A review of work on rhizosphere microbiota in Uganda
The rhizosphere is broadly defined as the soil volume under the influence of plant roots, enriched with exudates, secretions and mucilaginous materials. It supports an active microbial population distinctive from the bulk soil. Subsequently, there are many interactions between plant-microflora, plant-macro-fauna, microflora–macrofauna and soil-plant-microflora. Some relationships are positive and others parasitic. Significant among the beneficial ones are symbioses between leguminous plant species and legume nodule bacteria and mycorrhizal association occurring widely among plants. The former has been extensively studied and substantial gain made in harnessing biologically fixed nitrogen. Mycorrhizal investigations are still inadequate, especially production of commercial inoculants. Similarly, plant disease and their causative agents raise great concern hence a lot of work has been done. There other benefits that have not been well tapped like production of growth promoting substances and bio-control agents. Despite the evident importance of the rhizosphere there are no specific citations of deliberate studies on its micro-biota in Uganda. Therefore there is urgent need for research to determine, the abundance, diversity and distribution of rhizosphere biota, their impact on natural and agro-ecosystem functioning. The studies should also document indigenous knowledge, impact of current policies and build physical and human capacities to handle current and future challenges.
The ecto- and endo-rhizosphere demarcate volumes of soil adjacent to and influenced by plant roots. While the former is the distinct boundary between the root surface and soil; the latter represents the cortical region invaded and colonized by microorganisms. The rhizosphere involved active bacterial growth around plant roots (Hiltner, 1904) quoted by Paul & Clark (1996). Apparently, the roots influence a large bulk of soil. For instance, a single wheat plant may be several meters long (Bolton, Frederickson & Elliott, 1993). Furthermore, the rhizosphere is highly complex because of the numerous interactions existing between microbes and microbes, microbe and plants, microbes and fauna, fauna and plant and plant and soil.
Some of the above interactions are symbiotic as exemplified by legumes and rhizobia and mycorrhizal plants. Equally common are pathogenic relationships as many fungi, bacteria and nematodes attack plants (Alexander, 1961). Other interactions e.g. commensalisms and proto co-operation between the plant and its rhizosphere inhabitants also exist. In the subterranean partnership, the higher organisms contribute excretory products and sloughed off tissue while the dominant underground flora hardly affects the host plant. Nonetheless, most of the benefits are derived from the microscopic populations. Gram negative bacteria mainly in genera Pseudomonas and Acetobacter, plus denitrifiers dominated the rhizosphere microbiota whereas Gram positive or variable e.g. Bacillus, and Arthrobacter are few (Paul & Clark, 1996). Likewise, populations of micro biota and root grazers drastically rise.
The microbiota and the host plants influence one another thus demanding integrated management strategies; whereby both plant disease control and nutrient uptake, could be employed in agro-natural ecosystems to improve productivity.
Rhizosphere in agricultural systems
Comparison of rhizobiota in agricultural system: effects of conversion from natural to agricultural systems
In natural ecosystems, there are many more plant species than in agricultural systems. Yet, plant exudates, secretions and mucilage contributions greatly influence the rhizosphere biota. For example, oat and pea roots excreted 14 and 22 amino acids respectively while both exuded fructose and glucose (Bolton et al., 1993). Possibly, the natural system has a greater number and diversity of rhizosphere organisms compared with agricultural systems with reduced plant species becoming more pronounced in mono-cropping systems.
In Uganda, rhizosphere biota studies have mainly concentrated on legume nodule bacteria (Stephens, 1967; Stobbs, 1969; Silver, 1976, Rwakaikara-Silver & Alumai, 1999) and plant pathogens (Hansford, 1937; Alemu, 1966). There is no documented research in Uganda about actinorrhizal, and few unpublished studies on arbuscular mycorrhizal associations; yet, these are important topics needing investigation.
Nkwiine & Rwakaikara- Silver (in the same review) elaborate on the gaps that must be addressed to maximize benefits accruing from symbiotic plant–microbe relations. Similarly, Ssekamatte & Okwakol elsewhere in this issue report on pathogens and their control methods. Exploration of other rhizosphere nonparasitic nonsymbiotic organisms is necessary. There is renewed interest in biocontrol of plant pathogens and currently Trichoderma species are being tested for virulence against bean root-rot pathogens.
Rhizosphere biota under differing ecosystems particularly natural versus agricultural systems has not been well documented. An attempt was made to characterize indigenous rhizobia in a few sites in some African countries including Uganda (Woomer et al., 1997). This is an important aspect that should be investigated so as to understand microbial changes (both quantitative and qualitative) and their impact on crop productivity.
