Breeding Crops for Tolerance to Acidic Soils in Ethiopia: A Review

Soil acidity and associated low nutrient availability is one of the constraints to crop production on acid soils. In Ethiopia, soil acidity is a well-known problem limiting crop productivity. The management of acid soils should aim at improving the production potential by the addition of amendments to correct the acidity, manipulate the agricultural practices and using acid tolerant crops to obtain optimum crop yields. In this paper, we review some of the most recent applications of different breeding approaches for improving crop yield under acidic soils condition. In addition to this review paper aimed to put together recent achievements made through research on developing soil acid tolerant cereal and food legumes in Ethiopia. These newly released cereal and legume crops gave additional option for our farmers living in acid soil prone areas


INTRODUCTION
Soil acidity is one of the major abiotic constraints affecting crop productivity which is caused by a low potential of hydrogen (pH).It is among the major land degradation problems, which affects ~50% of the worlds potentially arable soils (Kochian et al., 2004).Considerable grain yield reductions of crop under low soil pH have been reported in numerous studies.In Ethiopia currently about 40% of the total arable land was affected by soil acidity, out of this about 27.7 % is moderately acidic and 13.2% is strongly acidic (Adane, 2015).As a result, most of the soils have a pH range of 4.5 to 5.5 and contain low organic matter and also low nutrient availability (Achalu, 2014).The poor fertility of acidic soils is due to a combination of mineral toxicities (Al, Mn, and Fe) and nutrient deficits caused by the leaching or decreased availability of phosphorus (P), calcium (Ca), magnesium (Mg), sodium (Na), and micronutrients such as molybdenum (Mo), zinc (Zn), and boron (B) (Gupta et al., 2013).In the humid tropics, soils become acidic naturally due to leaching of basic cations under high rainfall conditions.At pH below 5, Al is soluble in water and becomes the dominant ion in the soil solution.In acid soils, excess Al primarily injures the root apex and inhibits root elongation (Sivaguru and Horst, 1998).The poor root growth leads to reduced water and nutrient uptake, and as a result crops grown on acid soils are constrained with poor nutrients and water availability.The net effect of which is reduced growth and yield of crops (Marschner, 2011;Wang et al., 2006).Crop tolerance of acidic soil has become extremely important in the agricultural development of the humid tropics (Kamprath and Foy, 1985).The use of tolerant crop varieties is considered to be the best complement to non-genetic management option for combating Al-toxicity problem (Rao et al., 1993;Abebe, 2007) This paper reviews crop improvement for tolerance to acidic soils using conventional and molecular technologies.It also reviews the genetic, physiological, and biochemical mechanisms by which plants tolerate low soil pH stress.The adoption of existing and improved acid-tolerant crop genotypes is also taken into account.

FORMATION OF ACID SOIL Distribution of Acid Soil in Ethiopia
Soil acidity and associated low nutrient availability are key constraints to crop production in acidic soils, mainly Nitisols of Ethiopian highlands.Haile et al. (2017) estimated that 43% of the Ethiopian cultivated land is affected by soil acidity.Nitosol/Oxisol soils are the main soil classes dominated by soil acidity.These soils are predominantly acidic and have been found that more than 80 % of the landmasses originated from Nitosol are acidic.

ABSTRACT
Soil acidity and associated low nutrient availability is one of the constraints to crop production on acid soils.In Ethiopia, soil acidity is a well-known problem limiting crop productivity.The management of acid soils should aim at improving the production potential by the addition of amendments to correct the acidity, manipulate the agricultural practices and using acid tolerant crops to obtain optimum crop yields.In this paper, we review some of the most recent applications of different breeding approaches for improving crop yield under acidic soils condition.In addition to this review paper aimed to put together recent achievements made through research on developing soil acid tolerant cereal and food legumes in Ethiopia.These newly released cereal and legume crops gave additional option for our farmers living in acid soil prone areas.
Some of the well-known areas severely affected by soil acidity in Ethiopia are Ghimbi, Nedjo, Hossana, Sodo, Chencha, Hagere-Mariam and Awi Zone of the Amahara Regional State (ATA, 2014).The extent of soil acidity in Ethiopia is shown in Figure 1.About 28.1% of these soils are dominated by strong acid soils (pH 4.1-5.5)(ATA, 2014).Strongly acidic soils are usually infertile because of the possible Al and Mn toxicities, and Ca, Mg, P, and molybdenum (Mo) defciencies (Barber, 1984).

