Options for Improving Plant Nutrition to Increase Common Bean Productivity in Africa

Abstract

Common bean (Phaseolus vulgaris L.) is one of the most important grain legume crops in Africa. It represents an important share of food proteins and calories of poor agricultural populations in Eastern and Southern Africa. The production of bean in Africa is carried out primarily by small-scale farmers, who use little or no fertilizers or soil amendments. Average seed yields of beans in Africa are very low as compared to other production areas, mainly because of abiotic (edaphic and climatic) and biotic constraints. African soils are generally nutrient poor and application of adequate fertilizers is currently not feasible for economic and other reasons. The grain yield in the future can be increased by (i) using improved bean varieties that are better adapted to low soil fertility (ii) by application of fertilizers and managing soil fertility, and (iii) by optimizing the root symbioses to improve plant nutrient uptake under present conditions. Beans are forming two distinct types of symbiotic relations. They undergo nodulation with nitrogen-fixing bacteria and they also establish arbuscular mycorrhiza with Glomeromycota. Both of these symbioses affect in an important way the plant nutrient uptake. However, limited research efforts were made so far into studying the complex interactions between the three partners compared to the research focused either on biological nitrogen fixation or on mycorrhizal symbiosis. Thus the interactions among the symbiotic partners within the tripartite symbiosis are still poorly understood, though they might offer a potential to improve and sustain bean production in the tropics.

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9.1 Introduction

9.1.1 Relevance of Common Bean as Staple Crop in Africa

The cultivation of common bean (Phaseolus vulgaris L.) began thousands of years ago in rather fertile lands in cool climates at medium to high altitudes in the Americas. Common beans were imported to Africa about 300 years ago by Spanish and Portuguese traders. They are now grown by both small holders and commercial producers (Mauyo et al. 2007). The Eastern, Central, and Southern Africa are the main common bean-growing regions on the continent. Africa is probably the second largest producer of common beans after Latin America with nearly 5 millions ha yielding almost 3 million tons of seeds annually (FAO 2008). Although statistics indicate higher production of dry beans in Asia than in Africa, bean production in Asia is dominated by other botanical species than Phaseolus vulgaris L. (Singh 1999b). The average annual yields of common bean seeds in Africa vary between 167 kg ha⁻¹ in Eritrea and over 1,000 kg ha⁻¹ in Madagascar and South Africa (FAO 2008). Bean (mainly in form of seeds) is a major source of protein and calories in Eastern and Southern Africa (Pachico 1993; Broughton et al. 2003).

Between one-sixth to one-third of the dietary proteins intake by humans in the Eastern and Central African highlands comes from common beans, making them the most important pulse in the region. In Rwanda, common beans cover over 60% dietary protein requirements of both the rural and urban populations (Buruchara 2009). The commercial value (producer prices) of beans ranges, depending on the variety and country of production, between US$160 per ton of seeds (Niger in 2006) and well over US$1,000 per ton in Congo, Madagascar and Zimbabwe (FAO 2008). Therefore, bean production can be both a significant source of proteins for human consumption and also a significant source of income for farmers.

However, bean production in Africa is limited, and the yields realized by farmers are far below potential yields. The yields encountered on farmers’ fields are usually around 500 kg ha⁻¹, while the yield potential of the crop could be as high as 5,000 kg ha⁻¹ under optimal water and nutrient supply and in the absence of pests and pathogens (Verdoodt et al. 2004). Main reasons of this discrepancy are: (i) the low fertility soils on which they are grown, (ii) lack of nutrient inputs, (iii) planting bean varieties not adapted to the environment, and (iv) lack of disease and pest controls (Thung and Rao 1999). As a consequence, the production of common beans does not yet meet the increasing demand in sub-Saharan Africa (CIAT 2009).

9.1.2 Significance of Nitrogen, Phosphorus, and Soil Conditions for Bean Production

The major soils found in bean-growing areas in Africa are classified as Alfisols, Ultisols, Oxisols and Inceptisols. These tend to be acidic, low in organic matter, low in exchangeable calcium (Ca), magnesium (Mg) and potassium (K), low in available phosphorus (P), high in exchangeable aluminium (Al) and/or manganese (Mn) and have often a high P fixing capacity (Wortmann et al. 1998; Thung and Rao 1999). Optimal conditions for beans are, however, light loamy soils with pH between 5.5 and 7.0, rich in organic matter, and providing an adequate supply of water, nitrogen (N) and P (Singh 1999b).

Low availabilities of N and P in agricultural soils are among the most widespread plant nutritional constraints for crop growth and yields on a global scale and more specifically in Africa. Given the acknowledged accelerated nutrient mining and lack of fertilizer use (Sanchez and Swaminathan 2005), N and P deficiencies are major and omnipresent problems in African agriculture (Drechsel et al. 2001). For example, in Ethiopia, nutrient depletion amounts to 36, 6, and 32 kg ha⁻¹ year⁻¹ of N, P and K, respectively, while the average use of fertilizers in the country replenishes only about 10% of the nutrients removed by crops from the fields (Henao and Baanante 1999). In extreme cases such as in Rwanda and Malawi, where some of the soils are inherently quite fertile, soil nutrient depletion may reach (on a national level) up to 60, 10, and 60 kg ha⁻¹ year⁻¹ of N, P, and K (Roy et al. 2003), with negligible nutrient inputs (Drechsel et al. 1996). Moreover, when mineral fertilizers are used, they are rather applied to crops other than common bean. Bean seeds contain large amounts of N and P (35–45 mg N g⁻¹ and 4–5 mg P g⁻¹) and these concentrations do not vary largely among different growth conditions and bean cultivars (Araujo and Teixeira 2003). This means that for a bean production of 2,000 kg dry seeds ha⁻¹ year⁻¹, almost 100 kg N and about 10 kg P will be removed each year from the system with the harvested seeds.

Common bean can obtain N from the atmosphere through biological nitrogen fixation (BNF) carried out by symbiotic rhizobia. However, the BNF rarely covers the full N demand of beans (Thung and Rao 1999). This is in contrast to soybeans and other leguminous crops, which require either little or no starter N fertilizer to establish efficient symbiosis with N fixing prokaryotes, and subsequently cover most of their N demands through BNF (Mendes et al. 2003; Campo and Hungria 2004). Beans usually respond well to N fertilization up to 200 kg ha⁻¹ (Anderson 1974; Edje et al. 1975; Mayona and Kamasho 1988; Daba and Haile 2002; da Silveira et al. 2005) and rarely derive more than 50% of their N from the atmosphere (Bliss 1993a; Wortmann 2001). In spite of their relative dependency of soil mineral N, bean usually recover less than 50% of the applied N fertilizer, with highest reported values being about 70% (Thung and Rao 1999; dos Santos and Fageria 2007, 2008). This phenomenon is probably related to (i) the coarseness of bean roots (Zhu et al. 2005; Rubio and Lynch 2007), and (ii) the fact that beans develop best in soil with high organic matter content, i.e. releasing mineral N steadily through mineralization during the growing season (Thung and Rao 1999). Previous surveys estimated that over 60% of the bean production area in Central, Southern, and Eastern Africa was affected by N deficiency (Wortmann et al. 1998; Thung and Rao 1999). This caused yield losses of up to 40% compared to the N fertilized areas (Singh 1999b; Thung and Rao 1999).

In addition to N deficiency, in about 40–50% of African bean production areas, the common beans are affected by moderate to severe P deficiency (Wortmann and Allen 1994; Wortmann et al. 1998; Lunze et al. 2007). The naturally low P availability of African soils might be due to the low total soil P content and/or to their high P fixing capacity due to their high Al and iron (Fe) oxide contents and their low pH (Vitousek 2004; Wardle et al. 2004; Nziguheba 2007). Yield of beans can be reduced by as much as 60–75% in soils that are unable to release sufficient P levels during the growing season. P deficiency is also a major contributing factor limiting BNF in beans (Graham 1981; Thung 1992). This is because the BNF requires large amounts of P to be delivered to the rhizobia (Fig. 9.1), creating additional sink of P to the plant in the nodules, thus further depriving the plant of the P acquired from the soil (Leidi and Rodriguez Navarro 2000; Zaman–Allah et al. 2007). For these reasons, P fertilization has usually large positive effects on growth, BNF, and yields of the common beans in low P soils such as frequently encountered in Africa (Mbugua 1986; Aggarwal et al. 1997; Beebe et al. 2006). In these soils, an adequate P ­fertilization can thus alleviate both N and P deficiencies in beans.

