Status of research on soil microsymbionts in Uganda

Authors


*E-mail: bgbdiversity@acadreg.mak.ac.ug

Abstract

A symbiotic relationship involves two or more organisms living together for mutual benefit(s). Neither partner could do well without the other. Symbionts are the individual partners in the relationship. Microsymbiosis is a relationship in which one of partners is a micro-organism. Most of the symbioses involve higher plants acting as hosts to micro-organisms. Microsymbionts play a major role in plant nutrition especially for nitrogen, phosphorus and water availability in both natural and agricultural ecosystems. They are a valuable resource for national development especially to countries, like Uganda, whose economies are heavily agro-based. This review gives an inventory of the present knowledge on microsymbionts in Uganda and identifies future priorities for research, application and capacity building. In Uganda, not much is known or has been done regarding microsymbionts and their importance in both natural and agroecosystems. This may be associated with the fact that there are few scholars in the field of soil science available in the country. There is no specific policy on the conservation of microsymbionts. Attempts have been made on production and use of Rhizobium inoculants for promotion of the role of legumes in agricultural production. Other symbioses like mycorrhizae, Azolla and Frankia have not been exploited. Awareness raising and in-depth research on soil microsymbionts’ production and use are recommended.

Introduction

Ecologically sound technologies are a key to sustainable management of tropical soils. Most of them are based on biological processes by adapting germplasm to advance soil conditions, enhance soil biological activity and optimize nutrient cycling to minimize external inputs and maximize the efficiency of their use (Sanchez et al., 1996). Key functional groups like microsymbionts and earthworms have been used to develop such technologies (Woomer & Swift, 1994).

A symbiotic relationship involves two or more organisms living together for mutual benefit(s). Neither partner could do well without the other. Symbionts are the individual partners in the relationship. Microsymbiosis refers to one of a relationship in which one of the partners is a micro-organism. Most of the symbioses involve higher plants acting as hosts to micro-organisms. As already implied, microsymbionts play a major role in plant nutrition especially for nitrogen, phosphorus and water availability in both natural and agricultural ecosystems.

Unfortunately, little research work has been conducted in Uganda regarding soil micro-organisms and specifically microsymbionts and their importance in both natural and agroecosystems. Past research on maintenance and improvement of soil productivity in Uganda has concentrated on mineral fertilizers, fallow, phosphate rock, liming, manuring, mulching, intercropping, agroforestry and soil conservation (Braun et al., 1997). In all this work, there is very little, if any, consideration of scientifically designed approaches towards exploitation of soil microsymbionts for sustainable soil productivity and conservation of the environment. Furthermore, most of previous research conducted even elsewhere, has been concerned with plant growth responses with little consideration of the microsymbionts involved. This has a false impression of their specific functions in the process of production in both natural and managed systems.

There is, however, great potential for manipulating microsymbionts and their host associations for use in rehabilitating degraded landscapes, soils and environment of Uganda to attain sustainable land management, agricultural production and environment health. Therefore, this review aims at developing an inventory of the present knowledge about microsymbiants in natural and agroecosystems of Uganda and identifying future priorities for research, application and capacity building. Because of the limited scope of knowledge on microsymbionts in the country, most of reviewed work performed done elsewhere but is considered fit for application in Uganda.

Microsymbionts in natural and agricultural systems

Colonization of natural and agricultural systems by microsymbionts largely depends on the presence of suitable host plants, categories of the symbioses, availability of necessary growth requirements and the degree of disturbance or management of the systems. For instance, lack of suitable host plants has been noted to reduce populations of matchable microsymbionts in both natural and agricultural systems (Somasegaran & Hoben, 1994). Monocultures, plantations and pure stands, which seem to be on an increase in developing countries, are not suitable for conservation of microsymbionts.

Different types of microsymbionts are found in different niches of both natural and agricultural systems and for differing uses. Enhancement of roles played by microsymbionts in productivity of both natural and agricultural systems requires detailed knowledge of the characteristics of both the host plant and endophyte as well as of their biotic and abiotic environments as source of necessary growth requirements.

