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Microbial Processes: Promising Technologies for Developing Countries (1979)

Chapter: SOIL MICROBES IN PLANT HEALTH AND NUTRITION

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Suggested Citation:"SOIL MICROBES IN PLANT HEALTH AND NUTRITION." National Research Council. 1979. Microbial Processes: Promising Technologies for Developing Countries. Washington, DC: The National Academies Press. doi: 10.17226/9544.
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Suggested Citation:"SOIL MICROBES IN PLANT HEALTH AND NUTRITION." National Research Council. 1979. Microbial Processes: Promising Technologies for Developing Countries. Washington, DC: The National Academies Press. doi: 10.17226/9544.
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Page 48
Suggested Citation:"SOIL MICROBES IN PLANT HEALTH AND NUTRITION." National Research Council. 1979. Microbial Processes: Promising Technologies for Developing Countries. Washington, DC: The National Academies Press. doi: 10.17226/9544.
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Page 49
Suggested Citation:"SOIL MICROBES IN PLANT HEALTH AND NUTRITION." National Research Council. 1979. Microbial Processes: Promising Technologies for Developing Countries. Washington, DC: The National Academies Press. doi: 10.17226/9544.
×
Page 50
Suggested Citation:"SOIL MICROBES IN PLANT HEALTH AND NUTRITION." National Research Council. 1979. Microbial Processes: Promising Technologies for Developing Countries. Washington, DC: The National Academies Press. doi: 10.17226/9544.
×
Page 51
Suggested Citation:"SOIL MICROBES IN PLANT HEALTH AND NUTRITION." National Research Council. 1979. Microbial Processes: Promising Technologies for Developing Countries. Washington, DC: The National Academies Press. doi: 10.17226/9544.
×
Page 52
Suggested Citation:"SOIL MICROBES IN PLANT HEALTH AND NUTRITION." National Research Council. 1979. Microbial Processes: Promising Technologies for Developing Countries. Washington, DC: The National Academies Press. doi: 10.17226/9544.
×
Page 53
Suggested Citation:"SOIL MICROBES IN PLANT HEALTH AND NUTRITION." National Research Council. 1979. Microbial Processes: Promising Technologies for Developing Countries. Washington, DC: The National Academies Press. doi: 10.17226/9544.
×
Page 54
Suggested Citation:"SOIL MICROBES IN PLANT HEALTH AND NUTRITION." National Research Council. 1979. Microbial Processes: Promising Technologies for Developing Countries. Washington, DC: The National Academies Press. doi: 10.17226/9544.
×
Page 55
Suggested Citation:"SOIL MICROBES IN PLANT HEALTH AND NUTRITION." National Research Council. 1979. Microbial Processes: Promising Technologies for Developing Countries. Washington, DC: The National Academies Press. doi: 10.17226/9544.
×
Page 56
Suggested Citation:"SOIL MICROBES IN PLANT HEALTH AND NUTRITION." National Research Council. 1979. Microbial Processes: Promising Technologies for Developing Countries. Washington, DC: The National Academies Press. doi: 10.17226/9544.
×
Page 57
Suggested Citation:"SOIL MICROBES IN PLANT HEALTH AND NUTRITION." National Research Council. 1979. Microbial Processes: Promising Technologies for Developing Countries. Washington, DC: The National Academies Press. doi: 10.17226/9544.
×
Page 58

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Chapter 3 Soil Microbes in Plant Health anc! Nutrition The parts of a plant above the ground can be compared to the tip of an iceberg, in that the portion under the surface—the root system—is so exten- sive. The root system is also very active metabolically and provides a continu- ous source of food for soil microorganisms in the form of secretions of organic compounds and sloughed-off dead cells and cell debns. Since the zone where roots and soils meet is a special environment, it has been named the rhizosphere (root zone). This zone comprises several poorly defined, hetero- geneous regions in which microorganisms are particularly active (Table 3.13. Although activity in the rhizosphere is of great importance to the plant, it affects only a small fraction (about 5 percent) of the root surface. Some microorganisms are loosely associated with roots, but others develop on the root surface and many can invade root tissue, with effects that can be bene- ficial or harmful. Certain soil-inhabiting microorganisms produce diseases of great significance to agriculture and forestry. Others are beneficial—they part- ly inhibit the growth of disease organisms or kill them. The vast majority of the pathogens that infect roots are fungi, and they are exceptionally difficult to control or eradicate. In some cases, the invasion of roots by microorganisms is desirable. This is true for the root-nodule bacteria of the genus Rhizobium that fix nitrogen, as well as for mycorrhizal fungi, which assist roots in accumulating phosphate and other essential minerals. Nitrogen fixation is the subject of Chapter 4 in this report; mycorrhizal fungi are discussed in this chapter. However, it should be emphasized that rhizosphere microorganisms can affect plant wel- fare in a number of ways that are not yet well understood or easily con- trolled. The processes of nutrient cycling, growth stimulation or inhibition, and diseases are of great significance, but they are very complex population effects rather than the result of simple interactions between roots and known microorganisms. The rhizosphere is also influenced by external factors such as soil moisture and even the intensity of light reaching the plant. No single microorganism may be essential to the process, but the combined effect of the rhizosphere population can be profound. 47