CAUSES OF SOIL ACIDITY
Soil acidification is a complex set of process resulting in the formation of an acid soil.The amount of Hydrogen cation (H+) activity in the soil solution determines the soil pH and is influenced by edaphic, climatic, and biological factors.High rainfall affects the rate of soil acidification when rainfall washes away bases (Ca2+, Mg2+, K+, Na+, and carbonate ion (CO3-2)) from the soil.Hydrolysis results in a reduction in soil pH when a metal is dissolved in water, releasing protons.
The hydrolytic displacement of base cations and the provision of additional acids from oxidation reactions are the main natural causes of soil acidification, which lead to base-deficient, aerated sands under strong leaching conditions such as high rainfall and drainage (Fey, 2001).Poor agricultural practices (use of ammonium fertilizers and crop removal) also contribute to the acidification of the soil (Rowell, 1998).Continuous application of inorganic fertilizer without soil test, in the end, can increase soil acidity.
The use of N fertilizers in ammonia form is a source of acidification (Fageria and Nascente, 2014; Guo et al., 2010).Soil acidification is intensified by the removal of cations through the harvesting of crops and by acid precipitation from polluted air (Hede et al., 2001).

Toxification of Acid Soils
Acid soil toxicity is caused by a combination of high solubility of toxic heavy metal elements (iron, copper, manganese, zinc, and aluminum), a lack of essential nutrients (phosphorus, magnesium, calcium, potassium, sodium), and low soil pH (Bian et al., 2013).Low soil pH can therefore generate excesses of aluminum, iron, and manganese, which hamper crop production.As aluminum and iron are released during the acidification/weathering process, they become more accessible on cation exchange sites, in solution, or simply on exposed surfaces.
Both ions react readily with phosphate, forming relatively insoluble compounds through a process known as phosphate fixation.High Al and Fe oxides and hydroxide in low soil pH are responsible for P fixation, making it unavailable to plants (Oboru, 2008).The pH of soils for best nutrient availability and crop yields is considered to be between 6.0 and 7.0, which is the most preferred range by common field crops (Duncan, 2002).A summary of crop relation to soil reaction is given in Table 1.Cotton, alfalfa, oats and cabbage do not tolerate acid soils and are considered suitable to neutral soils with a pH range of 7-8.Wheat, barley, maize, clover and beans grow well on neutral to mildly acid soils (pH 6-7).Grasses tend to tolerate acidic soils better than legumes, so liming to pH 5.5 may control acidity without limiting production.Legumes, however, need more Ca and perform best between pH 6.5 and 7.5.Among crops tolerant to acid soils are millet, sorghum, sweet potato, potato, tomato, flax, tea, rye, carrot and lupine (Somani, 1996).

MANAGEMENT OF ACID SOIL
Liming is a major and effective practice to overcome soil acidity constraints and improve crop production on acid soils.Soil acidity can be corrected easily by liming the soil, or adding basic materials to neutralize the acid present.The most economical liming materials and relatively easy to manage are calcitic or dolomitic agricultural limestone (Pilbeam and Morley, 2007;Rengel, 2011).Integrated soil fertility management (ISFM) is one of the approaches to manage and improve soil health and fertility status (Agegnehu and Amede, 2017).ISFM is one of the components of the management of acid soils.Farmyard manure (FYM) and crop residues are among organic plant nutrient sources, which could ameliorate the physical and chemical properties of soils.The addition of organic fertilizers to acid soils has been effective in reducing phytotoxic levels of Al resulting in yield increases.The possible alternative of using organic sources such as crop residues, manures, compost and biochar are substitutes for lime (Agegnehu and Amede, 2017;Sharma et al., 1990).Similar study showed that the residual effects of manure and compost applications signifcantly increased electrical conductivity (EC), pH levels, plantavailable P and NO3-N concentrations (Eghball et al., 2004).The use of acid-tolerant crop cultivars constitutes an efficient and permanent alternative to increase yields in acidic soils (Horst et al., 1997).