Another factor to consider while looking at microsymbionts in both natural and agricultural systems is land use conversion. It was estimated that Uganda has remained with 21% of its original forest lands and lost the rest to other uses (Republic of Uganda, 1994, 1996). Such land use conversion has effects on microsymbiont systems. Influence of such disturbance or management practices has been well demonstrated by studies on mycorrhizae. Research findings have shown that natural systems are highly colonized by fungal species diversity (Smith, 1995). Different species respond differently to conversion of natural systems into agricultural systems. Arbuscular mycorrhizae (AM) fungi spores are very few in undisturbed forests and increase with low to moderate degrees of disturbance. With highly intensive input agriculture, the number of arbusclar mycorrhizal propagules and species richness decrease (Sieverding, 1991). In addition, heavy grazing of grassland especially in a semi-arid region, significantly reduces AM development (Bethlenfalvay et al., 1988). For ectomycorrhizal (EM) fungi, when natural systems are converted into agricultural systems the production of sporacarps ceases.

Comparison of ecosystems in relation to diversity and abundance of microsymbionts

Diversity, abundance and activities of microsymbionts are key parameters that measure the usefulness of the organisms in an ecosystem. Comparison of various ecosystems in relation to such parameters gives information regarding the degree of ecological environmental soundness of the systems. Few such specific studies have been conducted in East Africa or in Africa as whole, except some research trials initiated by Rhizobium Ecology Network of East and Southern Africa in 1991 on characterization of indigenous rhizobial populations in the region. Results of the work showed that Bradyrhizobium spp. are the most frequently observed species in wet and semi-arid lowlands (2.37 and 1.84 log10 cells g−1 of soil respectively) and were consistently high in the humid areas of Uganda. The same work also revealed that rhizobia nodulating bean, Phaseolus vulgaris, are the greatest in highland soils (3.01 log10 cells g−1 of soil), particularly in the Kenyan and Rwandan highlands (Woomer et al., 1997).

Linkage of microsymbionts with above-ground diversity

Above ground diversity is well linked to microsymbionts as their hosts in the mutual benefit relationship. The above-ground diversity performs well, if infected by microsymbionts, especially when growing on nutrient deficient soils and/or in moisture stressed soils.

Symbiosis of Rhizobium and legumes is a most exploited relationship involving microsymbionts in Uganda and globally. Under both natural and agricultural systems and with suitable ecological conditions, Rhizobium species are highly linked with grain and pasture legumes, and nitrogen fixing trees (Danso, Bowen & Sanginga, 1992). The microsymbionts are linked to the aboveground diversity as they are directly supplied with energy-rich photosynthetic compounds through the flow of plant (legume) sap. Rhizobia in turn provide fixed nitrogen to the plant. (Day & Witty, 1977; Somasegaran & Hoben, 1994). In Uganda, some exploitation has been done on legume-rhizobia symbiotic relationship for increasing the legume yields.

Frankia forms nodules with nonleguminous. Table 1 shows a list of shrubs and trees found to be nitrogen-fixing with Frankia symbiosis. These include Casuarina species, which are vigorous nitrogen fixers, harvested for construction timber after 5 years of growth (NAS, 1982). Growing of these trees is gaining popularity in Uganda. There have been few research studies on Frankia and this limits their symbiont use in plant production systems.

Table 1.   Genera of nitrogen-fixing plants with Frankia symbiosis
GenusNo. of nodulated species
  1. Source:Moirud & Gianinazzi-Pearson (1984).

Albus34
Casuarina25
Cenothus31
Cercocarpus4
Chamaebatia1
Colletia3
Coriaria14
Cowania1
Cowania2
Satisca6
Discaria3
Dryas17
Elaeagnus1
Hippophae1
Kentrothamnus26
Myrica2
Persia1
Rubus3
Sheperdia1
Talguena1
Trevoa2

Cyanobacteria relate with a diverse range of host plants including ferns, lichens, liverworts, gymnosperms (cycads) and angiosperms (gunnera). Such wide host spectrum for cyanobacterium indicates a potential for genetic manipulation to increase host range.

Among cyanobacterial symbioses, Azolla symbiosis has been the most researched one although not in Uganda. Researchers have, however, overlooked the rest of cyanobacteria nitrogen fixing systems and little is known about them.

