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5 Technologies for Soil Improvement More than two-thirds of the agricultural land in sub-Saharan Africa (SSA) is considered to be severely degraded, and the situation is equally alarming in South Asia (SA) (FAO, 1994; GEF, 2003). If agricultural pro- duction in those regions must double in the next 2 decades, as implied by estimates of the future demand for food, substantial effort must be made to restore and maintain the productivity of their soils. If more food must be produced on the same amount of available land, agriculture must be intensified, and this will require that inputs to the soil be used as efficiently as possible (Henao and Baanante, 2006). This chapter examines technologies to restore and maintain the physi- cal structure of soils, improve the efficiency of water and nutrient use, and manipulate the rhizosphereâwhere plant roots interact with microbesâto enhance the soil and plant performance. It presents both some well-known methods for protecting and building soils that have not been widely ad- opted in SSA and SA but are essential for soil health and some novel, science-based concepts for improving soil that require research and ad- ditional exploration. Soil Degradation in Sub-Saharan Africa and South Asia The severe problems of soil degradation and desertification in SSA and SA are attributed to the long-term use of extractive farming practices that fail to rebuild the soil with organic material and mineral nutrients that maintain soil productivity and prevent erosion. The negative nutri- 145
146 Emerging Technologies to Benefit Farmers ent balance in soils of SSA (Henao and Baanante, 2006), underpinned by poverty, affects 95 million hectares of arable land that have reached such a state of degradation that only huge investments in soil restoration can make them productive again (IFDC, 2006). In densely populated SA, soil is often irrigated with polluted or contaminated water because of poor re- source management and competition for the resource. The overpumping of groundwater aquifers also has led to the deposit of salt on the land, which destroys soil productivity. Socioeconomic, political, and cultural factors reinforce conditions that affect soil quality. For example, the main source of fuel for household en- ergy in SA, other than fossil fuel, is wood, crop residues, and cattle manure (Venkataraman et al., 2005). The use of those traditional fuels has set in motion a cycle of natural resource degradation. Rather than being used as soil amendments, crop residues and manure are removed, and this has de- pleted the soil organic carbon (SOC) pool, created a negative nutrient bud- get, increased the susceptibility of soils to erosion, and reduced agronomic productivity. Runoff from soil leads to contamination and eutrophication of water resources, and the incomplete combustion of the biomass leads to emission of soot and noxious gases that have adverse effects on human health (Venkataraman et al., 2005). The degradation of the environment as a whole is a self-reinforcing system (Figure 5-1), and there is an urgent need to identify and foster technologies and management practices that can break the cycle of agrarian stagnation, enhance food security, and improve the environment. Restoring Soil Quality with Established Management Practices Soil provides the physical, chemical (including water), and biological environment for sustaining plant growth. There are strong interdepen- dences among soil characteristics, and maximizing the productivity of the soil requires attention to each of them. Because soils and the climatic and socioeconomic conditions in which they exist differ regionally, approaches to soil management are highly situational. There are many soil types in SSA and SA, from the highly erodible desert Aridisols and the easily compacted Alfisols to the less-permeable Vertisols (clayey soils with low infiltration rate and high susceptibility to erosion), and each has distinct needs and vulnerabilities. Some crops grow better than others in particular soil types, and the nutrient content of soils can vary widely. Nevertheless, successful soil management systems have several common objectives: to increase carbon content, enhance water infiltration, ensure the availability of water at the plant-root zone, reduce erosion, create a positive nutrient budget, and encourage beneficial organisms.
Technologies for Soil Improvement 147 FIGURE 5-1â Soil-degradation-induced poverty, starvation, and political, ethnic, and social unrest are linked. 5-1.eps SOURCE: Lal, 2007a. Reprinted with permission. bitmap image Established techniques used in various combinations to accomplish those objectives are summarized in Box 5-1. All the techniques have proven agronomic benefits, but for various reasons they have yet to be widely adopted in SSA and SA. Research has shown that the technologies can in- crease crop productivity and improve soil environments within 2 to 5 years (Lal, 1987, 2006a,b, 2007b, 2008; Kapkiyai et al., 1999; Sanchez, 2002; Wani et al., 2003; Singh et al., 2005; Smaling and Dixon, 2006; Rockstrom et al., 2007). The fundamental effects of the techniques in Box 5-1 are to improve soil structure, provide nutrients essential for plant growth, and maintain water availability in the soil. Improving Soil Structure with Established Practices A major benefit of the management approaches in Box 5-1 is that they can be used to restore and maintain optimal SOC for healthy soil structure and tilth. SOC provides energy for soil microbes and other fauna and flora;
148 Emerging Technologies to Benefit Farmers BOX 5-1 Established Management Practices to Maintain Soil Productivity To improve soil structure and biological health, reduce erosion, and increase efficiency of water and fertilizer use: â¢ Mulching with natural materials and plastic. â¢ Leaving crop residue. â¢ Application of manure and biosolids. â¢ Incorporation of cover crops in the rotation cycle. â¢ Agroforestry. â¢ Contouring of hedge rows. â¢ Terracing and engineering structures. â¢ Precision farming. â¢ Conservation tillage and nontilling. â¢ Controlled grazing. â¢ Improved pasture species. â¢ Controlled use of irrigation. â¢ Land-use planning and land-tenure reform. To improve soil nutrient budget: â¢ Integrated nutrient management. â¢ Biological nitrogen fixation. â¢ Judicious use of chemical fertilizers. enables the soil to hold water and nutrients; increases fertilizer-use efficiency by decreasing losses through erosion, volatilization, and leaching; and ulti- mately improves crop yield. The critical minimal SOC for the productivity of most soils of SSA and SA is 1.1 percent. Most agricultural soils of SSA and SA are severely depleted and have lost 75 to 85 percent of their original SOC pool. The concentration in degraded and desertified agricultural soils in SSA and SA is often as low as about 0.1 to 0.2 percent. SOC is highly correlated with productivity. Field experiments in SA have shown that the yield of mustard grain increased by 360 kg/ha for each ton of increase in the SOC pool in the surface soil layer (the top 15 cm) (Shankar et al., 2002). In central India, adoption of management practices to increase SOC in Vertisols increased crop yield from 1.0 t/ha per year to 4.7 t/ha per year (Wani et al., 2003).