ACID SOIL TOLERANCE MECHANISM IN CROP
Aluminum tolerance can be divided into mechanisms that facilitate Al exclusion from the root apex (external tolerance mechanisms or apoplastic mechanisms) and mechanisms that confer the ability to tolerate Al in the plant symplasm (internal tolerance mechanisms or symplastic mechanisms) (Kochian, 1995;Kochian et al., 2004).Several external tolerance mechanisms have been suggested, of which the most important are: 1) exudation of organic acids (Pellet et al.,1995;Magalhaes et al., 2007); 2) immobilization at the cell wall (Taylor, 1991;Kochian, 1995); 3) exudation of phosphate (Taylor, 1991;Ryan et al., 1993); 4) active Al efflux across the plasma membrane (Taylor, 1991); 5) production of root mucilage (Henderson and Ownby, 1991); 6) Al exclusion via alterations in rhizosphere pH (Taylor, 1991;Kochian, 1995), and 7) selective permeability of the plasma membrane (Taylor, 1991).The Al-activated mechanism of malate exudation is well described in wheat (Sasaki et al., 2004), rye (Ligaba et al., 2006), whereas the mechanism of Al tolerance in maize, soybean, sorghum, and barley involves mainly citrate release (Maron et al., 2010).In addition to malate, citrate exudation has also been reported to contribute to Al tolerance in wheat and rye (Yokosho et al., 2011).The most important internal tolerance mechanisms are Al-binding proteins, chelation in the cytosol, compartmentation in the vacuole, evolution of Al tolerant enzymes, and elevated enzyme activity (Taylor, 1991).Substantial experimental evidence supports the synthesis of Al-binding proteins (Somers et al., 1996).

Genetic Mechanisms of Aluminum Tolerance
Fourteen genes from seven different species are known to contribute to Al3+ tolerance and resistance and several additional candidates have been identified (Table 2).Some of these genes account for genotypic variation within species and others do not (Ryan et al., 2011).As explained below, a thorough understanding of both the genetics and physiology of resistance was pivotal for finally identifying the first Al3+ resistance genes.(Conner and Meredith, 1985) and field evaluations (Johnson et al., 1997).Laboratory-and greenhouse-based techniques for screening for Al tolerance are widely used because they are quick, highly accurate, nondestructive, and can be applied at early developmental plant stages.Field-based techniques are more laborious (Carver and Ownby, 1995).

Nutrient Solution Culture
Solution culture is the most common screening medium for Al tolerance which provides easy access to the root system, strict control over nutrient availability and pH, and non-destructive measurements of tolerance (Carver and Ownby, 1995).Different assays have been applied to identify Al tolerant and Al sensitive genotypes, of which the most widely used, are hematoxylin staining of root tips and root growth measurement (Baier et al., 1996;Carver and Ownby, 1995).Plant parameters such as root and top dry weight, height, tiller number, and number of spikelets per ear have also been used to evaluate Al tolerance (Mugwira et al., 1978).Aluminum-induced callose (1, 3-b-DGlucan) synthesis after short Al treatment in nutrient solution has been reported to correlate well with Al tolerance (Horst et al., 1997).Results obtained using the nutrient solution technique has proven to be highly relevant to acidic field conditions.Genotypes classifed as Al tolerant based on the nutrient solution evaluation very often show improved agronomic performance under acid soil and Al stress (Baier et al., 1995).