In his book on Azolla, van Hove (1989) gives a lot of practical approaches to domestication of Azolla symbiosis in Africa. Cyanobacterium anabaena forms a symbiotic relationship with species of Azolla, a free-floating fern commonly found in still waters. Azolla provides nutrients and a protective leaf cavity for the C. anabaena which, in turn, provides nitrogen for Azolla. In Uganda, the symbiosis has great potential use in paddy rice growing and the fish industry as a nitrogen fertilizer source and protein feed respectively.

In all ecosystems, i.e. forest, savanna mountains and semi-arid areas, there is a great plant's dependence on mycorrhizae. Plants are dependant on mycorrhizae for enhancement of nutrients like phosphorus and zinc and water availability, providing tolerance to low nutrient and water stress in some ecosystems. Mycorrhizal associations also provide growth substances and may reduce stresses, diseases or pest attack (Bethlenfalvay, 1992; Sylvia & Williams, 1992; Davet, 1996; Smith & Read, 1997).

Plant dependence may be qualitatively rated from strong to none as with examples shown in Table 2. Variations in the plant's response are determined largely by the type of root system it has. Plants with well developed, fine, dense roots such as grasses are dependent on mycorrhizae only in nutrient-poor soils (Baylis, 1970). Plants with a weakly developed, coarse root system and few root hairs are dependent on mycorrhizae under all conditions and examples include cassava, onions, young citrus plants (Sieverding, 1991; Muller-Samann & Kotschi, 1994).

Table 2.   Qualitative rating of vesicular-arbuscular mycorrhizal dependence of host plants
StrongIntermediateWeakNone
AlliumArachisAgrostisCaryophyllaceae
AsparagusCicerFestucaChenopodiaceae
CassavaGossypiumSecaleCruciferae
CitrusMedicagoSolanumCyperaceae
CoffaeSorghumOryzaePhytolaccaceae
PrunusPapsalumLupinPinaceae
VignaPhaseolus Pinaceae
VitisZea Zygophyllaceae

Diversity of microsymbionts

Currently, the classification of rhizobia has been revised and confirmed to have four genera each having different numbers of species as shown in Table 3. By DNA–DNA homology analysis, many species of rhizobia were found to be relatively unrelated. Yet, they form effective symbioses with many legumes in common (Elkan, 1992). This genetic diversity of these rhizobia gives a broad germplasm from which selection for different environments and hosts can be made. In addition, the microsymbionts relate well to the aboveground diversity as demonstrated in what has been established as different cross-inoculation groups of legumes nodulated by rhizobia as shown in Table 4.

Table 3.   Current taxonomic classification of rhizobia
Recognized generaRecognized species
Bradyrhizobium (Jordan, 1982)B. japonicum (Jordan, 1982)
Rhizobium (Jordan, 1982)R. leguminosarum (Jordan, 1982
 R. meliloti (Jordan, 1982)
 R. loti (Jordan, 1982
 R. galegae (Lindstrom, 1989)
 R. tropici (Martinez et al., 1991)
 R. huakuii (Chen et al., 1991)
Azorhizobium (Dreyfus, Garcia & Gillis, 1988)A. Caulinodans (Dreyfus et al., 1988)
Sinorhizobium (Chen, Yan & Li, 1988)S. Fredii (Chen et al., 1988)
 S. xinjiangensis (Chen et al., 1988)
Table 4.   Rhizobia and the legumes they nodulate
Common nameScientific nameCross-inoculation group of legumes nodulated
  1. Source:Sarrantonio (1991).

Clover rhizobiaRhizobium leguminasarun biovar. trifoliiClover group (Trifolium) sp.
Pea rhizobiaR. leguminasarum biovar. ViceaePea and vetch group (Pisum spp., Vicia spp., Lens spp.)
Bean rhizobiaR. leguminosarum biovar. phaseoliBean group (Phaseolus vulgaris, P. coccinius)
Lotus rhizobiaR. lotiChick pea (Cicer arietum) Lotus spp. Lpinus spp.
Alfalfa/medic rhizobiaR. melilotiAlfalfa (Medicago) spp. Sweet clover (Melilouts)
  Foenugreak (Trigonella)
Soya bean rhizobiaBradhyrhizobium japonicumSoya beans (Glycine max)
 Sinorhizobium fredii 
 R. fredii 
Stem rhizobiaAzorhizobium caulidansSesbania rostrata
S. rhizobiaRhizobium spp.S. gradiflora
 S. Speciosa, S. aegyptica 
Leucaena groupRhizobium spp.Leucaena spp.
 Sepium, Prosopis spp.Gliricidia
Cowpea groupBradyrhzobium spp.Vigna spp., Macroptillium spp., Aradiis spp., Sylosanthes spp., Centrosema spp., Desmodium spp., Crotalaria spp., etc.