Fig. 9.1

Conceptual model of main phosphorus, nitrogen, and carbon fluxes in the tripartite symbiosis of common bean, arbuscular mycorrhizal fungus, and nitrogen-fixing prokaryote. For simplification, mycorrhizal fungus is shown only left to the roots and nodules are only shown on the right side of the root system. Phosphorus (dotted arrows) is derived either from the seed reserves (not shown here) or from the soil. Soil phosphorus uptake is realized either via the arbuscular mycorrhizal fungus (mycorrhizal uptake pathway) or directly through rhizodermis/root hairs (direct or root uptake pathway). Significant portion of the phosphorus transported through the vascular tissues is diverted towards the nodules due to high phosphorus demand of the biological nitrogen fixation (BNF). Nitrogen (dashed arrows) is taken up either by the roots from the soil, or obtained from the atmosphere through the BNF process mediated by the prokaryotes. Reduced carbon compounds derived from plant photosynthesis and transported belowground (solid arrows) are utilized by roots (not shown here), nitrogen-fixing prokaryotes, and the mycorrhizal fungi (Jansa et al.)

About 40–50% of the bean production areas in Central, Eastern and Southern Africa are estimated to be affected by Al toxicity, which might result in 50–60% losses in yields (Thung and Rao 1999; Broughton et al. 2003). Furthermore, about 10% of the bean production areas in Africa suffer from Mn toxicity (Thung and Rao 1999; Weil 2000). Mn toxicity is typically found in soils with high rainfall and/or poor drainage, low pH, and medium to high organic matter contents. Large areas producing beans are suffering from moderate K deficiency, but this is usually not considered a major limitation for bean production (Wortmann et al. 1998; Thung and Rao 1999). Other constraints such as drought and biotic stresses also strongly limit bean production. Although these other constraints may be as important as N and P deficiencies, causing up to 100% harvest losses (Wortmann et al. 1998; Singh 1999b), they are not the subject of this review that is particularly focused on plant nutrition and root symbiotic interactions. Importance of biotic stresses for bean production and breeding efforts aiming at overcoming them have been reviewed elsewhere (Kelly 2004; Hillocks et al. 2006).

This review aims at: (i) Characterization of the components of bean cropping systems in Africa including plant genetic variability and root and root symbioses functioning; (ii) Identification of possible system changes consisting of one – or two – step modifications of the current practices, in order to improve nutrient acquisition and use by the plants and subsequently the yields, and; (iii) Proposing some further perspectives requiring deeper changes of the production systems, to increase yields and sustainability of the bean production system. Associated research needs are outlined, which are required to implement these changes. This contribution focuses on soil-microorganisms-plant relationships and leaves out social and economic aspects of the bean production, seed storage, marketing, and processing for human consumption. Although these other aspects of bean science are certainly important, they cannot be considered in this review.

9.2 Characterization of the Components of Bean Cropping Systems

9.2.1 Current Fertilization Strategies and Cropping Systems

Although frequently grown, common beans are rarely fertilized in subsistence farming in Africa. Bean production thus contributes to the widespread soil nutrient mining and eventually to soil degradation (Giller and Cadisch 1995; Wortmann et al. 1998). When mineral fertilizers are used, they tend to be applied to maize or other high-value cash crops such as banana but not to beans as reported in case studies from Malawi and Zimbabwe (Snapp et al. 1998; Nyakudya et al. 2005). Although it was repeatedly demonstrated that fertilizers would increase production, unaffordable prices and low quality of mineral fertilizers, together with the lack of local infrastructure, markets, institutions, and political will limit large scale applications of mineral fertilizers (Sanginga et al. 2007).

High levels of N and P fertilizers would indeed be necessary to overcome the low fertility of many African agricultural soils. Sanchez and Uehara (1980) and Munthali (2007) estimated that applications of 500–1,000 kg P ha⁻¹ would be required to realize major and long-lasting crop yield increases in Oxisols. Similarly, large N inputs (more than 100 kg N ha⁻¹ year⁻¹) would be required to improve bean seed yields above 2,000 kg ha⁻¹ year⁻¹ (da Silveira et al. 2005). Since these long-term measures are currently impossible to implement, small amounts of spot – or band-applied fertilizers, mostly of local origin, have been promoted to achieve at least moderate and short-term increases in crop yields (Smithson et al. 2003; Woomer et al. 2003; Jama and Pizarro 2008). Another strategy to improve crop yields is to use locally produced green or animal manures. It has been shown that applications of plant residues (for example Tithonia diversifolia and Senna hirsuta at rates of 4 t ha⁻¹) are as effective as application of inorganic NPK fertilisers containing same amounts of N as the organic materials for increasing maize and bean yields (Kayuki and Wortmann 2001; Vanlauwe and Giller 2006). However, the plant materials usually contained less P than the corresponding inorganic fertilizers. Thus it has been recommended to use plant residues together with low rates (e.g. 10 kg ha⁻¹ year⁻¹) of easily soluble P fertilizers (Vance 2001). On acid soils, this should be combined with liming so as to avoid strong P fixation and Al toxicity (von Uexküll and Mutert 1995; Fageria and Santos 1998). Using organic fertilizers could also limit soil organic matter depletion and thus limit soil N and bases depletion and slow down acidification (Giller et al. 1997; Thung and Rao 1999; Rutunga and Neel 2006). However, land scarcity, demand for organic materials to be used as fuel or construction materials, and generally low animal production in Africa will not allow broad application of manures in any near future (Fermont et al. 2008).

Common bean is an important component of several cropping systems on a global scale. It can be grown in monocultures (mainly in Latin America), or in different relay, strip and intercropping systems (Singh 1999b). In Africa, beans are produced either as monocultures (more bush, occasionally climbing beans) or, more often, as a component of intercropping systems (Wooley et al. 1991; Wortmann et al. 1998). Traditionally, beans are intercropped or relay-cropped with maize, banana, cassava or with other crops (Wortmann et al. 1998; Broughton et al. 2003). Climbing bean cultivars are often grown together with maize or cassava, which provide the required mechanical support instead of additional stakes or trellises. Intercropping of beans with maize seems to be the traditional way of producing these two crops, as documented by Phaseolus archaeology (Hastorf 1999; Zeder et al. 2006). Intercropping is first regarded as insurance against severe environmental stresses or high incidence of diseases, diversifying the farmer’s production basis and decreasing production risks (Broughton et al. 2003). Further arguments for adopting intercropping systems as compared to the monocropping are the potential N benefits to the cereal component through the BNF of the legume component, reduced erosion, water conservation, and shading of the beans from direct sunlight (Clark and Francis 1985a; Vieira 1998). On the other hand, intercropping of beans and maize reduces yield of each component because of resource competition (Silwana et al. 2007). Transfer of N from bean to maize remains controversial due to generally low BNF efficiency of the common bean as compared to other legumes such as soybean or chickpea (Martin et al. 1995; Zhang and Li 2003; Ghosh et al. 2007). Although greater amount of plant biomass is sometimes produced in intercropping system as compared to the monocultures, the yields (either in terms of calories or proteins) usually do not exceed the higher yielding monocrops (Clark and Francis 1985b). In case of fodder production, intercropping maize with beans would yield the same amount of silage but with higher nutritional quality (=higher crude protein concentration) than that of the maize alone (Dawo et al. 2009). In addition to intercropping, bean may also be grown in rotation with cereals such as maize or sorghum (Wortmann 2001). Although crop rotation is known to efficiently contribute to disease and pest control, nutrient use efficiency, and system sustainability (Liebman and Dyck 1993; Kandji et al. 2003; Sangakkara et al. 2003; Vanlauwe et al. 2008), it is not widely practiced in Africa. It is usually limited to areas, where sufficient and reliable short-rains would provide sufficient moisture for the bean crop, usually sown in the short-rain season in zones with bimodal rainfall pattern (Broughton et al. 2003) or where sufficient water would be still available during the dry season such as in protected valley bottoms (Wortmann et al. 1998).