Technologies for Soil Improvement 149 In Kenya, an 18-year study showed that maize and bean yields were in- creased from 1.4 t/ha per year to 6.0 t/ha per year when stover was returned to the soil as mulch, and fertilizer and manure were applied to increase the SOC pool from 23.6 t/ha to 28.7 t/ha in the surface layer (Kapkiyai et al., 1999). One estimate suggests that increasing the SOC pool in the agricul- tural soils of SSA and SA by 1 t/ha per year would increase total annual food grain production in SSA by 4.6 Â± 1.6 Ã 106 t and in SA by 18.6 Â± 7.1 Ã 106 t (Lal, 2006a,b). As noted earlier, management practices that rebuild SOC have not been widely applied throughout SSA and SA. Weak government institutions and extension, inadequate infrastructure, and resource-poor agricultural systems are barriers to the adoption of such practices. However, growing interest in carbon sequestration projects (Box 5-2) might provide an opportunity to improve SOC dramatically while increasing farmersâ income. Improving the Soil Nutrient Budget with Established Practices An important limiting factor in soils of SSA and SA is fertilization. Rice, wheat, and maizeâthe three major staple food cropsâcan require as much as about 100-200 kg of nitrogen-based fertilizer per hectare to pro- duce optimal yields under ideal moisture and temperature conditions. SSA and SA farmers typically are unable to afford such high rates of nitrogen fertilizer, and crop yields therefore are chronically low. Extractive farming practices are unsustainable, but adoption of man- agement practices listed in Box 5-1 can help to create a positive nutrient balance in the soil. Integrated nutrient management techniques consist of a combination of organic amendments, such as the use of manure and compost, and the judicious use of inorganic fertilizers (Vanlauwe and Giller, 2006). Those practices have to be implemented alongside those that build soil structure and carbon content (Lal, 1987, 2006a,b, 2007b, 2008; Kapkiyai et al., 1999; Sanchez, 2002; Wani et al., 2003; Singh et al., 2005; Smaling and Dixon, 2006; Rockstrom et al., 2007). As noted earlier, biofertilization accounts for about 65 percent of the nitrogen supply of crops worldwide, primarily via Rhizobiaceae-legume symbiosis (Lugtenberg et al., 2002). Although background concentrations of nitrogen fixation by free-living or endophytic bacteria are probably low (about 5 to 10 kg/ha), the bacteria produce bioavailable nitrogen at the root interface. The standard fertilization method of soil amendments is inefficient: only 40 to 60 percent of the nitrogen applied is taken up by plants, because it is lost through leaching or immobilized by soil microbes. Encouraging the growth of beneficial organisms in legume crop systems reduces the need for fertilizer.
150 Emerging Technologies to Benefit Farmers BOX 5-2 Carbon Sequestration: A Possible Opportunity for Resource-Limited Farmers Carbon sequestered in soils can be traded as a commodity in accord with the Clean Development Mechanism of the Kyoto Treaty, the BioCarbon Fund of the World Bank, the Chicago Climate Exchange, the European Climate Exchange, and national or domestic industry (Schlamadinger and Marland, 1998; Tucker, 2001; Diakoulaki et al., 2007). Although there are only a few projects to date in SSA and SA, carbon trading has the potential to bring a new income stream to resource-poor farmers (Kandlikar, 1996; Persson et al., 2006). Trading carbon credits implies payments to farmers of SSA and SA for environmental services through international industry and private and public sectors. With the adoption of the soil and crop management practices listed in Box 5-1, atmospheric carbon dioxide can be sequestered in agricultural soils. The rate of increase in soil organic carbon (SOC) after conversion to restor- ative land use follows a sigmoid curve and attains a maximum 5 to 20 years after adoption. Sequestration of carbon in agricultural soils worldwide has the potential to sequester 0.4 to 1.2 billion tons of carbon per year, or about 5 to 15 percent of global fossil fuel emission of carbon (Lal, 2004). Control of desertification and restoration of degraded soils have the potential to sequester an additional 0.9 to 1.9 billion tons per year (Lal, 2001). SOC sequestration in improved agricultural and restored ecosystems in SSA and SA ranges from 100 to 1,000 kg of carbon per hectare per year (Lal, 2000). Higher rates of SOC sequestration are observed in humid climates and in fine-textured soils, and lower rates in dry climates and in coarse-textured soils. Projects to sequester carbon in soils receive qualification to be used by world markets through independent validators. Involvement of diverse stakeholders in trading carbon credits has the potential to promote industryâs interest in this strategy (Johnson and Heinen, 2004) and to encourage development of a relevant climate policy for the region (Fouquet, 2003). Soil-Water Conservation with Established Practices Soil and water are closely linked in agricultural systems. Conserving water in the root zone and enhancing the efficiency of its use require that soil structure and quality be improved (Rockstrom et al., 2007). At the same time, the conservation of soil requires that it be protected from ero- sion by water and wind. The management practices listed in Box 5-1 can address both goals. In arid and semi-arid regions with low vegetation cover and crusted or compacted soils of low infiltration capacity, water runoff is high, especially
Technologies for Soil Improvement 151 in the monsoonal climate of SA, where rainfall is concentrated over short periods of 100 hours or 25 consecutive days (Agarwal, 2000; Biswas, 2001; Swaminathan, 2001). Runoff is a source of contamination and pollution of surface water and groundwater, and the leaching of chemicals from agricul- tural lands, especially in the intensively farmed areas of the Indo-Gangetic (IG) Basin, is a severe problem (Pachauri and Sridharan, 1999). Improving soil structure is the key to improving water infiltration into the soil. The maintenance and enhancement of soil organic matter, the use of biosolids or mulch, and conservation and no-till techniques are important strategies for improving soil structure. Mulching with biomass or plastic is also effective in reducing water losses by evaporation. Agroforestry, which is practiced to some degree in SSA and SA, has been shown to improve soil quality. However, trees growing in farmersâ fields may compete with crops, and there has been little success in adop- tion of such systems (Rhoades, 1997; Buresh and Tian, 1998). Recent research in the Sahel suggests that native shrubs are a previously unrecog- nized alternative that