B33">Lindstr&#xf6;m and Mousavi, 2020</xref>). In reaction to the flavonoids released in plant root exudates, rhizobial lipochito-oligosaccharide signal molecules known as Nod factors are produced (<xref ref-type="bibr" rid="B14">Froussart et&#xa0;al., 2016</xref>). Nodule organogenesis begins when the plant detects the Nod factors. This is done by the root hair tips curling, which creates an infection thread, mitotic division of root cortical cells, and the formation of a nodule primordium (<xref ref-type="bibr" rid="B50">Rao, 2014</xref>). Thousands of living rhizobial symbionts, the majority of which are in the distorted form known as bacteroids, essentially colonise each root nodule (<xref ref-type="bibr" rid="B52">Ren, 2018</xref>). These bacteroids are encircled by membrane fragments from plant cells. N is fixed in these structures, known as symbiosomes-like stuctures, which may include numerous bacteroids or simply one (<xref ref-type="bibr" rid="B10">Babalola et&#xa0;al., 2017</xref>). Rhizobia differentiate into N<sub>2</sub>-fixing bacteroids that use nitrogenase to catalyze the conversion of atmospheric N into ammonia (<xref ref-type="bibr" rid="B37">Mahmud et&#xa0;al., 2020</xref>; <xref ref-type="bibr" rid="B29">Jaiswal et&#xa0;al., 2021</xref>).</p>
</sec>
<sec id="s4_2">
<title>Rhizobia inoculation and its constraints</title>
<p>Various researchers have reported on the application of microbial consortia or single microbes as inoculum that could be employed in agriculture to remedy degrading soil conditions; however, the effective transfer of microbial inoculants from the lab to the field remains a challenge that requires urgent attention (<xref ref-type="bibr" rid="B1">Ahemad and Kibret, 2014</xref>; <xref ref-type="bibr" rid="B47">Pulido-Su&#xe1;rez et&#xa0;al., 2021</xref>). The transfer of microbial inoculants to the field is challenged by numerous factors such as crop species and crop variants, varying climatic conditions between fields, as well as by the exponential rise in the number of microbial isolates in recent years (<xref ref-type="bibr" rid="B39">Mfilinge et&#xa0;al., 2014</xref>; <xref ref-type="bibr" rid="B26">Ikenganyia et&#xa0;al., 2017</xref>).</p>
<p>According e.g. to <xref ref-type="bibr" rid="B53">Sajid et&#xa0;al. (2011)</xref>; <xref ref-type="bibr" rid="B57">Singh et&#xa0;al. (2016)</xref>, and <xref ref-type="bibr" rid="B28">Jaiswal and Dakora (2019)</xref>, often regions regarded as geographic origins of legumes correlate with diversity hotspots of their respective symbionts. In addition, the performance of isolates on various local hosts varied, according to <xref ref-type="bibr" rid="B21">Gr&#xf6;nemeyer et&#xa0;al. (2014)</xref>, who found that most Namibian isolates were more effective in inducing nodulation on peanut and hyacinth bean grown in Namibia as opposed to the Angolan strains when used on the same varieties. Rhizobial strains frequently perform poorly in environments that are distinct from their original habitats, and <xref ref-type="bibr" rid="B9">B&#xfc;nger et&#xa0;al. (2021)</xref> recently found that their efficacy depends on environmental parameters like soil temperature and soil texture, amongst others. Furthermore, <xref ref-type="bibr" rid="B3">Allito et&#xa0;al. (2020)</xref> suggested that soil pH and consequentially the amount of accessible phosphorus have sizable effects on inoculant success. However, <xref ref-type="bibr" rid="B30">Kanonge-Mafaune et&#xa0;al. (2018)</xref> pointed out that optimising the concentration of rhizobial cells per unit seed three times in cowpea and four times in beans has improved responses to inoculation and grain productivity. Comparing the usage of inoculants in consortia form to individual forms, <xref ref-type="bibr" rid="B40">Moreira et&#xa0;al. (2010)</xref> observed that the use of inoculant in consortia form increased growth of the woody legume species <italic>Albizia lebbeck</italic> (L.) Benth, <italic>Enterolobium contortisiliquum</italic> (Vell.) Morong, and <italic>Leucaena leucocephala</italic>. It has also been discovered that seed coat compounds play a significant role in nodule development (<xref ref-type="bibr" rid="B51">Redjeki et&#xa0;al., 2013</xref>). This could be true as reported by <xref ref-type="bibr" rid="B25">Ibny et&#xa0;al. (2019)</xref> that variation in Bambara groundnut seed colour influences the choice of microsymbiont partners, through the attraction of native and familiar rhizobia with potential symbiotic efficiency within crop species.</p>
</sec>
</sec>
<sec id="s5">
<title>Concluding remarks</title>
<p>It is anticipated that the adoption of contemporary technology will play a crucial part in the progress of the underutilised Bambara groundnut in the world and Africa in particular to increase production to feed the World&#x2019;s growing populations. Rhizobial inoculants are one way to boost the production of Bambara groundnut that need to be explored and developed for the benefit of the agricultural sector. There is also a need to develop better strains of inoculants that suits the local environmental conditions and replace/solve the problem of exotic rhizobial strains whose survival rates in local soils are low due to severe and difference in the environmental and soil conditions. Since the Bambara is a native crop to Africa, an abundance of native rhizobia that are well adapted and capable of forming symbiotic relationships with the crop to efficiently fixing N may be available in local soils. It is suggested that temperature-resistant <italic>Bradyrhizobium</italic> strains should be isolated and selected on local soils (<xref ref-type="bibr" rid="B22">Gr&#xf6;nemeyer and Reinhold-Hurek, 2018</xref>). Therefore, it is highly recommended for a comprehensive approach to the use of &#x2018;inoculants&#x2019; and this should, include diagnostics of the field environment in relation to the desired crop. Furthermore, a holistic approach that investigate to determine the best agricultural practices, screening of available culture collections for inoculants, research in the area of microbiomes, and, integration of all the possible solutions into large-scale industrial production and field applications.</p>
</sec>
<sec id="s6" sec-type="author-contributions">
<title>Author contributions</title>
<p>All authors listed have made a substantial, direct and intellectual contribution to the work, and approved it for publication.</p>
</sec>
<sec id="s7" sec-type="funding-information">
<title>Funding</title>
<p>The German-Namibian cooperation was funded by grants of the Federal Ministry of Education and Research (BMBF, grant no. 01DG21008) and the German Academic Exchange Service (DAAD, grant no. 57558109) to BR-H and LNH in the framework of &#x201c;Partnerships for sustainable solutions with Sub-Saharan Africa&#x201d;.</p>
</sec>
<sec id="s8" sec-type="COI-statement">
<title>Conflict of interest</title>
<p>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.</p>
</sec>
<sec id="s9" sec-type="disclaimer">
<title>Publisher&#x2019;s note</title>
<p>All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.</p>
</sec>
</body>
<back>
<sec id="s10" sec-type="supplementary-material">
<title>Supplementary material</title>
<p>The Supplementary Material for this article can be found online at: <ext-link ext-link-type="uri" xlink:href="https://www.frontiersin.org/articles/10.3389/fagro.2022.1004771/full#supplementary-material">https://www.frontiersin.org/articles/10.3389/fagro.2022.1004771/full#supplementary-material</ext-link>
</p>
<supplementary-material xlink:href="DataSheet_1.pdf" id="SM1" mimetype="application/pdf"/>
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