9.2.2 Genetic Variability of Beans

Phaseolus vulgaris L. belongs to a large genus, where five different botanical species have been domesticated (Debouck 1999). The genetic origin of common bean is from Ecuador and northern Peru. Wild beans dispersed from its origin northwards and southwards and formed two distinct gene pools, the Mesoamerican and the southern Andean. Post-domestication divergence resulted in three domesticated races in each of these two pools (Singh et al. 1991; Broughton et al. 2003). There are more than 30,000 domesticated and over 1,000 wild accessions of common bean housed in the germplasm collection at CIAT, Cali, Colombia (CIAT 2009). Smaller germplasm collections exist also at other institutions around the world, of which the largest is probably the one at the USDA Western Regional Plant Introduction Station at Pullman, WA. In spite of this large reservoir of genetic diversity, genetic base of commercial cultivars is rather narrow, encompassing less than 5% of the available genetic diversity of the species (Broughton et al. 2003). Out of the diversity present in the planted cultivars, only a small portion is present in Africa (Wortmann et al. 1995).

Large genetic variability exists among the common bean varieties, being manifested by a range of seed sizes and colours, tastes, growth habit etc. (CIAT 2009). For example, variation of growth habit in common bean appears to be continuous from determinate bush to indeterminate, climbing types (Singh 1982). Genetic variability of the common beans allows highly versatile use of this plant in different cropping systems, matching local culinary preferences, and local environmental constraints (Broughton et al. 2003). Indeed, large variability of traits related to mineral nutrition, tolerance to drought and other abiotic environmental stresses has been described among different bean lines (Rao 2002; Singh et al. 2003; see also a summary in Table 9.1). In brief: Low N, P and drought tolerances appear to be related to the rooting patterns, rate and duration of nutrient acquisition from the soil, and to internal utilization efficiency of the N and P. Tolerance to Al and Mn toxicities appears related to lateral root formation, root exudation and callose formation rates. The knowledge about the variability of traits among the bean lines allowed selection of adapted genotypes for particular environmental conditions and identification of genes responsible for trait expression (Kelly 2004; Blair et al. 2007). These efforts already resulted in release of dozens of improved varieties to and adoption by the farmers within the last decades (Hillocks et al. 2006). These were mainly varieties with improved disease resistance and tolerance to drought and low soil fertility. In combination with advanced breeding approaches (marker assisted selection, genomic sequencing, functional genomics, etc.), current genotype improvement efforts promise possibility of accelerated and specifically targeted breeding of common beans so as to match variety of demands (Miklas et al. 2006; Gepts et al. 2008). Although the structuring of genetic variability in beans is becoming understood, genes or gene clusters responsible for resistance to diseases, tolerance to drought, low pH and low P availability in soils are being identified and breeding strategies and molecular engineering technologies exist for insertion of the desired traits into specific genotypes, other barriers are still limiting widespread release and adoption of the improved cultivars by the farmers. Main limitations are the lack of information about availability of new lines, their benefits and required management measures, and the uncertainty about the anticipated short- and long-term changes in the production systems, which would further focus the breeding efforts. In Africa, these limitations are at least partly outweighed by participatory breeding and distribution of seeds, which have long tradition and established as viable, though less efficient alternative to the global breeding efforts (Broughton et al. 2003; Gepts 2006). For example, it was documented that even forces like civil war in Rwanda could not stop local seed exchanges and maintaining diversity of bean varieties on a local scale (Sperling 2001).

Table 9.1 Overview of variability among common bean genotypes with respect to their performance and yields under different abiotic environmental constraints

9.2.3 Biological Nitrogen Fixation

Common beans undergo symbiotic interaction with rhizobia capable of fixing atmospheric dinitrogen (N₂). This consists of formation of nodules on host roots, which harbour the bacterial symbionts, and the N₂ fixation process in the nodules, which occurs thereafter. The knowledge about signalling between the plant and the bacterial partners is well advanced, especially when compared to other kinds of symbioses like the mycorrhizas (Hungria and Stacey 1997; Cocking 2003). The molecular dialogue involves flavonoids produced by the plants, nod-factors derived from the bacterial cell walls, lectins in plant cell membranes, and an array of other molecules and signal-transfer pathways, some of which still remain to be characterized (Ferguson and Mathesius 2003; Oldroyd and Downie 2006; Shaw et al. 2006; Garg and Geetanjali 2007). Currently, we are witnessing fast developments in genome sequencing of legumes and rhizobia as well as functional genomics studies, unravelling the relationships between different genes involved in establishment and functioning of the symbiotic nitrogen fixation (Colebatch et al. 2004; Gonzalez et al. 2006b).

The common bean associates with a wide range of rhizobial strains and Rhizobium etli is the dominant microsymbiont at both centers of genetic diversification of the beans (Aguilar et al. 2004; Grange et al. 2007). Other rhizobial species such as R. tropici, R. gallicum, and R. leguminosarum were shown to associate with the beans in Colombia, Brazil, Argentina, Egypt, Tunisia, Ethiopia and elsewhere (Mhamdi et al. 1999; Beyene et al. 2004; Shamseldin et al. 2005; Kaschuk et al. 2006a; Stocco et al. 2008). As much as five different rhizobial species were shown to co-colonize common bean roots simultaneously in Spanish soil (Herrera-Cervera et al. 1999). Thus, bean can be classified as a promiscuous host, associating with a range of taxonomically rather distant prokaryotes (Martinez-Romero 2003). Genomic sequencing of R. etli indicated positioning of the symbiotic genes clustered within a “symbiotic island” on plasmids (Flores et al. 2005; Gonzalez et al. 2006b). Close relationship was found among symbiotic genes from different strains of rhizobia nodulating common bean, independent of the ribosomal DNA-based classification (Laguerre et al. 2001), although some differences were noted between mechanisms of nodulation by R. tropici and other bean-nodulating rhizobia (Broughton et al. 2003; Martinez-Romero 2003). In general, this supports the theory of frequent horizontal genetic transfer of extrachromosomal DNA across rhizobial species, and indicates co-evolution of the beans with the bacteria possessing certain symbiotic gene makeup rather than with taxonomically well-defined lineages (Vinuesa and Silva 2004).

Although there is a high level of similarity within the symbiotic genes among the rhizobial species nodulating common beans, the different strains and species of the prokaryotes may be genetically and metabolically quite different (Martinez-Romero 2003). This predisposes them to occupy different environmental niches and exert differential efficiency in N₂ fixation with different bean genotypes under different situations. In general, extreme conditions of soil pH, temperature, salinity, and moisture, and low nutrient availabilities (except N) are not favourable for the rhizobia (Graham 1981; Gonzalez et al. 2001; Saadallah et al. 2001a; Abdelmajid et al. 2008). Availability of P is recognized to be of primary importance for the nitrogen fixation in beans, because the nodules represent a strong P sink (Tsai et al. 1993; Vadez et al. 1999; Hellsten and Huss-Danell 2001; Drevon et al. 2005). Similarly, carbon costs associated with nodule development and BNF represent an important sink of reduced carbon for the plant, potentially leading to slower plant growth especially upon low light availability (Neves and Hungria 1987). It is known that the BNF activity in beans can be negatively affected by external N supply, and that this relationship is further affected by P availability. For example, upon low (1 mM) nitrate concentration in soil, increasing amount of P promoted both nodule formation and N₂ fixation in beans. However, at higher (10 mM) nitrate concentrations, nodulation and N₂ fixation did not improve with increasing P supply (Leidi and Rodriguez Navarro 2000). N₂ fixation (measured as acetylene reduction rate) and nodule weight in common beans were highest if no N fertiliser was added to the soil, and declined to very low levels at 336 kg N ha⁻¹. The N₂ fixation rate reached maximum values early in the season and declined to low values before seed filling was complete (Buttery et al. 1986). High levels of tolerance to abiotic stresses were found amongst different rhizobial strains. For example, low pH, high temperature and drought-tolerant rhizobia were found in some tropical soils, e.g. in Brazil (Hungria and Vargas 2000; Martinez-Romero 2003), and high salinity and high pH tolerance was described in R. etli isolated from Egyptian soils (Shamseldin and Werner 2005; Shamseldin 2008). Drought tolerance of certain rhizobial strains appear to be linked to high trehalose production by the prokaryotes within the nodules (Zacarías et al. 2004; Suarez et al. 2008), conferring drought tolerance onto the associated plants.