potentially can be used to enhance the fertility and quality of soils without such competition (Kizito et al., 2007). Piliostigma reticulatum and Guiera senegalensis play multiple roles in improving soil qualityâsuch as providing carbon to the soil (Lufafa et al., 2008), increas- ing nutrient availability in soil beneath and near the canopy (Dossa, 2007), and moving subsoil water to the surface (Caldwell et al., 1998; Kizito et al., 2009)âand have been shown experimentally to increase yields in peanut and millet by more than 50 percent (Dossa, 2007). Developing woody spe- cies companion plants has great potential throughout semi-arid SSA and SA to restore degraded landscapes, buffer desert encroachment, and increase crop productivity. However, alternatives for fuel are needed because these shrubs are cut and burned each year, and this constitutes a loss of organic inputs that the impoverished soils need. The efficient use of water will be critical in the future, not only because of its increasing scarcity (as described in Chapter 4) but because of its po- tential to bring salts into the soil that inhibit water uptake by crops and damage the physical structure of the soil. In parts of northwestern India, the problem of soil salinity was once associated mainly with a high ground- water table (waterlogging) that brought salt into the root zone through capillary action. More recently, overexploitation of groundwater has led to a decline in water tables, so farmers are forced to use poor-quality saline groundwater for irrigation that has led to high-sodium conditions that destroy the soil (Datta and De Jong, 2002). An important technology, which is gaining momentum in the IG Basin of SA and elsewhere, is the conversion of flooded rice paddies to aerobic rice. The latter, with specific varieties that can be grown as upland culture similar to wheat or corn, can save the scarce water resources and greatly
152 Emerging Technologies to Benefit Farmers improve water-use efficiency. Effective weed control measures are important for successful adoption of aerobic rice, but adoption of this technology would be directly relevant to the entire IG Basin and the 12.5 million hect- ares of area now under rice-wheat culture. Soil conservation and desertification control, which have high priority in SSA and SA, also can be effectively controlled by practices outlined in Box 5-1, including no-till or low-till farming with retention of crop residue mulch and incorporation of cover crops in the rotation cycle. To transition into no-till farming, appropriate seeding equipment and herbicides need to be available and affordable. The effectiveness of no-till farming can be en- hanced by integrating it with agroforestry, establishing contour hedge rows of perennial grasses or shrubs, establishing engineering techniques, and using complex crop rotations. Those measures improve ecosystem services of soil resources and increase crop yields. Vertisols can be effectively managed through adoption of the conservation-effective technology described above. The use of soil condi- tioners, such as mulch and biosolids, will result in improved soil structure and productivity. Zeolites and related materials, described in the next sec- tion, also have specific potential for improving Vertisols. NOVEL Technologies to Improve Soil Productivity The practices described in the preceding sections are considered estab- lished because their use has been studied extensively and their contributions to increased crop yields have been documented through research. However, understanding which combinations of practices work best in different envi- ronmental and social circumstances requires additional study and planning. Because that has not been done for most of SSA and SA, it presents an important opportunity and an unmet need for agricultural development. The increasing demand for food and changing land and water condi- tions have prompted scientists to search for new tools to build soil struc- ture, maximize the efficient use of water, and provide essential nitrogen and phosphorus to crops. Advances in plant, microbial, and computational biology; materials science; electronics; and optical sensing may provide new tools to improve soil productivity. Several technologies that are emerging from those fields of science are described below. Remote Sensing of Plant Physiology for Nutrient Management and Soil Quality More effective use of remote sensing technologies could enable farmers to better manage inputs to increase crop yields, decrease input costs, and reduce the potential for adverse environmental effects. If farmers could have access to remotely measured plant health and soil conditionsâsuch
Technologies for Soil Improvement 153 as water content, acidity, aeration, and the availability of nutrientsâthey could take appropriate steps to address soil quality before adverse effects occur. The low yields of cereal crops in SSA (about 1,000 kg/ha) could po- tentially be quadrupled by using sub-surface drip irrigation (mentioned in Chapter 4) and technology to manage fertilizer and nutrients. Remote sensing technology for nutrient management was initially based on the Normalized Difference Vegetative Index, which predicts plant cover (Stone et al., 1996). It was later used to document extensive variability between plants at distances 30 cm or less in production fields (Raun et al., 1998; 2001). The present technology is based on optical sensors with high spatial resolution that have the ability to predict yield potential midway through the growing season. It permits calculations of fertilizer rates based on projected nitrogen removal, and it permits adjustment of fertilizer rates as a result of conversion of organic to inorganic nitrogen (Johnson and Raun, 2003). Considering the extremely low rates of nitrogen application in SSA, improved nitrogen fertilizer practices, such as fertigation with drip ir- rigation, can enhance nutrient-use efficiency and substantially increase crop yields. Spectral data on plants and soils could be measured remotely and the information sent to farmers on cellular phones or other communication de- vices. Alternatively, a simple low-cost handheld âoptical pocket sensorâ and institutional support to deliver the data and education about management practices to farmers in SSA and SA could be developed. As discussed in Chapter 2, the use of hyperspectral imaging can coupled with the develop- ment of sentinel species able to emit specific stress signals that are detectable remotely or locally would assist farmersâ management practices. Zeolites and Synthesized Nanomaterials Zeolites, members of a family of crystalline aluminum silicates that consist of a unique tetrahedral