Mycorrhizal associations have been linked to improved plant water uptake. Through efficient water uptake they quickly reduce water in the rhizosphere for the other flora reducing their impact on the plant. Additionally, root and hyphal penetration improved soil structure enhancing water–air relations.
The status of rhizosphere microbiota is influenced by the stage of plant development (Alexander, 1961; Lynch, 1990; Paul & Clark, 1996). Furthermore, human activities such as tillage or deforestation disturb the microbiota.
Comparison of ecosystems in relation to diversity and abundance of rhizosphere biota
Trees dominate forest and mountainous ecosystems unlike savanna ecosystems, which mainly support grass species. Consequently, the rhizosphere biota is qualitatively and quantitatively different. Trees often stimulate more fungal species (especially mycorrhizae) than bacteria whereas the reverse is true for grasses (Alexander, 1961).
Forest and Mountain vegetation reduces surface temperatures compared with those obtaining in other ecosystems consequently modifying the microclimate. Accordingly, both plant species and the microbial populations adapt to the prevailing conditions. Contrary, semi-arid and arid locations experiencing high temperatures and low moisture support drought resistant plant species. The latter invariably stimulate different microbial populations in their rhizosphere.
Linkages of rhizosphere biota with aboveground biodiversity: comparison under different ecosystems
The microflora in the rhizosphere is greatly affected by the growing plant that forms the major aboveground biodiversity (Alexander, 1961; Paul & Clark, 1989; Bolton et al., 1993).
Plant impact is mainly exhibited through additions of organic substrates to the rhizosphere, whose materials also influence the solubility of certain inorganic nutrients. Root penetration with subsequent improved soil structure, indirectly enhances microbial oxidations. Among the organic plant exudates in the rhizosphere are growth promoting substances e.g. auxins (Alexander, 1961; Paul & Clark, 1989). Besides, some plants produce some biocides e.g. asparagus produces a glycoside toxic to stubby root nematodes. Tomato, onion, pea and bean plants produce other phytoalexins, such as tomatin, allicin, pisatin and phaseolin respectively (Kartz et al., 1987; Lynch, 1990). The toxins may be important in agricultural systems where the afore-mentioned crops are grown. Additionally, there is increased water uptake that possibly halts denitrification and leaching of nitrates detected even in a plant as small as 15 cm high (Paul & Clark, 1996, 1989).
Stimulation of microsymbionts e.g. mycorrhizae and rhizobia and/bradyrhizobia associations is an important consideration. In temperate regions, certain forest trees associated with basidiomycete fungi confer a mutualistic interaction that results in increased efficient plant nutrient uptake (Swift, Heal & Anderson, 1979). Nonetheless, mycorrhizal association with nonbasidiomycetes is also documented (Paul & Clark, 1996).
Work in Uganda is largely concentrated on rhizobia and plant pathogens; inevitably substantial efforts are required to relate microbiota to above-ground plant species particularly in the rhizosphere. Both the plant and the rhizobiota strongly influence each other making it critical to understand the interactions for optimal benefits (Bolton et al., 1993).
Diversity, abundance and distribution of rhizosphere biota in Uganda
Diversity: species (taxonomic) richness
Rhizosphere biota in Uganda has not satisfactorily been identified and classified. Attempts elsewhere in the world are equally sketchy. The process is plagued by a number of pitfalls that are encountered in microbiological studies (Swift et al., 1979; Giller et al., 1997). However, in Uganda, Emechebe (1975) listed important plant pathogens and a revised compilation (Sekamatte & Okwakol) will be presented in the same.
Microsymbionts in Uganda particularly Rhizobium species have been described based mainly on host-nodulation attributes. Several reports suggest that most legumes nodulate with indigenous species/strains (Stephens, 1967; Stobbs, 1969; Silver, 1976; Woomer et al., 1997). While substantive work has been carried out in agro-systems, little is documented under natural systems in Uganda, necessitating urgent studies in this area to correct the anomaly.
Distributional (spatial and vertical) patterns
Organisms in the rhizosphere occupy the volume of soil close to plant roots. Roots may extend to great lengths and depths, hence expanding the distribution of the microflora. It is generally reported that the number of microbes decreases as the distance from the root increases (Table 1).
Table 1. Changes in number of microbes at increasing distance from the root surface
The depth of the roots, availability of oxygen, moisture and organic substrates undoubtedly control vertical distribution of rhizosphere biota. Generally, these decrease with depth. Direct citation of vertical rhizobial distribution in Uganda is lacking; unless indirectly corroborated to nodule positioning on the root system (Silver, 1976).