As already mentioned above, common bean is usually considered to fix N₂ poorly, being generally more responsive than other legumes to N fertilization (Graham 1981). The beans may also require starter N fertilizer to fully realize the BNF benefits under low soil fertility, particularly if rhizobial inoculants are used (Daba and Haile 2002). However, significant differences in the capacity to support BNF were found among bean cultivars and were shown to be heritable (StClair and Bliss 1991; Wolyn et al. 1991; Bliss 1993a). Some commercial bean lines, usually those of bushy growth habit, have the lowest N fixation efficiency among all legume crops, being far below 50% of plant N derived from the atmosphere (Isoi and Yoshida 1991; Bliss 1993a; Hardarson et al. 1993; Martinez-Romero 2003). This means that the BNF rarely provides adequate N supply to the bean crops during the whole growth cycle (Hardarson and Atkins 2003). The weak nodulation and N₂ fixation rates as compared to other grain legumes have several reasons: (i) Beans are usually grown under marginal soil conditions and high temperatures, with lacking P supply, and in presence of water stress and toxic elements. Such conditions generally suppress nodulation and/or N₂ fixation by the rhizobia (Hungria and Vargas 2000; Jebara and Drevon 2001); (ii) Beans are often grown under conditions not matching those in their areas of origin, where they would preferentially associate with R. ­­etli. Since bean is generally a promiscuous legume associating with a range of rhizobial species and strains (Martinez-Romero 2003), it is likely that competition with less efficient rhizobia would impair nitrogen fixation under conditions, which were not conductive for their most efficient microsymbiont (Rao 2002; Martinez-Romero 2003); and (iii) Selection for early flowering and short growth cycle might have impaired N benefits from the BNF due to shortening the vegetative period when the N₂ fixation takes place (Graham 1981; Chaverra and Graham 1992; Thung and Rao 1999). However, it has also been recognized that certain combinations of bean and rhizobial genotypes under certain conditions considerably vary in the extent of N₂ fixation. For example, seed yields of 1–2 t ha⁻¹ year⁻¹ could be achieved with some bean genotypes and highly efficient rhizobia without N fertilization, and in the absence of other limitations such as high temperatures, low P availability, and drought (Hungria and Neves 1987; Bliss 1993b; Thung and Rao 1999). This means, on one hand, that current bean production rates in large parts of Africa can still be substantially improved by better utilization of BNF, provided appropriate management of other constraints. On the other hand, this also means that for production rates above 2 t ha⁻¹ year⁻¹, common bean is likely to require N fertilizer inputs ­anyway. It has also been demonstrated that bean genotypic variability in efficiency of BNF is at least partly linked to adaptation of the different plant genotypes to low P conditions, particularly by higher internal P use efficiency of the plants (Araujo and Teixeira 2000; Tang et al. 2001; Vadez and Drevon 2001). Although different rhizobia may differ in their metabolic response to low P supply (Al-Niemi et al. 1997; O’Hara 2001), it is not well known whether there is any significant variation in internal P use efficiency among the different rhizobial species and strains, or whether the observed preferences in association of beans with particular rhizobia under low P conditions are mediated by the plants. All in all, satisfying P demands of the plants is of primary importance for optimizing the BNF efficiency and associated yield increases.

Rhizobial inoculation, although having the potential of improving common bean yields and production sustainability under field conditions (Vargas et al. 2000; Guene et al. 2004; Cardoso et al. 2007), is usually not practiced by farmers in Africa and elsewhere. This is somehow in contrast to other legumes like soybeans, which associate with much narrower range of rhizobia, and which generally derive greater benefits from the BNF than the common bean. For example, optimizing BNF in soybean can be achieved either by planting promiscuous varieties supporting greater rhizobial diversity, or by industrial inoculation of the fields. The latter is a multimillion business globally, though less widespread in Africa than in other parts of the world. For common beans, industrial inoculation would suffer from low economic returns (Ndakidemi et al. 2006), lack of information on competitiveness of introduced vs. indigenous rhizobia under field conditions (Hungria et al. 2000; Martinez-Romero 2003), as well as lacking technology, institutions, education, and markets for targeted production, distribution, and application of rhizobial inoculants for common bean. This last point is particularly relevant for Africa, where investments into agricultural innovations are limited because of institutional and market constraints (Sanginga et al. 2007; Jama and Pizarro 2008).

9.2.4 Arbuscular Mycorrhizal Symbiosis

Apart from the association with rhizobia, beans also establish a root association with fungi from the phylum Glomeromycota (Daft and El-Giahmi 1974). The mechanisms of establishment of this symbiosis called arbuscular mycorrhiza (AM) show several parallels to the rhizobial association. This knowledge has been established by studies on symbiotic mutants and on the gene expression and signalling events in the different symbioses involving beans and other legumes such as peas, medic, and Lotus japonicus (Shirtliffe and Vessey 1996; Morandi et al. 2005; Gherbi et al. 2008). Although the association with AM fungi is evolutionarily older and more widespread in the plant kingdom than the BNF (Parniske 2008), it is less understood as compared to the rhizobial association, mainly because of unusual (polynuclear) genome organization of the AM fungi, lack of transformation system allowing genetic manipulations of the AM fungi, and their resistance to grow on synthetic media in the absence of a host plant (Marsh and Schultze 2001; Sanders 2004; Jansa et al. 2006).

Under field conditions, roots of common beans are normally colonized by the AM fungi (Yan et al. 1995b), although variability was observed between the plant genotypes in the extent of root colonization as well as in the plant responses to establishment of AM symbiosis (Ibijbijen et al. 1996; Oliveira and Sanders 2000; Hacisalihoglu et al. 2005). However, great variation exists among results of different studies using slightly different approaches, which is quite typical for mycorrhizal research. For example, Mosse and Thompson (1984) identified the bean cultivar Canadian Wonder as poor host of AM fungi, with colonization levels under laboratory conditions with two AM fungal strains remaining below 10% of root length colonized, in contrast to genotype Jamapa, where values above 50% were consistently observed. However, another study on root colonization of the genotype Canadian Wonder under field conditions reported values near 100% of the root length colonized within few weeks after sowing (Oliveira and Sanders 1999). In extreme case, bean mutants have been identified, which proved completely resistant to mycorrhizal colonization (Shirtliffe and Vessey 1996; Cardenas et al. 2006).