frame within which sit large ions or other molecules, have multiple applications in soil and water conservation (To- kano and Bish, 2005). Natural deposits of zeolites occur throughout the world, but they can also be synthesized and tailored for specific uses. The utility of zeolites is derived from their unique flexible internal structures that permit the exchange of ions and reversible dehydration (Watanabe et al., 2004). Because they absorb and slowly release water, zeolites can be used as a soil amendment to improve water retention in sandy and low-clay soils and to improve porosity of impermeable soils. They could be used to conserve water in the root zone in conjunction with traditional techniques, such as mulch farming and application of manure (Bhattacharyya et al., 2006; Pal et al., 2006; Oren and Kaya, 2006). When pretreated with nutrients, zeolites can be used as an agent for the slow release of nitrogen and phosphorus. They can also be used to enhance the availability of micronutrients, such as zinc (Oren and Kaya,
154 Emerging Technologies to Benefit Farmers 2006). Alternatively, zeolites can be used in soil remediation to absorb metal cations and reduce local concentrations of toxic substances that in- hibit plant growth and nitrogen-fixing soil microbes (Pisarovic et al., 2003). The potential diversity and multiple uses of zeolites make them ripe for further research and development. Changing the structure of the molecular framework, the internal cations, and guest molecules can change the char- acteristics of the zeolite and its effectiveness in a particular application. The dimensionality and size of zeolite pores also define many of its properties. Advances in nanotechnology suggest that it is possible to engineer zeo- lites further or develop similar materials with precisely determined proper- ties. One opportunity is to increase the efficiency of fertilizer by developing slow-release delivery molecules that decrease losses to water and air and increase uptake by plants. A second potential application of nanotechnology is as a soil sur- face conditioner that enhances soil structural stability, reduces erosion, and dissipates heat. In many of the countries in SSA and SA, heat stress on crops intersects with other abiotic and biotic stresses to reduce yield (Senthil-Kumar et al., 2007). High-soil temperatures exacerbate the stress of drought and point to a possible point of intervention (Mittler, 2006). Use of innovative technology for conserving water in the soil is a promising option to address heat and drought (Kijne, 2001). In addition, when dry Vertisols are rapidly exposed to water, they re- lease a large amount of heat at the soil surface, which causes slaking of soil aggregates that reduces the ability of water to percolate downward and re- sults in water runoff. Although no current method addresses this problem, it is conceivable that materials could be developed to interrupt the process by improving the biophysical stability of soil aggregates and dissipating the heat emitted during wetting. A third application of nanomaterials is to improve the quality of irriga- tion water. Zeolites have been used in some parts of the world to remove some contaminants from water, but nanoparticle filters of ceramics, carbon, and zinc oxides that effectively remove contaminantsâincluding viruses, bacteria, lead, arsenic, uranium, and pesticidesâare now being produced. Inexpensive applications are needed to remove those contaminants and oth- ers, such as sodium and salts, from irrigation water. Further development of this technology has the potential to reduce a major health burden and improve soils in rural communities in SSA and SA. The application of nanomaterials and zeolites, particularly the synthetic types, on an entire farm is prohibitive for resource-poor farmers of SSA and SA, so finding ways to bring the cost down would be essential. However, at their current price, they would be appropriate for specific niches, such as in screenhouses and greenhouses for production of vegetables or horticultural crops to supply large urban centers.
Technologies for Soil Improvement 155 New Cultivars, Plant Breeding, and Biotechnology The productivity associated with soil, water, and nutrients depends in part on the requirements of the crops they support. The tools of modern plant breeding and biotechnology, described in greater detail in Chapter 3, offer the hope that crops can be developed to better tolerate specific soil- related constraints. Genes that provide some degree of tolerance of cold, drought, salinity, aluminum and manganese toxicity, anaerobiosis, and low nutrient conditions are being widely investigated (Fageria and Balizar, 2005; Chinnusamy et al., 2006; Eicher et al., 2006; Umezawa et al., 2006; Sunkar et al., 2007). Because drought is a prevailing concern, improving the water-use ef- ficiency of crops (biomass produced per unit of water transpired) is of particular interest. Breeding for early flowering and developing crops that can be planted at a higher density to minimize soil-water evaporation are two strategies to cope with water deficits. Sowing such crops as sorghum and millet in clumps can increase water-use efficiency and improve yields (Bandaru et al., 2006). Developing new varieties of aerobic rice to shift the rice-wheat-based cropping systems of the IG Basin away from flooded rice paddies would save massive amounts of groundwater and improve soil, although new ways to control weeds would be needed (Peng et al., 2006). Two additional opportunities at the interface of soil and plants are discussed below. Development of Better Roots Current research suggests that it is possible to optimize root structure for various purposes, including increased carbon sequestration, improved grain yields, and better water and nutrient uptake. High-resolution root expression mapping (Birnbaum et al., 2003, 2005; Brady et al., 2007) and root architecture imaging and analysis have potential to enhance or select for desirable root traits, such as rapid and early shallow root emergence, diffuse and extensive root architecture and root hairs, and long tap roots (Philip Benfey, Duke University, presentation to committee, October 15, 2007). It may be possible to develop improved cultivars with a favorable root:shoot ratio and improved harvest index, which favors both grain and biomass production. Development of Transgenic Nitrogen Fixation in Non-legumes As noted earlier, biofertilization accounts for about 65 percent of the nitrogen supply of crops worldwide, primarily through Rhizobiaceae- legume symbiosis, in which Rhizobium bacteria fix atmospheric nitrogen and deliver it to plants via nodules on roots (Lugtenberg et al., 2002).