Temporal patterns (succession)
Rhizosphere biota essentially follows vegetation changes and successions, as the populations are closely dependent upon the plant roots. Thus, sparsely vegetated ecosystems or landscapes existing in desert and degraded lands, likely have fewer rhizosphere biota. Secondly, such plants produce more lignified material, which calls for lignolytic microflora mainly fungi.
As the vegetation progresses through grassland the prevalent organisms would be bacteria changing to fungi as forest ecosystem manifest. Agricultural land has less plant species diversity diminishing the rhizosphere microflora. For example, legumes stimulate nodule bacteria unlike grasses or orchards (Diaz et al., 1989). Furthermore, rhizosphere of beet, tobacco, mustard and several legumes favourably stimulate Azotobacter but not onions, wheat and corn. Absence of a host legume causes a decline in a number of homologous rhizobia (Alexander, 1977); yet such information of temporal succession on rhizosphere biota in Uganda is lacking.
The importance of rhizosphere biota in the ecosystems
The impact rhizosphere micro-biota may be positive or negative or both but definitely modifies microbiologically mediated reactions e.g. denitrification and nitrification. For example, there is a distinction in population of rhizosphere and nonrhizosphere soil in bacterial taxonomic groups (Table 2).
Table 2. Variation in microorganisms in bulk and rhizosphere soil
|Taxonomic group bacteria||9.1||7.7||24|
|Nutritional groups ammonifiers||8.7||6.6||125|
High production of CO2 and organic acids indicative of elevated microbial population and activity improves solubilization of certain nutrients. Temporarily increased flora may also intensify nutrient immobilization especially of N and P. Further, aerobic bacteria deplete O2 hence create anaerobic conditions, which may curtail root respiration and active nutrient uptake. Anaerobiosis thus created may favour the prominence of denitrifiers although denitrification may not necessarily increase.
Rhizosphere biota also favour plant growth by producing growth factors e.g. auxins, and forming symbiotic associations e.g. rhizobial and mycorrhizal types. On the other hand, some organisms produce toxic compounds while others are pathogenic and reduce plant growth.
In Uganda, there is reasonable knowledge about Rhizobium-legume symbiosis and pathogenic relationships. There is, however, poor knowledge about other rhizosphere relationships. In both cases, there is a need to either strengthen or initiate studies to elucidate these interactions.
Indigenous knowledge, if available, is not documented. Casual observations indicate that most land users, especially farmers are conscious about the value of leguminous and nonleguminous crops. They understand the importance of crop rotation, although they may not directly relate it to soil biota.
Country capacity for rhizosphere biota studies
Significant among rhizosphere organisms are, plant microsymbionts such as rhizobia, cyanobacteria, actinorrhizal and mycorrhizae, parasitic and plant pathogens. Commensalism and protocooperation may prevail among bacteria, nematodes, fungi and protozoa. The National Institutions to handle studies on these organisms include: Faculties of Agriculture, Science, Veterinary Medicine and the Medical school of Makerere University, which have laboratories with basic equipment for the initial work. National Agricultural Research institutes e.g. Kawanda and Namulonge also have microbiological laboratories besides Entebbe virus Research Institute. Nonetheless, there are limited scientists in both categories of institutions thus posing a human resource constraint.
Rhizosphere biota and sustainable land management
Relationship of rhizosphere biota to agricultural productivity
The role rhizobiota play in sustainable agriculture is immense. The microsymbionts review will be elaborate on this attribute. These organisms participate significantly in harnessing and enhancing nutrient availability for plants, particularly in agricultural systems. Several citations highlight benefits accruing from legume-Rhizobium symbiosis (Stephens, 1967; Stobbs, 1969; Silver, 1976; Nkwiine, 1992; Jjemba, Kintukwonka & Male-Kayiwa, 1994; Semana & Silver, 1997; Rwakaikara-Silver & Alumai 1999; Giller, 2001). In addition, actinorrhizal (frankia and nonleguminous plants) contributions (Paul and Clark, 1996; Giller, 2001) and mycorrhizal associations are important rhizobiota (Alexander, 1961, 1977; Swift et al., 1979). Agro forestry and improved legume cover crop technologies largely exploit biological nitrogen fixation particularly the rhizobia-legume symbiosis.
Apart from ensuring that fixing and nonN2-fixing crops are interchanged to enhance N availability; crop rotation also breaks pest cycles particularly pathogens. Absence of the host may reduce pest infestations.
Some of the rhizosphere biota is capable of degrading recalcitrant molecules such as lignin especially if roots are lignified. This may assist in decomposition and hence nutrient cycling. Some rhizosphere produce growth promoting substances while others generate phyto-toxins possibly utilizable as bio-control agents for diseases and insect pests or nematodes.