Establishment of mycorrhizal symbiosis in beans confers multiple benefits to plant nutrition, growth, disease resistance and drought tolerance (Newsham et al. 1995; Moawad and Vlek 1998). The nutritional aspects of AM symbiosis have frequently been studied in the past in various plants including common beans. AM symbiosis usually confers improved acquisition efficiency to the plants of P and Zn, particularly under soil conditions, when the availability of these elements for plants is low (Giller and Cadisch 1995; Sharma et al. 1999; Rao 2002). These nutritional effects are generally stronger in beans than in grasses (Isobe and Tsuboki 1998), most probably due to the differences in the root system architecture. The acquisition of P and/or Zn by mycorrhizal plants is often exceeding by a factor of 2 or more the acquisition of the same elements by the nonmycorrhizal plants (Ibijbijen et al. 1996; da Silveira and Cardoso 2004; Ortas and Akpinar 2006). This is consistent with previous classification of beans as strongly mycorrhizal-dependent plants due to their better growth in non-fumigated as compared to methyl bromide fumigated soil (Plenchette et al. 1983). Next to the nutritional effects, multitude of other benefits have been attributed to AM symbiosis, such as more efficient utilization of P fertilizers by the plants, improved root development, increased tolerance of plants to drought and to heavy metal pollution (Sieverding 1991; El-Tohamy et al. 1999; Thung and Rao 1999; Augé 2004). The mechanisms behind all these effects are not completely understood, but they seem to be related to improved mineral nutrition of the plants, changes in internal hormonal balances in the plants, relief from stress through changes in soil properties and selective ion uptake from soil solution, immobilization of heavy metals in the fungal biomass as well as promotion of development of associated microbes in the mycorrhizal hyphosphere (Joner et al. 2000; Augé 2004; Joner et al. 2004; Kohlmeier et al. 2005; Hause et al. 2007; He et al. 2007). On the other hand, plants supply the AM fungi with reduced carbon originating from their photosynthesis. This means that the observed growth effects are indeed composite effects of plant performance promotion through mechanisms such as improvement of scarce nutrient uptake combined with associated carbon costs (Lynch and Ho 2005). Thus the overall greatest net benefits of AM symbiosis are usually seen under stressful environment such as low P and/or Zn availability, high Al or heavy metal availability, and drought, this means under situations, where plants would normally invest great fraction of their carbon budget into root development and exudation (Nielsen et al. 2001; Jansa et al. 2006).

In spite of numerous papers on AM symbiosis in beans with respect to mineral nutrition and growth benefits, other four important aspects of mycorrhizal symbiosis in beans received relatively little attention in the past. These are: (1) Interactions between plant, AM fungi, and pathogens; (2) Phenomenon of AM fungi interconnecting plant individuals from the same and different species; (3) Functional diversity in AM fungal communities; and (4) Mechanisms of interactions between plants, AM fungi and rhizobia within so called tripartite symbiosis. We briefly handle the first three points in this section and then we expand on the last point in the following section.

• 1. Colonization of bean roots by AM fungi may interfere with development of soilborne pathogens such as Fusarium solani (Linderman 1992; Dar et al. 1997). The mechanisms are not precisely known, but competition for space, induced resistance, modification of root and rhizosphere physico-chemical properties and composition of associate microflora upon development of the AM fungus have all been proposed (Dar et al. 1997; Osbourn 2001; Filion et al. 2003). Of particular importance appear to be the induced systemic resistance to pathogens like Rhizoctonia due to AM fungal colonization of roots (Cordier et al. 1998; Guillon et al. 2002; Pozo and Azcón-Aguilar 2007). Such a resistance could potentially also be used for “immunization” of plants so as to increase their resistance against devastating foliar pathogens (Fritz et al. 2006).

• 2. AM fungi are colonizing soil as far as 15 cm beyond the root zone (Jansa et al. 2003a) and are very little specific with respect to the choice of their host plants (Smith and Read 2008). Therefore, mycelium networks of different plant individuals (belonging or not to the same species) may easily overlap in soils. Further, root systems of neighbouring plants can be directly interconnected by a shared mycelium network of the same AM fungal species. This situation is particularly relevant for beans not only because mycorrhizal effects on single plant and on plant stand levels are rather inconsistent and appear strongly modulated by plant density (Facelli et al. 1999; Facelli and Facelli 2002; Li et al. 2008), but also because beans are frequently grown in association with different (mycorrhizal) crop plants such as maize and sugarcane. The possibility of direct transfer of nutrients, water, and carbon between different plant species sharing a common mycorrhizal network has often been mentioned in the literature (Sierra and Nygren 2006; Wilson et al. 2006; Egerton-Warburton et al. 2007), but unequivocal experimental evidence for such transfers is virtually missing (Pfeffer et al. 2004; Whitfield 2007; Voets et al. 2008). Therefore, rather than direct transfer of compounds between the different plants, it seems that processes like diverting mycorrhiza-mediated fluxes of mineral nutrients between soil and plants acting as different sinks on a common supply line should be more carefully studied (Whitfield 2007).

• 3. Arbuscular mycorrhizal fungi are usually present as multispecies communities in soils and often more than one species is present in a single root system of the host plants under field conditions (Jansa et al. 2003b). This is in contrast to most experiments, usually scrutinizing the effects of a single strain of AM fungus alone on plant growth, nutrition, and disease tolerance. We know that different AM fungal strains and species differ in their growth patterns, efficiency to acquire P from different distances from roots and/or other features (Jakobsen et al. 1992; Munkvold et al. 2004; Jansa et al. 2005). However, by simplifying the plant-AM fungal diversity of our experimental systems beyond the levels encountered in nature, we have missed possible interactions between members of a composite fungal community such as underground diversity facilitation (Maherali and Klironomos 2007) or functional complementarity (Koide 2000; Jansa et al. 2008). These phenomena deserve further attention, due to their direct relevance to the field reality. Moreover, it has been recognized that specific bacterial community does associate to the soil mycelium of the AM fungi, that these communities depend on the identity of the “carrier” AM fungus, and that these additional players may be important for soil nutrient release and other underground processes (Johansson et al. 2004; Artursson et al. 2006; Toljander et al. 2006). It would be very interesting to test whether different species compositing an AM fungal community differ not only in niche partitioning but also in functional partitioning, e.g. one species delivering P, another Zn, and another conferring disease resistance to soilborne pathogens. Since various agricultural practices such as tillage, crop rotation, and fertilization have been shown to affect the composition of the AM fungal communities in soils, it can be anticipated that these changes will also affect mycorrhizal functioning in beans and other host plants (Rosemeyer and Gliessman 1992; Jansa et al. 2006). There is a great need to quantify these changes now. Symbiotic mutants may play an important role here, especially if it would be possible in the future to obtain symbiotic mutants of beans retaining their capacity to establish association with rhizobia, but not with the AM fungi (i.e. nod⁻myc⁺ phenotype).

So far, no particular breeding efforts have been undertaken to maximize mycorrhizal benefits to the beans, neither by the native AM fungal communities nor by industrial inoculant strains. Nevertheless, it is possible that screening for low-P tolerance might have unintentionally identified genotypes, which benefited from the AM symbiosis more than others – although evidence for this remains equivocal (Yan et al. 1995b). Positive growth responses of beans to mycorrhizal inoculation in non-sterile soil have been described (Daniels-Hylton and Ahmad 1994). However, no industrial inoculation by AM fungi is yet applied to common beans at any larger scale in the world to the best of our knowledge. This is because of lacking low-cost technology for production and application of AM fungal inoculum and uncertainties about competitiveness of the industrial AM fungal strains with native AM fungal communities.

9.2.5 Tripartite Symbiosis

The signalling pathways activated during establishment of both rhizobial and mycorrhizal symbioses by leguminous plants show high level of parallelism and interdependency (Stracke et al. 2002; Gherbi et al. 2008; Kosuta et al. 2008), indicating common evolutionary origin of the different symbioses (Parniske 2008). Since some sort of nodules occur also in podocarps, which do not accommodate any N₂ fixing prokaryotes, but the AM fungi (Baylis 1969; Russell et al. 2002), it is possible that nodulation presents an ancient feature of plants to interact with symbiotic microbes, and that this only later adapted for accommodation of the rhizobia. Further, nutrient and carbon balances and growth effects on the plants depend on identity and activity of both kinds of microsymbionts in their roots (Mortimer et al. 2008). This advocates that the interaction between plants, rhizobia, and AM fungi shall not be regarded in separation from each other, as it frequently happened in the past due to historic reasons, but that efforts shall be made to study this three-­member (tripartite) symbiosis as one unit. Clearly, this means that a higher level of internal dynamics and regulatory processes will need to be considered and that additional nutrients and carbon fluxes (Fig. 9.1) will need to be quantified and understood as compared to any two-member symbiosis. However, quite remarkable amount of empirical knowledge was accumulated already about nutrient and carbon balances and mutual interactions within a tripartite symbiosis of different legumes, and some general patterns begun to emerge recently. Here we briefly review the state-of-the-art and attempt to disentangle the interdependencies between the different nutrients and carbon fluxes in bean tripartite symbiosis.