156 Emerging Technologies to Benefit Farmers Extending that relationship to non-legume crops would be a major step forward in plant science and would be transformative for farmers in SSA and SA. There are two potential approaches to engineering nitrogen fixation in non-legume plants. The first involves altering the plants to enable infection by rhizobia, which results in nitrogen-fixing nodules (Jones et al., 2007). Accomplishing that would require a nearly complete understanding of the Rhizobium-legume symbiosisâa complex process of signaling between the plant and bacterium partners at every stage of interaction from attraction and attachment to invasion and colonization. Dozens of bacterial genes would be required to develop non-legume Rhizobium nodulating crops, and this would entail mimicking millions of years of evolution (Eric Triplett, University of Florida, presentation to committee, October 15, 2007). An alternative approach is to transform plants with nitrogen-fixation (nif) genes; this does not require a symbiotic relationship with a microor- ganism. Establishing N2-fixation in cereals and other non-legumes would require a whole complex biochemistry to support active nitrogenase, includ- ing oxygen protection. Three nitrogenases are well known, and some bacte- ria have all three. It may be possible to express the bacterial KpnifH gene in plant chloroplasts (Cheng et al., 2005). Alternatively, it could be transferred to the mitochondria (Frazzon et al., 2007). Overall, this procedure could be difficult in that at least 10 genes would have to be inserted into plants to transform nif genes into organelles (mitochondria or chloroplasts), but it might be possible if approached in an organized way (Eric Triplett, Uni- versity of Florida, presentation to committee, October 15, 2007). Possible approaches could be direct transformation of organelles and the nuclear transformation of genes that possess the appropriate upstream target se- quence to ensure organelle localization of the resulting protein (Remacle et al., 2006; Liu et al., 2007). There may be pathways to fixing nitrogen other than those most famil- iar to the scientific community. Ortwin Meyer at the UniversitÃ¤t Bayreuth found that Streptomyces thermoautotrophicus isolated from a burning charcoal pile could fix nitrogen (Gadkari et al., 1992). The organism grows aerobically at 65Â°C with N2 as a sole nitrogen source and CO or CO2 + H2 as a sole carbon source, and it contains no genes with homology to traditional nif genes (Ribbe et al., 1997). There has been no follow-up of this work for 10 years, but the results suggest that simpler nitrogen-fixing systems that exist in nature could be used by plants (Eric Triplett, University of Florida, presentation to committee, October 15, 2007). Potential concerns about transgenic plants and microbes include con- trol over insertion sites for introduced DNA sequences as they affect the plant genome and mutagenesis, linkage of favorable genes to genes that could confer resistance to an antibiotic or a herbicide, insertion of unde- sired bacterial plasmid sequences, and gene flow from transgenic plants to
Technologies for Soil Improvement 157 nontransgenic crops or wild plants (Rosellini and Veronesi, 2007). How- ever, with adequate foresight embedded in research plans to consider out- comes for control mechanisms of transgenes, modifications of the genome should be minimal and completely known, so unexpected effects could be avoided (Rosellini and Veronesi, 2007). Manipulating Microorganisms in the Rhizosphere The rhizosphere is a diverse, highly competitive, and complex ecologi- cal environment for microorganisms. It encompasses intracellular root tis- sue, root surfaces, and the surrounding soil that is influenced by the root, including the physical structure of aggregates and pore space and within the intestines of soil animals. On plants or soil surfaces, microbes exist in thin water films and biofilms, occupying a small (1 to 5 percent) portion of the total soil space where environmental conditions are sufficient to support microbial life. The rhizosphere is biologically and chemically different from bulk soil and very more important in determining the effects of plant patho- gens, plant growth-promoting microbes, and biogeochemical processes that together strongly affect the yield and quality of crops. We now know that soil microbes exhibit highly regulated cell-to-cell communication by using signaling compounds to monitor their surround- ings and alter their activities, and plants are also involved in these signaling mechanisms. Knowledge of quorum sensing compounds that induce a wide array of physiological responses in soil bacteria has dramatically advanced (Lithgow et al., 2000; Fray, 2002). In addition, much is now known about the importance of root exudates as sources of nutrients and carbon that promote and sustain organisms. Roots exude ions, free oxygen and water, extracellular enzymes, mucilage, and a wide assortment of primary and secondary metabolites with various functions, most of them unknown (Bertin et al., 2003; Uren, 2007). The exudates are low-molecular weight compounds such as amino acids, sugars, organic acids, phenolics, and other secondary metabolites, and they include less diverse high-molecular weight polysaccharides and proteins. Plants expend considerable energy and re- lease a substantial amount of carbon material through exudation, which can include more than 30 percent of the energy captured by photosynthesis (Morgan and Whipps, 2001). Root exudates and leachates affect microbial communities in two main ways: they provide rich and relatively readily available sources of energy and nutrients to microbes, and growing evidence suggests that chemical signals between plant roots and microbes influence community structure and functions. Those effects create a functionally complex community with a high level of competition for colonization by bacteria and fungi that may be beneficial, neutral, or pathogenic to plants. In the last 10 years, research has increasingly indicated the feasibility