Soil Bioassays
Soil bioassays have a distinct advantage over nutrient solution culture when Al tolerance may be influenced by soil dependent external factors (Ring et al., 1993).The use of soil media has received less attention than solution media for Al tolerance evaluation, and relatively few examples of its use can be found in the literature (Stølen and Andersen, 1978).

Field Evaluation
The ultimate and most direct method of evaluating for Al tolerance is by measuring economic yield (forage or grain) under field conditions.Field evaluation is normally conducted in two duplicate tests: one in an unamended and naturally acid plot, and the other in a lime-amended plot.The data are reported as the ratio of grain yield in the unamended plot to that in the lime amended plot to adjust for differences in yield potential without acid soil stress (Carver and Ownby, 1995;Johnson et al., 1997).The two most important problems observed when evaluating for Al tolerance in the feld are the presence of fungal pathogens such as take-all (incited by Gaeumannomyces graminis var.tritici), in which infection is often favored by the application of lime to low pH soils (Johnson et al., 1997), or spatial variability of pH in the surface and subsurface soil layers (Carver and Ownby, 1995).There are several examples of evaluating for Al tolerance in the field, but they are more expensive and laborious (Stølen and Andersen, 1978;Baier et al., 1995;Johnson et al., 1997).

Hematoxylin Staining Method
The hematoxylin staining method is an extremely powerful tool for observing tolerance without laborious quantitative measurements.The hematoxylin dye forms complexes with tissue Al that has been immobilized as AlPO 4 by phosphate on or immediately below the root surface (Ownby, 1993).There are several variations of the hematoxylin method.Polle et al. (1978) used the hematoxylin-staining pattern of root tips as an indicator of Al tolerance.As the intensity of staining increases, reflecting a higher level of Al uptake, the level of tolerance decreases.
Another procedure using hematoxylin, the modifed-pulse method, evaluates Al tolerance based on the ability of Al tolerant seedlings to continue root growth after a short pulse treatment with high Al concentrations (Aniol, 1984).Aluminum sensitive seedlings do not show root re-growth because their apical meristem has been damaged.This method can be applied to determine Al tolerance through either measuring root regrowth (Gallego and Benito, 1997) or evaluating seedlings on a 1 to 3 scale (tolerant, medium tolerant, and susceptible) based on their ability to present root regrowth (Riede and Anderson, 1996).

Root Growth Method
The root growth method considers two Al tolerance parameters: root growth (RG) and a root tolerance index (RTI) (Baier et al., 1995).The RG parameter is measured root growth under Al stress while RTI is root growth under Al stress compared to root growth without Al stress.A low-ionic-strength nutrient solution combined with a low Al concentration is used, as evidence suggests that Al tolerance studies should be conducted using solutions containing ionic strength and Al activity approximating soil composition.Assessment of Al tolerance based on root growth and RTI has been used extensively in genetic and molecular studies (Baier et al., 1996;Riede and Anderson, 1996;Somers et al., 1996).

SUCCESSES IN BREEDING FOR LOW SOIL PH TOLERANT CROPS IN ETHIOPIA Soil Acidity Tolerant Food Legume Crop
Fifteen common bean varieties were evaluated for acid soil tolerance at Jimma research center and Mettu Research sub center (Hurumu trial site).The analysis of variance showed that the main effect of amendments, varieties and years, and the interaction effect of amendments by different varieties and years had a significant effect on grain yield and biomass of common bean.At Mettu the highest (2703.7 kg/ha) mean grain yield of common bean was obtained from SER 119 variety under both lime and phosphorus treated main plot and the highest (1864.4kg/ha) mean grain yield of common bean was obtained from the same varieties under control soil condition.The highest (6.44t/ha) above ground biomass was obtained from SER 119 variety under both lime and phosphorus treated plot, while the highest (4.17t/ha) above ground biomass was obtained from Awash-1 variety under control soil conditions at Mettu (Table 10).Common bean varieties SER 119 & Awash-1 gave the best performance for most of the traits tested and these are promised varieties among the other (Table 10).
Table10.Mean values of common bean yields and above ground biomass as affected by interaction of amendments, varieties and year at Mettu.  7).Tolessa (2018) research results also indicated that, the existence of significant genotype x amendment interactions for all root, nodule and yield and yield components parameters imply the presence of differential response of Soybean genotypes for different soil amendments.Soybean genotype PI567046A & HAWASSA-04 variety gave the best performance for most of the traits tested and these are promised genotypes among the other tested.Tolerance index and mean productivity value indicated that Soybean genotype PI567046A and variety HAWASSA-04 performed well for most of the traits and selected as tolerant (Tolessa, 2018).