Both rhizobia and AM fungi require reduced carbon compounds originating from the plant photosynthesis to cover their energy and construction needs. Each of the microsymbionts appears to consume up to 25% of plant photosynthates (Paul and Kucey 1981; Kucey and Paul 1982; Snellgrove et al. 1982; Harris et al. 1985; Jakobsen and Rosendahl 1990) and their combined effect appears to be a sum of those figures. This means that the rhizobia and AM fungi compete for a large fraction of plant carbon. On the other hand, some evidence suggests that plant may increase its photosynthetic rates so as to compensate for the carbon supplied to its root symbionts (Harris et al. 1985; Wright et al. 1998). It has also been shown that such stimulation of photosynthetic rates negatively correlates with plant nutrient status (Jia et al. 2004), which may be the primary cause of downregulation of the symbioses upon sufficient plant nutrient status (Schulze 2004; Bittman et al. 2006; Valentine and Kleinert 2007). However, it is not known, which microsymbiont presents the dominant carbon sink, how the carbon is partitioned in the tripartite system, and how the fluxes are regulated. Recently, temporal partitioning has been suggested between AM fungal and rhizobial symbioses developing on the same bean roots, with the fungi being a major carbon sink from the early stages of plant growth, and nodules increasing their importance later in the ontogeny (Mortimer et al. 2008). Obviously, more information need to be collected on the carbon fluxes in the tripartite symbiosis, with particular attention to fine temporal and spatial resolutions, and looking at the effects of genotypic variation of plants, rhizobia, and AM fungi, as well as how the processes were influenced by changing environmental conditions (Zhang et al. 1995; Haase et al. 2007).

In exchange to carbon, the AM fungi provide to the plant P and other mineral nutrients such as Cu and Zn taken up from the soil. The efficiency of P supply via the AM fungi depends on availability of P in the soil as well as on intrinsic properties of the AM fungal species involved (see above). A significant portion of the P is immobilized in the nodules, where the P concentration may exceed several fold the P concentration in roots and shoots (Israel 1987; Al-Niemi et al. 1998; O’Hara 2001). Thus, affecting plant P acquisition, the mycorrhizal symbiosis plays an important role in enabling the rhizobial symbiosis to develop and function. Whether there are direct (not plant-mediated) interactions between the mycorrhizal fungi and the rhizobia, is not yet known – although some investigations showing unique AM fungal communities inhabiting legume nodules indicate this possibility (Scheublin et al. 2004). Nitrogen fixation by the bacteroids inhabiting root nodules is dependent almost exclusively on the nitrogen fixing capacity of the prokaryotes. Atmospheric dinitrogen is nearly always present in excess, and the fixation process is then governed by physiological state of the bacteroids, mineral nutrients and energy supply from the plants, as well as by removal of the reduced nitrogen from the nodules (Hartwig and Trommler 2001; Schulze 2004). Since the AM fungi are likely to obtain N for covering their own structural and metabolic demands from the soil (Hawkins and George 1999; Jin et al. 2005), it is not obvious, whether there could be any direct interactions between the rhizobia and the AM fungi, apart from some limited competition for root space to colonize. For example, Baird and Caruso (1994) reported about different appearance of nodules in bean plants colonised or not with AM fungi. The plants inoculated with both symbionts formed nodules in large clusters as opposed to the single or loosely clustered nodules that formed on plants inoculated only with the rhizobia. Certainly, most of the interactions between the two microsymbionts are mediated through the host plant – which has to supply its associated microbes with carbon, but which also derives multiple benefits and can perform better under nutrient limiting or otherwise stressful conditions (Izaguirre-Mayoral et al. 2000; Ruiz-Lozano et al. 2001).

Indeed, the literature is full of examples of additive or synergistic effects of establishment of tripartite symbiosis on growth and yields of different leguminous plants including common bean (Bethlenfalvay et al. 1987; Vejsadová et al. 1988; Azcón and Barea 1992; El Ghandour et al. 1996; Ibijbijen et al. 1996; Requena et al. 1997). For example, the bean plants inoculated with both rhizobia (mixture of R. leguminosarum and R. tropici) and AM fungi (Glomus sp.) produced significantly more biomass and greater pod yields compared to non-inoculated control and to singly inoculated plants (Aryal et al. 2003). It has also been noted that dual inoculation of the beans with rhizobia and AM fungi resulted in greater relative benefits if nutrients were supplied as organic in contrast to mineral fertilizers (Aryal et al. 2003, 2006). This has been explained by absence of inhibition of the BNF and AM fungal activities in organically fertilized plants as compared to the soils amended with mineral fertilizers, because the latter increased the immediate N and P availabilities in the soil thus mediating suppression of the symbioses by the plants (Aryal et al. 2006). On the other hand, great variability of responses was observed between different genotypes of beans combined with different strains of AM fungi and rhizobia (Daniels-Hylton and Ahmad 1994; Ibijbijen et al. 1996; Neeraj 2005). For example, bean cultivars Negro Argel and Rio Tibagi in association with rhizobia derived greater P uptake benefits from association with Glomus manihotis than with G. etunicatum, whereas such differences were not evident in Carioca. However, these differences did not necessarily translate into differences in growth responses, probably due to differential carbon requirements by the different AM fungi (Ibijbijen et al. 1996). These results indicate that the best performing and most yielding combination might need to be selected for each bean genotype, probably also with regards to the target environmental conditions (Ahmad 1995). This is because different genotypes of beans as well as different genotypes of AM fungi and rhizobia do likely have different ecological optima for their performances. Moreover, the different microsymbionts will also be differentially affected by agricultural practices such as tillage and pesticide application (Zahran 1999; Jansa et al. 2006; Laguerre et al. 2006). Thus, optimizing the bean symbioses for a particular agroecosystem will certainly be a great challenge of the future research.

9.3 Improving Yield of Beans in Stressful Environments

The agriculture in Africa is confronting major challenges, facing the ongoing human population growth and its aspiration for sufficient food quantity, healthy diet and greater standard of living on one side, and stagnating crop yields, soil degradation, climatic change and raising uncertainties about future rainfall distribution on the other side (Lal and Singh 1998; de Wit and Stankiewicz 2006; Battisti and Naylor 2009). There are few possibilities how to improve agricultural production in general and the production of common bean in particular, and to increase the sustainability of agriculture in the tropics, particularly in the sub-Saharan Africa. It is possible by: (i) Improving soil management practices, e.g. using better fertilization strategies; (ii) Modifications of the cropping systems; (iii) Using improved crop cultivars; (iv) Exploitation of the potential of soil microorganisms establishing symbioses with plant roots; or (v) Combination of these different options (Singh 1999a; Broughton et al. 2003; Kelly 2004). In this section, we present potential measures requiring one- or two-step modifications of the current practices. These should be relatively easy to apply and would positively impact the production system, although their implementation may take certain time and require additional research efforts. In the following section, some deeper changes are proposed, which would generally require several modifications of the production systems or major paradigm shifts, but shall offer longer-term and more sustainable perspectives.

9.3.1 Management of Soil Fertility

There is a great need to increase agricultural productivity in large areas of tropical Africa, due to enormous population pressure and inherent low fertility of local soils. If the human food demands in these areas are to be met by local production, dramatic increases in agricultural productivity must be realized now (Lal 2007). This is not possible without fertilization of the crops and without management of soil organic matter. Although fertilizers are sometimes applied in sub-Saharan Africa (Vanlauwe and Giller 2006), their quality and applied amounts rarely match the needs. Therefore, fertilizer application shall be greatly increased and go hand-in-hand with improvement (or at least slowdown of degradation) of soil organic matter status. This applies invariantly for production of any crops including the common bean. Although N demand of beans is lower than that of cereals since part of it can be covered from the BNF, bean production can still be greatly improved by application of N fertilizers (see above). Demand of beans for P fertilization is at least as high as for other crops, and low P availabilities in the soils seem to be one of the main limitations of bean production in sub-Saharan Africa. However, little knowledge is available about fertilizer demands of cropping systems others than the monocrops. This is very relevant for bean production since it is most often grown in association with other crops. Additionally, blanket fertilizer recommendations may be of limited relevance in smallholder farms, which experience a great heterogeneity in soil types and past managements (Zingore et al. 2007).