While knowledge about the above phenomena is available, gaps still exist. For example, it is still important especially in Uganda to get effective Rhizobium strains for different hosts in the various agro-ecological zones. In most cases, except for soybean, responses to inoculation are sporadic (Stephens, 1967; Silver, 1976). Woomer et al. (1997) mainly attribute this failure to the presence of an adequate and aggressive native rhizobial population.
There is also urgent need to identify, characterize and evaluate the local mycorrhizal associations. For example, it is imperative to define the benefits derived from tithonia because speculative explanations imply tithonia-mycorrhizal interactions. Furthermore, biocidal chemicals produced by rhizosphere biota should be exploited to develop bio-control packages to increase crop productivity and maintain environmental quality.
Management of soil rhizosphere biota
Inoculating legume seed with rhizobia or direct application into soil or in irrigation water is commonly practiced thus influencing rhizosphere biota although seldom done in Uganda. Frequently, there are corresponding plant response and increased yields (Lange & Parker, 1961; Francis & Alexander, 1974; Semana & Silver, 1997). Occasionally the responses were nonsignificant, owing to several causes including ineffective strains (Parker, 1977) or competition from indigenous rhizobial flora (Silver, 1976; Miller & May 1991; Woomer et al., 1997).
Similarly, application of pesticides to control pathogens is sometimes recommended. Nonetheless, a new paradigm considering integrated pest management is the current strategy and will, probably involve soil biota or their products. This approach may reduce the impact of chemical pesticides particularly on nontarget organisms in the rhizosphere.
Crop rotation, where the host plant is regularly excluded, may also modify the rhizosphere micro-flora. Thus, modern methods of manipulating rhizosphere organisms include inoculation, application of agrochemicals, crop rotation and, to a limited extent change in the plant genotype. On the contrary, traditional management of rhizosphere biota has largely relied on crop rotation or shifting cultivation.
In Uganda and probably elsewhere in the world, there is no specific policy on rhizosphere biota. However, policies on agriculture, soils, environment and wild life may indirectly influence soil biota.
Plan for Modernization of Agriculture (PAM) would definitely influence rhizosphere biota. The policy is geared towards using more efficient production methods to boost yields. The expected results would be food security and increased household incomes. Ultimately, reduced poverty may relieve pressure on land and allow land to rejuvenate.
Although Uganda has not had a soils policy, soils resource management plans and the classification system are outdated. A draft policy has been prepared awaiting government approval and institutionalization. Guidelines to manage soils properly are likely also to protect rhizosphere biota.
The Land Act, 1998, guaranteed security of land tenure to individuals formerly squatting on land belonging to land-lords. Probably this will encourage investments in land husbandry technologies. Farmers can plant trees of long-growing periods, construct soil conservation structures like contour bands or terraces, purchase organic or inorganic fertilizers or both. These land activities would eventually influence soil biota.
The National Environment Management Statute 1995 mandated (NEMA) to protect the environment. Therefore, destructive practices like uncontrolled bush fires, deforestation, encroachment on marginal and fragile areas are prohibited or require the user to employ suitable methods. There are also protective policies gazetted areas e.g. forest, game and wildlife that provide various services. The Uganda constitution also has provisions that indirectly would protect rhizosphere biota through careful management of above ground biota.
Globally, Uganda signed and ratified the United Nations Convention on Biological Diversity whose main objective was to protect biological species. Uganda is in a process of developing a biodiversity strategy and action plan.
Recently microorganisms have attracted political and economic attention as Shand, (1997) has skillfully highlighted. Complex problems are raised, which include the definition and delineation of a microorganism, the question of intellectual property rights (IPR) and acquisition of human genetic material. In Uganda, the Uganda National Council for Science and Technology is spearheading discussions on this issue. The Council is also developing guidelines regarding IPR and access to genetic resources.
Future priorities for research, application and capacity building
While globally a great deal of knowledge in microbial and rhizosphere population has been generated, there is no or very scanty information in Uganda. Furthermore, Uganda's economy still depends on agriculture and other natural resources; it is therefore, imperative that information is urgently obtained. The following research areas are proposed in order of priority.
- • Strengthen the Rhizobium-legume N2 fixation research, i.e. ensure adaptable and efficient strains are available for important tree, pasture and grain legumes.
- • Make an inventory of rhizosphere biota in major natural (forest, rangelands, semi-arid) and agro-systems.
- • Actinorrhizal-nonlegumious crops studies.
- • Azolla–cyanobacteria N2-fixing system should be explored in paddy rice.
- • Explore the ability or rhizosphere biota in production of plant growth promoting factors, particularly in solubilizing insoluble forms of nutrients e.g. phosphate rock and bio-control agents.
- • Develop methods of controlling nutrient losses.