There have been a few taxonomic studies on Frankia, and thus knowledge of the interrelationships between Frankia isolates is rudimentary. There are two distinct groups within this genus, one forms sporangia within nodules, and the other does not (or may do so only occasionally). The sporangium-forming types fix less nitrogen, grow more slowly and are more difficult to isolate and grow in pure culture. It appears that both groups can nodulate the same host.

van Hove (1989) considered that the genus Azolla generally contains two sections:

  • 1Section Rhizsperma: having megasporocarps with nine floats and glochidia are absent or unbarbed. These include A. nilotica and A. pinnata.
  • 2Section Azolla: having megasporocarps with three floats and glochidia are present and barbed. These include A. caroliniana and A. mexicana, A. microphylla, A. filiculoides and A. rubra.

Harley & Smith (1983) divided mycorrhizal associations into five categories consisting of:

  • 1Vesicular-arbuscular mycorrhizae (AM) in which zygomycetes fungi produce arbuscules, hyphae and reside within root cortex cells.
  • 2Ectomycorrhizae – where Basidiomycetes and other fungi form a mantle around roots and a Hartig net between root cells.
  • 3Orchid mycorrhizae – where fungi produce coils of hyphae within roots (or stems) of orchidaceous plants.
  • 4Ericoid mycorrhizae – involving hyphal coils in outer cells of the narrow ‘hair roots’ of plants in the plant order cricales.
  • 5Ectendo – arbutoid and monotropoid associations, which are similar to EM associations, but have specialized anatomical features.

Spatial distribution and the determining factors

Climatic conditions, variation in vegetation (presence or absence of host plants), food sources, and soil conditions, are primarily responsible for determining the spatial distribution and abundance of microsymbionts.

No specific studies are there on spatial distribution of microsymbionts in Uganda. But generally, when the soil surface is exposed (without vegetation or mulch cover), the numbers may be low due to lack of moisture and to the germicidal action of the sunlight. Usually, the numbers decrease with the soil depth (Paul & Clark, 1996). The rate of the population decline will depend on the soil conditions especially, density of plant roots, organic matter content and aeration.

All ecosystems have some microsymbionts. Rhizobia and other nitrogen fixing microbes are widely distributed and are especially dependent on their macrosymbionts (Paul & Clark, 1996). There are maps available indicating the geographical distribution of legume and other crops (Jones, 1972) that live in symbiosis with microbes to fix nitrogen.

Arbuscular mycorrhizae are widely distributed in all ecosystems especially when soils are deficient on nutrients. But ectomycorrhizae are less common in tropical soils than temperate soils (Meyer, 1973). This is attributed to high tropical temperatures. Also deforestation in Africa has been noted to lead to reduced mycorrhiza propagules.This has often caused failure of forest plant species recolonization leading to new situations favouring the ‘derived savannas’ (Janos, 1987).

The distribution of Azolla in Africa has been described by van Hove (1989) with respect to species as indicated below: A. nilotica: Native of east Africa, strenching from Sudan to Mozambique.

Azolla pinnata var. pinnata is found throughout Africa south of the Sahel, Madagascar and Australia.

Azolla pinnata var. imbricata: originates from subtropical and tropical Asia. Commonly used in China and Vietnam.

Azolla caroliniana, A. mexicana and A. microphylla: all originate from temperate, sub tropical and tropical regions of North and South America.

Azolla filiculoides and A. rubra: are native of America and the far east.

Importance

This section analyses how soil symbioses can be used in improving natural and agricultural production systems. This is a very important aspect of this review during this era of global focus on science for the people. Most symbioses involve higher plants (macrosymbionts) acting as hosts to micro organisms (microsymbionts). Such associations do exist naturally in both natural and agricultural systems.

Microsymbionts of great significance and which are most common together with their importance have been shown in Table 5. They include those that avail biologically fixed nitrogen and enhance bio-availability of nutrients like phosphorus and water supply to the plant and contribute to promotion of environmental health.