158 Emerging Technologies to Benefit Farmers of manipulating soil microorganisms to reduce the need for off-farm in- puts and to stimulate plant growth. This section describes novel strategies for plant protection, disease suppression, plant growth stimulation, and enhanced plant nutrition that have exciting potential for agriculture. To de- velop those strategies as technologies, it is imperative to have a better basic understanding of microbial ecology in major crop systems of SSA and SA. Phytostimulators A diverse array of bacteria and some fungi that can produce substances that promote plant growth and increase crop yields have been identified (Chen et al., 1994; Amara and Dahdoh, 1997; Biswas et al., 2000a,b; Hilali et al., 2001; Asghar et al., 2002; Khalid et al., 2004; Larkin, 2008). Many of the substances include phytohormones such as auxin, cytokinins, indole-3-acetic acid, and gibberellin, which are known to play various roles in root and leaf development and plant response to environmental stimuli, such as light and gravity (Hagen, 1990; Steenhoudt and Vanderleyden, 2000; Garcia de Salamone et al., 2001). Some organisms stimulate plant growth in other ways, for example, by enzymatically removing ethylene, a natural byproduct of plant metabolism that retards root growth, from the soil; Pseudomonas spp. accomplishes this with 1-aminocyclopropane-1- carboxylate (ACC) deaminase that hydrolyzes the ethylene precursor ACC (Penrose and Glick, 2001). Why rhizobacteria have evolved to produce phytohormones is not known. It may be that they stimulate greater production of root exudates and increase root development that provides enhanced nutritional benefits and space for microbial colonization, giving microbes with phytostimulat- ing properties an evolutionary advantage. Although the mechanisms of the relationship of rhizobacteria to plants are not yet well understood, the use of rhizosphere microbes that stimulate plant growth presents a promising opportunity to increase crop yields (Broughton et al., 2003). Inoculation of different crop types with various organisms has demonstrated measurable yield or growth increases (Box 5-3). Commercially available biological inoculation technologies have been developed and are available in industrialized countries, but the scientific underpinning of most of them is limited. Local environmental or agronomic conditions apparently influence the effectiveness of the organisms in in- creasing crop yields, and this variability needs to be investigated more thor- oughly (Larkin, 2008). For example, a strain of Bradyrhizobium japonicum that was inoculated on soybeans was found to grow best (and to increase soybean protein content) under cooler soil conditions (Zhang et al., 2002). Although yield increases can be demonstrated, the magnitude varies widely, in part because these microorganisms operate in complex microbial com-
Technologies for Soil Improvement 159 BOX 5-3 Examples of Organisms Inoculated onto Crop Roots That Increased Yield or Growth â¢ zospirillum on various crops. A â¢ hizobium leguminosarum on rice and wheat (only in presence of nitrogen R fertilizer) (Biwas et al., 2000a). â¢ seudomonas on potato (Kloepper et al., 1980). P â¢ acillus spp., producing various gibberellins, on alder (Gutierrez Munero et al., B 2001). â¢ seudomonas fluorescens strain on radish (Leeman et al., 1995). P â¢ acillus licheniformis on Pinus pinea L. seedlings (Probanza, 2002). B munities and can themselves have multiple effects on plants; for example Azospirillum produces phytohormones but can also fix nitrogen (Okon and Labandera-Gonzalez, 1994). The prospect of using soil microorganisms to boost crop growth is ex- citing, but substantial research is required to fully develop phytostimulating microbial systems. Research at all levels, from ecology to proteomics and metabolomics, will be needed to increase the predictability of outcomes. Disease-Suppressive Soils Over the last 15 years, there have been surprising discoveries of soil microbial communities that are able to protect plants and suppress plant pathogens. Intensive studies of disease-suppressive soils have led to the development of new methods of analysis and insights into the nature of soilborne disease suppression (Hoitink and Boehm, 1999; Weller et al., 2002; Bolwerk et al., 2005; Benitez et al., 2007; Borneman and Becker, 2007; Gross et al., 2007). Such advances indicate that it is possible to man- age soil microbial communities to suppress soilborne diseases and improve crop productivity (Mazzola, 2004). Generally speaking, there are three ways to manage crop-associated microbial communities actively. The first is to develop disease-suppressive soils through manipulation of carbon inputs. This involves adjusting the types and timing of organic inputs, for example, by using cover crops, ani- mal manures, and composts. Such approaches have been shown to provide site-specific reductions in disease and pest incidence (Abassi et al., 2002; Widmer et al., 2002; Stone et al., 2003; Rotenberg et al., 2005; Cespedes-
160 Emerging Technologies to Benefit Farmers Leon et al., 2006; Darby et al., 2006; Larkin, 2008). Some soils in Africa can be induced to cause high seed mortality in the pernicious weed Striga by adding organic matter and mineral nitrogen (GhÃ¨hounou et al., 1996; Ransom et al., 2000). The advantage is that primarily locally available resources can be used to maximize soil health in a sustainable way. The disadvantage is that outcomes vary with soil type, and a better understand- ing of the combinations of soil and locally available amendments that work well together is needed. The second way involves crop sequencing (Cook, 2006). This has proven effective for the control of âtake allâ disease in wheat, which is caused by the soilborne fungus Gaeumannomyces graminis var. tritici. In this case, disease control is mediated by the buildup in the rhizosphere where certain genotypes of Pseudomonas fluorescens have the ability to produce the antibiotic 2-4-diacylphloroglucinol that is inhibitory to the pathogen. This shift in the microbial make-up of the soil, and more spe- cifically the wheat rhizosphere, accounts for the well-documented take-all decline whereby the soil changes from microbiologically conducive to take- all to suppressive following one or more outbreaks of disease and with consecutive crops of wheat. The third approach uses inoculation of disease-suppressive microbes into the soil or the more common method of inoculation with seeds or other planting material. All soils harbor detectable populations of disease- suppressive organisms, but the diversity, relative abundance, and activities of the organisms can vary substantially from site to site. Molecular tools now allow us to identify microbes that are suppressive in situ and to re- cover them in a directed fashion (Borneman and Becker, 2007). Such an approach has already proved useful in collecting indigenous fungi that acted as effective inoculants to suppress soilborne diseases caused by nematodes (Olatinwo et al., 2006). Control of Fusarium wilt of watermelon with nonpathogenic strains of F. oxysporum is explained by induced systemic resistance to the patho- genic strains (Alabouvette et al., 2007). Effective âimmunizationâ of this sort will more broadly require considerable research; in one model, the interaction between maize and Trichoderma harzianum strain T22 in- duces systemic resistance, increases growth responses and yields, and in- creases nutrient uptake and fertilizer-use efficiency (Harman and Shoresh, 2007). Analyses of the genetics and genomics of disease-suppressive microbes have led to new methods to isolate the microbes in a directed fashion from any location (Bangera and Thomashow, 1999; McSpadden Gardener et al., 2001; Koumoutsi et al., 2004; Joshi et al., 2006; Paulsen et al., 2005) and to the development of effective and inexpensive inoculants (McSpadden Gardener et al., 2005).