Soil Acidity Tolerant Cereal Crops
Case studies showing seed yield improvements of some Oat genotypes under acidic soil conditions at Holeta agriculture research center are summarized in Table 5.The candidate varieties along with collected oat accessions were planted on acid soils in multi-locations.Analysis of variance revealed that 79Ab 382 80 SA 94 showed the highest mean seed yield under unlimed soil conditions as compared to other accessions (Table 5).This newly released food oat variety known with local name "Sorataf" gave additional option for our farmers and emerging food agro industries.Therefore, popularization and seed multiplication of this newly released food oat variety should be given a great emphasis especially on acid prone areas of Ethiopia (Fekadu, 2018).
To identify acid tolerant high yielding and promising bread wheat varieties an experiment was conducted at Holeta.The candidate varieties along with one hundred fifty bread wheat accessions collected from National Program Coordinating Centre (Kulumsa) were planted on acid soils in multilocations under unlimed conditions.Analysis of variance revealed that ETBW 6785 showed the highest mean grain yield across testing locations as compared to other accessions (Fekadu, 2018).

CONCLUSION
Soil acidity has become a great threat in food production through limiting the production potential of the crops because of low availability of nutrients, basic cations and excess hydrogen (H+) and aluminium (Al3+) in exchangeable forms.The practice of liming acid soils to mitigate soil acidity and reduce phytotoxic levels of Al and Mn has been recognized as necessary for optimal crop production in acid soils.I However, these methods have limited practicality for resource poor farmers to apply high rates of lime as well as mineral fertilizers, mainly due to their low purchasing capacity, low availability of lime, high cost of mineral fertilizers and lime transportation, has kept lime and mineral fertilizers from reaching smallholder farmer"s fields.Hence, the use of Crop varieties that are tolerant to acidic soils and produce reasonable good yield is paramount importance.Over the past decade, several researchers around the world have focused their efforts on identifying and characterizing the mechanisms employed by crop plants that enable them to tolerate Al toxic levels in acid soils.The two distinct classes of Al tolerance mechanisms are those that operate to exclude Al from the root apex and those that allow the plant to tolerate Al accumulation in the root and shoot symplasm.Plant genetic resources are a rich source of valuable traits that could be used to improve crop species.The presence of crops genetic diversity in Ethiopia is an opportunity for tolerance to low soil pH would increase the potential for the development of high-yielding cultivars with high levels of tolerance to low soil pH as well as toxicities of Al, Fe, and Mn.More research should be devoted to crop tolerance to acid soil.To raise the level of adoption of improved crop cultivars under acidic soils, farmers should be involved in the selection process through participatory breeding and selection approaches.

Table3.
Crop relation to soil reaction (pH) Table2.Summary of genes involved in Al3 + resistance or tolerance Table7.The interaction effect of amendments and Soybean genotypes on yield under lime and Phosphorus treated and untreated acid soil condition during 2017 and 2018 main cropping season.
Misgana et al., 2018).To identify acid tolerant high yielding and promising triticale varieties an experiment was conducted at Holeta.The candidate varieties along with one hundred forty triticale accessions were planted on acid soils in multi-locations under unlimed conditions.Analysis of variance revealed that ETCL 161 showed the highest mean grain yield across testing locations as compared to other accessions (Fekadu, 2018).