Phosphate rocks and crude oil and natural gas reserves (representing the important non-renewable resources for production of mineral P and N fertilizers) are abundant in sub-Saharan Africa, yet this does not seem to relieve the local farmers from the scarcity of high quality and financially affordable fertilizers. Additionally, many of the rock phosphates available locally show very low water solubility, which limits their direct use in agriculture (Vanlauwe and Giller 2006). Often mentioned organic fertilizers appear to be a good solution for improving soil fertility, replenishing nutrients removed from the fields with previous crops as well as enhancing soil organic matter status (Kayuki and Wortmann 2001). However, production of organic fertilizers demands both space and labour and in the end will not solve all the problems because of relocation rather than replenishment of losses of nutrients such as P and K at the farm or landscape levels (Vanlauwe and Giller 2006). Further, introducing organic materials to the soils may result in termite attraction to the fields (Bünemann et al. 2004) and in subsequent increase of the risk of crop losses due to higher pest pressure. Therefore, integrated soil fertility management is necessary to accompany system development on its way to sustainable productivity increase (Bationo et al. 2007; Frossard et al. 2009). One of the measures, which are recently being adopted to combat soil nutrient mining, is the application of small amounts of (mainly) locally produced fertilizers in bands below seeding rows or directly into the seeding holes, so called strategic fertilizer inputs. Although this usually does not have long-lasting effects on soil fertility, it increases agricultural productivity and optimizes fertilizer use efficiency at moderate costs, though with relatively high labour investments (Woomer et al. 2003; Frossard et al. 2007; Moody et al. 2008; Sokoto and Singh 2008). Application of the fertilizer in deeper horizons may confer additional benefits in drought-prone environments since the upper soil layer may be too dry for the plants to access nutrients in it during parts of the growing season (Du Toit 1997).

9.3.2 Modifications of the Cropping Systems

For various reasons (culture, tradition, insurance of yield, diversification of diet, control of pests, water and nutrient utilization efficiency), common bean will most probably continue to be a key component of intercropping systems rather than a sole crop in Africa (Francis and Sanders 1978; Daellenbach et al. 2005; Tamado et al. 2007). Careful selection of bean cultivars and planting times to minimize interferences between the combined crops is needed, and this requires good understanding of crop physiology and its nutrient demands (Graham and Ranalli 1997; Daellenbach et al. 2005). Efforts should be made to diversify cropping sequence by including vegetables such as cabbage or short (improved) fallows for animal feed production and soil fertility restoration. Not only this could disrupt cycles of certain pathogens, but it could also improve utilization of local phosphate rocks as shown previously (Weil 2000). Some legume fallow species may mediate significant N inputs to the system, unlike common beans (Chikowo et al. 2007), as well as they may contribute to substantial improvements of the soil organic matter content (Mando et al. 2005). However, different sites and production systems will certainly opt for different solutions. This means that understanding of each particular system is inevitable for proposing new options (Franke et al. 2008).

9.3.3 Improvement of Plant Genotype

Since only a small fraction of the common bean genetic variability is currently present in the commercial lines, a significant potential still exists to develop new lines or to introduce new traits into currently cultivated genotypes (Singh 2001). Furthermore, novel traits can also be introduced from closely related botanical species by traditional breeding methods (Rodriguez-Uribe and O’Connell 2006; Marquez et al. 2007) or from virtually any other organism by genetic engineering approaches (Veltcheva et al. 2005; O’Kennedy et al. 2006). These options shall be used to widen the genetic base of future bean varieties in Africa. Past breeding efforts greatly improved the resistance of beans against various pathogens. It is desirable to further enhance widespread adoption of the improved genotypes by the farmers and to improve spreading information about their availability, benefits, and requirements. Further efforts shall continue to search for and implement alternative resistance mechanisms to viral, fungal and/or bacterial diseases, since it is expected that current resistance mechanisms will be overcome by the pathogens at some point (Laine and Tellier 2008). Development of genotypes adapted to low soil fertility should also be given high priority now. However, in the long term, their importance is limited for two reasons – first, nutrient mining must be stopped in Africa to prevent nearing system collapse, and, second, it seems that high internal use efficiency of nutrients does not necessarily translate to high yields as the production of seeds requires quite a narrow range of nutrient concentrations per unit of weight of seeds. Furthermore, it appears that tolerance to low soil fertility is not necessarily ­determined by a single or a few genes, as is often the case in disease resistances, and that the genetic determinants of the tolerance to low fertility are often not known. Rather, secondary markers are used such as root growth pattern and BNF efficiency for selection of lines adapted to low fertility soils (Araujo and Teixeira 2000). Genotypes adapted to high temperatures and soil acidity and Al and Mn toxicities will probably be important at both short and long-term, since they do perform better in many places in Africa suffering from these constraints. These adaptations may also support greater symbiotic activity in the roots due to higher root vitality and generally better plant performance and photosynthesis under stressful conditions (Hungria and Vargas 2000; Miyasaka and Hawes 2001).

Breeding for drought tolerance is a major challenge. Although it is clear that selection for tolerance to drought will increase yields in areas with limited rainfall, as well as it may improve performance of the beans in low P soils (Beebe et al. 2008), breeding efforts alone could not solve the problem of large environmental variations such as catastrophic droughts and extremely erratic weather. These events will, according to current climate models, become more frequent in some parts of Africa due to climatic changes, and they will probably remain largely non-predictable (Phillips and McIntyre 2000; de Wit and Stankiewicz 2006; Battisti and Naylor 2009). Moreover, pronounced changes in growth habit and/or plant water and nutrient efficiency may impose a trade-off (a penalty) on the yields and/or disease resistance (Haugen et al. 2008). Therefore, it is important to promote drought tolerant bean varieties that also yield well under a range of water and nutrient supply conditions and where other beneficial traits (such as resistance to diseases) are not sacrificed.

There is very little done with respect to breeding for greater symbiotic benefits in the common beans, in spite of the fact that a great impact of lines with enhanced BNF efficiency is anticipated for the resource poor farmers (Herridge and Rose 2000; Crouch et al. 2004). Although some variability in BNF efficiency was identified among different common bean genotypes, very few lines derived more than 50% of their N from the atmosphere (see above). Therefore, the potential to improve BNF in beans is still high. In some legume species (pea, soybean, barrel medic, Lotus), so called super – or hypernodulating mutants were identified, which showed very high fixation rates of atmospheric N₂ being unaffected by mineral nitrogen availability in soils (Fujikake et al. 2003; Schnabel et al. 2005; Ishikawa et al. 2008). Hypernodulating genotypes are not yet known for common bean. Compared to the BNF, even less is understood about genetic basis of variation in benefits derived from the AM symbiosis in the common bean, and to the best of our knowledge, there have been no breeding efforts to improve mycorrhizal symbiosis in beans. For any future breeding programs, it is highly recommended to check whether the rates of root colonization by AMF and nodulation as well as the symbiotic benefits are not decreased as a side effect of the breeding/genetic modifications. This appears relevant as gradual decrease in mycorrhizal responsiveness was described for modern as compared to old wheat and soybean cultivars (Khalil et al. 1994; Zhu et al. 2001), indicating that plant genotype improvement efforts may also bring along some unintended damage of the genetic base. It has to be noted here that there is a potential to speed up the progress in targeted breeding for greater symbiotic benefits now as concerted research efforts resulted in establishment of a large population of induced mutants of common beans. This resource will allow identifying genetic base of certain symbiosis-related traits (Blair et al. 2007) and establish genetic markers for the marker assisted selection.