Technologies for Soil Improvement 161 A non-aflatoxigenic strain (AF36) of Aspergillus flavus has been iden- tified, and its application to cotton plants early in the growing season effectively displaced strains that produce aflatoxin and consequently led to a large reduction of aflatoxin in bolls (Cotty, 1994). A commercial competitive exclusion product called Afla-guardÂ® has been used success- fully to lower aflatoxin concentrations in peanut (Dorner and Lamb, 2006) and will be tested on pistachio in 2008. Non-aflatoxigenic strains have not yet been commercialized for maize, but a recent study applied toxin- producing and non-toxin-producing types of Aspergillus to soil in Nigeria, and the non-toxin-producing type spread to maize growing in the field and reduced aflatoxin concentrations by up to 99.8 percent (Bandyopadhyay et al., 2005). This work needs scaling up to test the efficacy of the strains in a larger scale across Nigeria and to develop an Africa-wide aflatoxin biocontrol program. Considerable progress has been made in identifying specific organisms and managing organic inputs to suppress diseases or to protect plants from infection in developed countries. Given the regionality of crop systems and the disease pressures, such new tools would be valuable for developing inoculants for commercial use in SSA and SA. Little such work has been done on their soils, and research on them is an opportunity to contribute to environmentally sustainable systems that reduce the need for pesticides. Biological Nitrogen Fixation The single most important factor in soils in SSA and SA is adequate fertilization. Most farmers cannot afford or do not have access to com- mercial fertilizers. Despite its dominance in the atmosphere, nitrogen is universally the most limiting crop nutrient because plants cannot transform atmospheric nitrogen into biologically active molecules. Diazotrophs are bacteria that are able to capture atmospheric nitrogen and transform it into molecules that are usable by plants. Some species live freely in the soil; others are endophytes, living in plant roots and obtaining energy from plants (An et al., 2001). The most well-studied relationship is that of the bacterial species Rhizobium with legumes. Although further basic research on this symbiotic relationship may result in a means of providing more nitrogen for agricultural systems, the increases are likely to be incremental. However, the use of legumes in agriculture as sources of nitrogen fertilizer could be expanded with regional applied research. There has long been interest in developing systems of biological ni- trogen fixation for non-legume crops, such as rice, wheat, sorghum, and millet. A wide array of root endophytic bacteria that can fix nitrogen have been identified (Box 5-4). Inoculating maize, sorghum, and wheat with Azospirillum has been shown to increase yields by as much as 30 percent,
162 Emerging Technologies to Benefit Farmers BOX 5-4 Genera of Root Endophytic Bacteria That Can Fix Nitrogen Burkholderia, Gluconacetobacter, Herbaspirillum, Azoarcus. Acetobacter, Arthro- bacter, Azospirillum, Azotobacter, Bacillus, Beijerinckia, Derxia, Enterobacter, Herbaspirillum, Klebsiella, Pseudomonas, Stenotrophomonas, and Zoogloea. SOURCES: Barraquio et al., 2000; James et al., 2000; Lodewyckx et al., 2002. but more research is needed to ascertain whether the yield increases are due to nitrogen fixation or to other mechanisms, such as the production of phytohormones (Dobbelaere et al., 2001). If successful, the technology could dramatically increase grain productivity in SSA and SA while reduc- ing the need for synthetic fertilizer. Typically, the largest plant response to diazotrophic bacteria has been in degraded soils and water-stressed regions when low or intermediate concentrations of fertilizer were applied (Dobbelacre et al., 2001). That is encouraging for SSA and SA farmers because those are the kinds of soils and conditions they regularly encounter. The most notable example for practical use of biological nitrogen fixation is sugarcane, in which 60 to 70 percent of the nitrogen comes from endophytic bacteria (Boddey et al., 1995). Studies on rice have shown that up to about 30 to 40 percent of the nitrogen uptake can be attributed to three diazotrophic species (Hurek et al., 2002). It should be pointed out that field level measurement of N2 fixation is difficult to definitively quantify. However, greenhouse studies that utilize the 15N dilution method to provide a full accounting of the N inputs have shown the potential of free-living N-fixing microorganisms to provide nitrogen to plants (Iniguez et al., 2004). That study demonstrated that up to 44 percent of the nitrogen taken up by wheat came from the fixed nitrogen of a bacteria Klebsiella pneumoniae 342. Iniguez and colleagues (2004) showed that (1) total nitrogen uptake was significantly greater than uninoculated or inoculated nifH K. pneumoniae mutant (genetically identical except unable to fix nitrogen) controls; (2) nitrogenase activity of K. pneumoniae 342 was occurring in wheat roots and not in the presence of the mutant strain; (3) fixed nitrogen was found in chlorophyll; and (4) Kochâs postulates were fulfilled (inoculum strain 342 was recovered from the host plant). To develop the technology, much more needs to be known about which physiological plant responses to endophytic diazotrophs will enhance ni-
Technologies for Soil Improvement 163 trogen fixation. The role of phytohormones, some of which encourage the development of root nodules where diazotrophic bacteria colonize, is not yet understood (Vessey, 2003). The energy and nutritional signaling require- ments needed to stimulate nitrogen-fixing bacteria must also be elucidated. It may be that considerably more carbon (as an energy source) is needed than is currently produced in modern non-legume crop rhizospheres. For example, legumes can fix agronomically significant levels of nitrogen but do so by using over 30 percent of the photosynthesate produced by the host plant. More work is also needed on the role of plant defenses in regulating endophytic colonization. Most of the work done to date has been in Arabi- dopsis but not in crop plants (Iniguez et al., 2005). Research is needed on the mechanisms of endophytic colonization relative to root characteristics and soil conditions that would enable beneficial bacteria to thrive and elude plant defenses. It is worth noting that modern crop breeding programs have typically developed crops under high nitrogen levels that emphasize above-ground yield without considering the rhizosphere. It may well be that those programs selected against rhizospheres that promote nitrogen- fixing microorganisms and against colonization of beneficial endophytic bacteria. Thus, plant scientists and microbiologists need to work in concert to develop truly effective rhizospheres of non-legume crop systems that can encourage nitrogen-fixing bacteria to optimize yields. Microbial Enhancement of Phosphorus Uptake by Crops In addition to nitrogen, phosphorus is an important nutrient for SSA and SA farmers. Many soils in the region have inherently low phospho- rus concentrations that are reduced by crop harvesting and soil erosion (Tiessen, 2005). Unlike nitrogen deficiency that can potentially be corrected by biological fixation, phosphorus deficiencies must be corrected both by adding phosphorus sources to soils and by increasing the efficiency of phos- phorus uptake by plants. It should be noted that fertilizer is inefficient in delivering bioavail- able phosphorus to plants, because it becomes rapidly âfixedâ in plant- unavailable soil fractions (Sanyal and De Datta, 1991). The strong chemical reactivity of phosphorus results in very low plant recovery, typically 10 to 20 percent of the phosphorus applied to soils (McLaughlin et al., 1988; Holford, 1997). Moreover, the global annual consumption of phosphorus- based fertilizers exceeds 30 million tonnes, and it is expected that the worldâs known reserves of high-quality rock phosphate will be consumed within the next 80 years (Isherwood, 2000; IFIA, 2001). Some bacteria (Pseudomonas spp. and Bacillus spp.) and fungi (most notably mycorrhizae but also Aspergillus and Penicillium) have been shown