Table 5.   Categories of soil microsymbionts and their importance
Categories of symbiosesImportance
Legume –RhizobiumNitrogen fixation
Plant roots – mycorrhizalImproved availability of phosphorus and moisture
Legume –Rhizobium– mycorrhizalNitrogen fixation and improved availability of phosphorus and moisture
Rhizosphere-associated microfloraImproving nutrient supply through solubilization of nutrients or direct nitrogen fixation

The contribution by symbiotic fixers of atmospheric nitrogen into the soil is well known as is their importance to global nitrogen economy. Different researchers have documented the magnitude of nitrogen fixed as shown in Table 6. The amounts of fixed nitrogen by the symbioses are quite high so as to offset the problems associated with the use of mineral nitrogen fertilizers especially in developing countries like Uganda that import fertilizers.

Table 6.   Reported ranges of biological fixed by microsymbionts’ systems in tropical soils
Microsymbiont system Fixation rates (kg ha−1 year−1)
Rhizobium/legume24–584 (Gibson, Dreyfus & Dommergues, 1982)
Frankia2–300 (Paul & Clark, 1996)
Cyanobacteria30–70 (Paul & Clark, 1996)
Azolla/Anabaena45–450 (Lumpkin & Plucknett, 1982)

In terms of yields, different crops have been reported to respond positively to inoculation with various microsymbionts. Incase of Rhizobium and grain legumes, Nkwiine (1999) reported 30–70% increase in soya bean yield. Increase of 80% of groundnuts yield (Nkwiine et al., 1998) has been obtained.

Sieverding & Saif (1984) obtained 29% increase in cassava yields with mycorrhiza inoculation. The same workers reported 65% increase in fodder legumes after 20 kg ha−1 of rock phosphate application followed by inoculation with efficient mycorrhizal strains. Furthermore, Jackson, Franklin & Miller (1972) obtained 50% yield increase by inoculating maize with an efficient mycorrhiza strain. Senna spectabilis responded to AM inoculation giving a root collar diameter, shoot production and root biomass increase of 85%, 213% and 241% respectively (Kung'u, 2004).

Because of the fact that they are usually many species with similar functions, they provide ecosystems with mechanisms of resistance to climate and other environmental changes. For example, in the cross-inoculation phenomenon in Rhizobium-legume symbiosis, the cowpea crop is nodulated by a wide range of Rhizobium species as indicated in Table 4. A tree is also able to form ectomycorrhizae with a lager number of fungi. The elimination or absence of a few of those microsymbionts may have no significant effect on the macrosymbiont. As such, these micro-organisms provide increased ecosystems resistance to perturbations (Daft & Hogarth, 1983; Ellis, Roder & Mason, 1992).

Microsymbionts have also been used as bio-indicators of ecosystem health. Loss of microsymbionts as a result of disturbance, pollutants or climatic factors is an early warning of changes in an ecosystem. Examples of this are lichenized fungi that respond to gaseous pollutants (Hawksworth, 1990) and mycorrhizal fungi that are affected by acid rain. Such organisms are specifically useful early indicators of ecosystem damage before trees and crops start to be adversely affected. It has been noted that knowledge on microsymbionts as bio-indicators of ecosystem health is still lacking (Salanki, 1986; Hawksworth, 1992).

Capacity, awareness and indigenous knowledge about microsymbionts

In terms of human capacity, there are few scholars in the field of soil science in Uganda and very few of them are knowledgeable on soil microsymbionts and their use.

Departments at Makerere University (Soil Science, Crop Science, Zoology, Botany and Agroforestry) together with institutes of NARO, constitute a capacity that could propel development of efficient microsymbiont systems in the country if well linked, coordinated and facilitated. The department of Soil Science initiated production of Rhizobium inoculants for legume production (Nkwiine, 1992). The inoculants are produced and made available to farmers for use in agriculture. The level of production and use of the inoculants are still limited by the low level of awareness among stakeholders in the country (Semana & Silver, 1997). Lack of soil biota specialists with expertise in natural resource management and rural/community development is associated with the lack of awareness of beneficial soil organisms among stakeholders in most developing countries.