Biofortification efforts may prove very important for the increase of nutritional quality of the beans for human consumptions. Ongoing research aims at identifying routes to enhance N, Zn, Fe, and vitamin contents in the seeds and the availability of these elements to humans (Donangelo et al. 2003; Blair et al. 2009). On the other hand, the concentration of P in the seeds shall be kept moderate to low as the major form of P in the seeds is phytic acid, which may interfere with resorption of valuable nutrients and other compounds in human gut (Frossard et al. 2000; Donangelo et al. 2003).

9.3.4 Enhanced Symbiotic Benefits

Apart from limited short-term perspectives in adapting the plant genotype for enhanced symbiotic benefits (e.g. super – or hypernodulating mutants) as discussed above, there are two major ways to improve the performance of the root symbioses established by the beans. One is changing the microbial communities (either by inoculation or indirectly by system management), and another is increasing the efficiency of the current symbionts by optimizing the environmental conditions. The latter may encompass simple measures such as using starter urea fertilizer to improve nodulation and BNF (Daba and Haile 2002; Mendes et al. 2003), using organic instead of mineral fertilizers to limit inhibition of the BNF and AM fungal symbioses (Aryal et al. 2006), or application of moderate P fertilizer levels to crops growing in severely P deficient soils to enhance mycorrhizal benefits (Picone 2002; Jansa et al. 2006).

No microbial inoculants are yet broadly applied in bean production. This is in spite of the facts that bean-associated rhizobia are relatively easy and cheap to produce, and also a growing number of companies is offering AM inoculum with broad plant-species specificity (Vosátka et al. 2003). Research results indicate potential of inoculation to improve plant nutrition and yields upon successful introduction of selected microbes into the rhizosphere, especially if combined in synergistic consortia (Requena et al. 1997; Lekberg and Koide 2005; Tilak et al. 2006). Apart from documented nutritional benefits (see above), introducing trehalose-overproducing rhizobia into bean rhizosphere could confer drought tolerance to the plants (Suarez et al. 2008). By enhancing development of AM fungi, soil aggregate stability could improve leading to reduction of soil erosion rates (Six et al. 2004; Cavagnaro et al. 2006). However, application of inoculants may prove to be a tricky task, and there is still only a limited mass of reliable data on survival and competitiveness of the introduced inoculants with the native ones in the soil, particularly with respect to the AM fungi (Hungria et al. 2000; Sessitsch et al. 2002; Moawad et al. 2005; Jansa et al. 2006; Bogino et al. 2008).

The consensus appears to be that symbiotic efficiency is not necessarily linked to competitiveness of the different microbial strains, as shown on example of rhizobia: The most efficient strains may not be able to survive in field soil, whereas less efficient strains (in terms of BNF efficiency) may be greatly competitive (Hafeez et al. 2001). Therefore, for industrial inoculum application, it appears imperative to select microbes, which are both highly beneficial and competitive under field conditions. Furthermore, securing inoculum quality and disentangling effects of microbes from that of inoculum additives is not an easy task (Catroux et al. 2001; Date 2001; Vosátka et al. 2003; Deaker et al. 2004). Thus the economic viability of inoculant technology in bean production shall be carefully scrutinized and compared, without preoccupations, to that of other measures such as application of mineral fertilizers (Wander et al. 2007).

Any modification to production system management is another interesting option for manipulation of indigenous microbial communities for improving the crop production. It is known that inputs of organic matter to the soil or change of tillage management may have pronounced effects on composition and activity of soil microbes including rhizobia and the AM fungi (Kiers et al. 2002; Jansa et al. 2003b, 2006; Kaschuk et al. 2006b; de Fatima et al. 2007). However, the role of the different symbiotic microbes in plant nutrition in these different agricultural management systems is very rarely quantified and separated from the other confounding effects (water availability, soil temperature, root growth, nutrient availability in soil solution etc.). This remains to be a major research gap, which shall be best closed by using well characterised bean genotypes (Jebara and Drevon 2001; Saadallah et al. 2001b) in combination with a selection of functionally diverse AM fungal and rhizobial strains (Hungria et al. 2000; Jansa et al. 2005, 2008). Such studies should also incorporate bean mutants deficient in AM and/or rhizobial symbioses formation. Using isotope labelling (either as mono – or multitracer) and spatially compartmented containers would allow direct observation of the role of AM fungi in the P, Zn, and Cu nutrition, for example (Joner et al. 2004, 2005). A second step would be identification of the diversity and activity of AM fungal and rhizobial communities in the bean-producing agroecosystems in Africa. Only then, the necessary background knowledge about the importance of root symbioses for bean production in the region would allow the decisions about potential of managing the microbial communities for improved bean production. As stressed by Vance (2001), the use of AM fungi and rhizobia in agroecosystems will be fully realised only as we: (1) Ascertain how the diversity of specific microorganisms contributes to growing crops; (2) Identify the biochemical and genetic mechanisms regulating nutrient exchange; and (3) Determine, whether there is a yield penalty for effective symbiosis.

9.4 Concluding Remarks, Challenges and Perspectives

Great challenges are approaching global agriculture in general and that in Africa in particular in the twenty-first century. Global agriculture will have to provide sufficient amounts of food for the still-growing human population on Earth and fulfil the higher food quality demands, using limited land and declining non-renewable resources. The failure in progress to fulfil UN Millennium development goals in Africa speaks for itself (Lal 2007; UN 2008). Better utilization of bean symbioses for sustainable and high bean yields are promising, though long-term perspectives with a lot of research still to be conducted. Realization of this outlook will require, at least, moderate P inputs, best in form of organic fertilizers. It is at least theoretically possible to achieve development of highly mycorrhizal – and BNF-dependent cultivars and efficient and cost-effective inoculation strategies with superior microbial strains, both in term of symbiotic benefits and in terms of competitiveness with indigenous strains, adapted to site-specific conditions. Therefore, plant symbioses deserve much research attention, although it is premature to make any promises now. Additionally, availability of water will be critical in the next decades in many places in Africa (Phillips and McIntyre 2000), and options to irrigate cropped fields shall be carefully considered, regardless of the current economy or political situations. Livestock production in Africa shall be promoted so as to improve quality and diversification of human nutrition, provide greater income to the farmers, and increase availability of manure for soil fertilization. As a consequence, some land used these days for subsistence cropping could be converted to mixed crop-livestock systems, which would offer diverse options for management of soil fertility, plant diseases, and combating soil degradation and erosion (Rutunga et al. 2007). Furthermore, nutrients contained in human excreta shall also be consequently recycled and their losses prevented. Utilization of human excreta is already practiced in some parts of Africa such as in peri-urban agriculture in Burkina Faso (Eaton and Hilhorst 2003), but high sanitary risks are currently associated with these practices. These should be addressed so as to prevent disease outbreaks. Very long-term perspectives of bean production would encompass changing soil conditions by application of charcoal. It has been shown that charcoal additions to the soil may benefit BNF and bean yields (Rondon et al. 2007). This fascinating and ancient avenue to improve soil fertility (Glaser 2007) is currently attracting lot of attention, although its obvious limitation in the modern times is the availability of sufficient biomass quantity for charcoal production (Sunseri 2005). However, large amounts of plant biomass may potentially be available in the context of climate change remedial measures in a way the developed countries compensating for their CO₂ footprint would provide biochar for soil amendments in the tropics. If carried on a large enough scales, this would bring along benefits to both developing and developed countries.

It is not quite clear what are the main reasons for the contemporary widespread adoption of common bean in Africa in spite of the fact that it is an alien plant species to the continent. Native legumes such as peas or lentils are not produced in any comparable amounts. However, these native alternatives could be considered as potential replacement for beans shall the efforts to adapt the bean production for future environmental situations fail. Furthermore, other income sources for local populations shall be identified and supported such as tourism and diversity conservation, with accompanied financial benefits, lowering dependency of local human populations on the subsistence farming (Huston 1993; Gadd 2005). It is clear that these perspectives are closely related to political stability and significant infrastructure development. Although these are not easy to achieve in any African country, as documented by the recent riots in Kenya, Madagascar and elsewhere, they are truly within the capacity of the local governments and must be solved solely by them.