164 Emerging Technologies to Benefit Farmers to enhance the availability of phosphorus to plants naturally through bio- chemical mechanisms such as solubilizing inorganic phosphorus by chela- tion or acidification (by production of organic acids, carbonic acid, or H+), mineralizing organic phosphorus by producing extracellular phosphatases or phytases, and increasing root growth or root-hair development by pro- ducing phytohormones (Jakobsen et al., 2005). Many studies have improved phosphorus nutrition and yield in a wide variety of crops by inoculating phosphorus-enhancing microorganism (Whitelaw, 2000; Leggettt et al., 2001; Jakobsen et al., 2005). Besides the expected response to phosphorus-deficient soils, studies have shown im- provement with phosphorus-enhancing microorganisms in the presence of rock phosphate (Barea et al., 2002). The latter is important for SSA and SA farms, where indigenous sources of rock phosphate could be used directly without manufacturing commercial phosphorus fertilizer. In addition, in high-phosphorus-fixing soils, rock phosphate can have longer residual ef- fects that last several years on acid soils (Sahrawat et al., 2001). Endomycorrhizae form arbuscular structures in close association with host cells of almost all annual crops. Ectomycorrhizae form associations with many woody plants, and their interactions with timber species are well studied. A plant provides carbohydrates to a fungus; in turn, the fungus develops an extensive hyphal network that can transport phosphorus and other nutrients to the plant (Smith and Read, 1997). That greatly increases the volume of soil that the plant can explore; in addition, mycorrhizae can mobilize phosphorus by excreting phosphatases and organic acids (Whitelaw, 2000). It should also be noted that co-inoculation of plants with mycorrhizal fungi and phosphate-solubilizing or -mineralizing microorgan- isms (so-called helper microorganismsâmany of the same ones mentioned above) can further increase the plant response to phosphorus and therefore the effectiveness of mycorrhizal fungi (see review by Jakobsen et al., 2005). It is relevant to this nutrient exchange that the mycorrhizal plants tend to resist drought and infection by soilborne pathogens. Direct exploitation of microbial processes to increase phosphorus up- take by crops has had little success so far, but if more information about the relationship between crops and these organisms is uncovered, the basis of a future technology to dramatically increase fertilizer efficiency may be recognized (Jakobson et al., 2005). Ultimately, the development of effective, low-cost, and simple inoculation strategies could help farmers to overcome phosphorus shortages in their soils. Agriculture might be transformed if we can combine knowledge of the microbial ecology of phosphorus-enhancing microorganisms with plant breeding or insertion of transgenes to develop roots with architectures, exudates, and signaling that optimize root and microbial responses to increase phosphorus uptake by crops.
Technologies for Soil Improvement 165 Microbe-Enhanced Drought Tolerance Bacterial species that can enhance the ability of plants to withstand water stress by increasing seedling root elongationâwhich promotes stand establishment and various other crop physiological responses, such as re- ductions in cell elasticity and osmotic potential and a rise in root cell water fractionsâhave been isolated (Alvarez et al., 1996; Creus et al., 1998). Co-inoculation of autochthonous arbuscular mycorrhizae and Bacillus thuringiensis has been shown to increase plant resistance to water stress because it reduces the amount of water required to produce shoot biomass (Marulanda et al., 2007). The findings suggest that the root microbial com- munity could be manipulated to improve the drought tolerance of plants, but research in this field is in its infancy. Various experiments with sorghum inoculated with Azospirillumâ which resulted in a larger root system, increased leaf water potential, lowered canopy temperatures, and increased stomatal conductance and transpirationâalso suggest the potential of the approach (Sarig et al., 1988; Fallik et al., 1994). Inoculated sorghum also had 15 percent greater total water extraction from soil than the noninoculated controls and obtained water from deeper soil layers than the controls. Similarly, Hamaoui et al. (2001) showed that inoculation of sorghum with Azospirillum brasilense significantly reduced the adverse effects of saline irrigation water because of stimulation of root development, delayed leaf senescence, and improved water uptake in saline soils (Sarig et al., 1990). Microbial-induced drought resistance is a potentially important tech- nology for SSA and SA farmers because large parts of the target region are semi-arid and crops regularly experience drought stress. However, research on the interactions of microbes with plants and the relationship of the interactions to drought resistance is in its infancy, and there is virtually no such research in SSA and SA. Research Considerations in Manipulating Microorganisms in the Rhizosphere Although a general understanding of root exudates and their overall importance relative to plant nutrition, pathogen responses, and benefi- cial microbial interactions has been established, the role and magnitude of chemical signaling of root to root, root to microbe or invertebrate, and microbe or invertebrate to root are just beginning to be understood (Uren, 2007). At this stage, what is done about these interactions is pro- vocative and offers exciting potential for their future use in agricultural technologies. Box 5-5 shows some of the fundamental information and resources
166 Emerging Technologies to Benefit Farmers BOX 5-5 Major Research and Technology Needs for Manipulating Microbes in the Rhizosphere â¢ icrobial genome sequencing and functional genomics of plant-associated M microbes that are important in the agriculture of sub-Saharan Africa and South Asia. â¢ iscovery of the genes that control microbial-plant signaling, biofilm forma- D tion, interspecies interactions, production of plant-growth-promoting sub- stances, nutrient uptake enhancement, plant protection, and the structures of multi-species microbial communities. â¢ asic multidisciplinary research on microbial ecology of microbial-plant inter- B actions that optimize growth of crops. needed to bring the manipulation of the rhizosphere to reality. Given the diversity and complexity of microbial communities and, until recently, the lack of tools to study them, the task requires a major interdisciplinary initiative. In that regard, it is worth pointing out that there is currently a distinct lack of interaction between microbiologists and plant scientists, and this has held back the field of rhizosphere science. The emphasis of plant sciences has been on breeding and developing plants for optimal yield and resistance to disease, pests, and environmental stresses. There has been little research on developing plants to promote interactions with beneficial microbes or to optimize the crop rhizosphere. To benefit farmers in SSA and SA, research should focus on local crops and local soil communities. Teams of soil and rhizosphere microbial ecologists, geneticists, molecular biolo- gists, plant physiologists, plant breeders, agronomists, and anthropologists need to be assembled in an integrative project to conduct multidisciplinary research on the major crops of the regions. As research proceeds, it will be important to put it into a regional and farm-level crop system context. To emphasize that, we present one example related to manipulation of biocontrol microbes. Larkin (2008) compared various biostimulants and known microbial control agents of potato dis- eases. All had measurable effects on soil microbial properties in the field, but none reduced disease in continuous potato plots; rather, effective con- trols occurred only in particular crop rotations. The results indicate that some rotations are better able to support the added beneficial organisms and amendments that enable more effective biocontrol of disease. Estab- lishment and persistence of microbial inoculants, soil amendments, and engineered rhizospheres probably depend on many soil and climate factors.
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