In Uganda, there is little local knowledge on microsymbionts. From interactions with farmers, particularly from south western and central regions of the country, it was noted that different views are held on these soil organisms. Farmers from the south western region call legume nodules formed by rhizobia ‘Orweezo’ literally interpreted as fertilizers. They associate the nodule abundance on roots with good performance of the legume crops in terms of yields. Farmers from the central region (Baganda and Basoga) regard legume nodules as an abnormal root growth. They sometimes mistake them for nematode galls. For other microsymbionts like mycorrhizae, the lack of local knowledge is even worse. So, there is a need for sensitizing the public on the microsymbionts, their importance and their use.

Relationship of microsymbionts to agricultural productivity

Plant–soil organism relationships, in the form of symbiosis, are crucial and unique support for agricultural productivity. Most of Ugandan soils are increasingly becoming degraded as indicated by low availability of major nutrients like phosphorus and nitrogen (Ssali, 2000). This is associated with increased frequency of prolonged draughts (Republic of Uganda, 1994, 1996). Feasible strategies for harnessing the microsymbionts for agricultural purposes should be made. If soil is degraded in the form of low availability of phosphorus, the importance of both types of mycorrhizal symbiosis in phosphorus and moisture supply has been very well demonstrated (Coush, 1974; Saif, 1986; Arias et al., 1991; Medina & Bilbao, 1991). After soil nitrogen depletion through leaching or crop removal, use of symbiotic associates (microbes) that have capacity to fix atmospheric nitrogen into soil is reported to contribute significantly (Giller & Day, 1985; Saif, 1986; Hayman, 1990; Hansen, 1994). The nodulation with Rhizobium is enhanced significantly probably due to the improved phosphorus supply to the plant mediated by the mycorrhizal symbiosis (Saif, 1986).

Management of soil microsymbionts

Soil being a basic niche of microsymbionts and their hosts (macrosymbionts), successful management of soil microsymbionts requires proper soil characterization and better understanding of the ecological requirements of the microsymbionts. Maximum benefits from use of microsymbionts in national plant production systems can only be realized when the organisms are easily available in an usable form and there is basic knowledge of their interaction with soil types, levels of nutrients, moisture regimes and land management practices (Doran & Linn, 1994; Brundrett et al., 1996), and intended delivery system of the technology to end users. There is an increasing level of use and better management of Rhizobium inoculants in Uganda, although as already indicated, awareness of the product is still low.

Rhizobium inoculants are easily produced. Massive production of quality mycorrhizae inoculum for plants has, however, remained a major problem not only in Uganda but also elsewhere. Furthermore, large quantity is required for field crops ranging between 1.7 × 105 and 4.2 × 103 kg inoculum per hectare (Powell, 1984; Menge, 1985). To overcome this limitation to AM use, Millner (1991a,b) suggested an approach that involves management of indigenous AM. It requires preserving indigenous AM populations to optimize the symbiosis for increased crop productivity, particularly in situations where indigenous AM are deficient in quantity and quality. The preservation process involves promotion of agronomic practices that stimulate indigenous AM populations and enhance their activities. Such practices include polycultures, rotations, application of manures and mulching. Farming practices such as prolonged monocultures and over tilling the soil tend to reduce the activities of indigenous AM population. Dodd et al. (1990), as an alternative to inoculation, the use of a plant host such as cassava able to increase the number of mycorrhizae propagules prior to the planting of the main crop such as cowpea. All the approaches require detailed knowledge of the characteristics of both the host plant and endophyte as well as the biotic and abiotic components of soil.

Policies relevant to conservation of microsymbionts

There is no specific policy on conservation of microsymbionts in Uganda. There is also no explicit policy on soil management in the country. The national quarantine regulations for importation and exportation of micro-organisms are relevant initiatives towards conservation of microsymbionts. Other initiatives include the environment policy, which resulted in the formation of Ministry of Water, Land and Environment in the country (Kamugisha, 1993). The Ministry's concerns are: soils, water resources, forests and other vegetation, wildlife and wetlands, which directly or indirectly affect the conservation of microsymbionts.

Conclusion

Microsymbionts should be harnessed during the process of modernizing agricultural production and improving environmental health in Uganda. Awareness raising and in-depth research on these important resources are paramount.

Ancillary