48 MICROBIAL PROCESSES TABLE 3.1 Comparison of the Numbers of Various Groups of Organisms in the Rhizo- sphere of Spring Wheat and in Control Soil Numbers per g Numbers per g Approximate in Rhizosphere in Control Rhizosphere: Organisms Soil(x 10-6) Soil(x 10-6) SoilRatio Bacteria 1,200 53 23 :1 Actinomycetes 46 7 7 :1 Fungi 12 0.1 120 :1 Protozoa 0.0024 0.001 2: ~ Algae 0.005 0.027 0.2 :1 Bacterial Groups Ammonifiers 500 0.04 12,500 :1 Gas-producing anaerobes 0.39 0.03 13: 1 Anaerobes 12 6 9: 1 Den~trifiers 126 0.1 1,260: 1 Aerobic cellulose decomposers 0.7 0.1 7: 1 Anaerobic cellulose decomposers 0.009 0.003 3: 1 Spore formers 0.930 0.575 2: 1 "Radiobacter" types 17 0.01 1,700: 1 Azotobacter <0.001 <0.001 ? Adapted from: T. R. G. Gray, and S. T. Williams. 1975. Soil Microorganisms, New York: Longman, p. 144. The sum of the various interrelationships of rhizosphere microorganisms and roots can benefit plant growth by influencing the availability of essential nutrients, by producing plant growth regulators, and by suppressing root pathogens. Mineral Cycling by Soil Microorganisms By decomposing plant and animal residues, soil microorganisms release carbon, nitrogen, sulfur, phosphorus, and trace elements from organic mate- rials in forms that can be absorbed by plants. This process, known as mineralization, is the primary source of atmo- spheric carbon dioxide. Without mineralization of organic carbon, the carbon dioxide content of the air, which is essential for plant photosynthesis, would be progressively reduced and plant production would ultimately cease. Main- tenance of the carbon cycle, therefore, is one of the most important biolog- ical processes on earth. Microbial activities similar to those responsible for the carbon cycle also transform soil nitrogen, sulfur, and phosphorus, and to a lesser extent are instrumental in the conversion of other elements. Although particular atten- tion has been directed to microbial transformations of nitrogen, plants also have a nutritional need for sulfur. The microbial transformations of nitrogen and sulfur are much alike because both elements can be oxidized and re- duced. Sulfur reduction is necessary for the synthesis of sulfur-containing

SOIL MICROBES IN PLANT HEALTH AND NUTRITION 49 amino acids. Under anaerobic conditions, sulfur reduction may produce hy- drogen sulfide, which can be harmful to plants. It accumulates in very wet soils, like rice paddies, and can cause straighthead disease of rice and other physiological plant disorders. At low concentrations, however, it can supply the sulfur requirements of some plants. A recent report indicates that oxidation of hydrogen sulfide by a bac- terium in the genus Beggiato a detoxified flooded rice soils. Beggiato a species may be significant in coastal marshes and estuaries as well as in rice paddies, and their capacity to influence plant growth favorably deserves further study. The oxidation of sulfur by bacteria of the genus Thiobacillus is also of poten- tial significance in agriculture. The product of this transformation is sulfuric acid, which can dissolve minerals that otherwise would not be available for plant growth. Farmers who add elemental sulfur to rock phosphate find that phosphorus is liberated more rapidly and in greater amounts than if the sulfur is omitted. The explanation for this is that Thiobacillus species oxidize the sulfur to sulfuric acid, which liberates the phosphorus from the insoluble rock phosphate. Microorganisms are also able to promote phosphorus solubilization by the production of chelators, which form complexes with metal ions and increase their solubility. Acid and chelate production can be easily demonstrated under laboratory conditions, but little is known of the phosphate-dissolving effectiveness of different types of microorganisms under natural soil condi- tions. Solvent action by microorganisms is not restricted to a few species; it is characteristic of many members of the rhizosphere population and can be accomplished in part by plant roots as well. The microbial transformation of nutrient elements other than those cited above is in some instances similar to, and in other instances quite different from, the process just discussed. Un- fortunately, much more is still to be learned about this subject. Microorganisms require many of the same nutrient elements that are essen- tial to plants for their growth. When nitrogen, sulfur, or phosphorus is in short supply, the rhizosphere population will compete with roots for nourish- ment. Because of their abundance, small size, and relatively large surface area, and because they surround the absorbing part of the root, microbes will absorb nutrients at the expense of the plant. Ultimately, plants will display signs of nutrient deficiency and crop yields may decrease. Barber and Martin (1976) have recently found that for barley, 10-20 percent of the photosynthate may be released from roots in nonsterile soil. Less was released in sterile soil. The rhizosphere may exact a price in terms of energy given up to the soil by the plant. There has been speculation that in the rhizosphere oxygen consumption occurs more rapidly than diffusion, so that anaerobic sites may form in places in the root; such reduced conditions could be important in making ferrous ions from ferric, for instance, which increases iron solubility. Wheat roots

so MICROBIAL PROCESSES have high populations of denitrifying bacteria, so oxygen-free conditions must exist in their presence. Microorganisms are prolific producers of vitamins, amino acids, hormones, and other growth-regulating substances. Many bacteria and fungi isolated from soil are able to synthesize compounds that provoke a growth response in plant tissue. Some produce indoleacetic acid or gibberellins, which are hor- mones that control plant growth, while others produce vitamins. Many may also produce unidentified growth factors. Rhizosphere microorganisms are variously credited with promoting increased rates of seed germination, root elongation, root-hair development, nutrient uptake, and plant growth. Inoculation Root uptake of organic compounds has received more attention in We U.S.S.R. than elsewhere, and Russian investigators claim rhizosphere micro- organisms influence the quality as well as quantity of tissue produced by plants. Although there are no experimental results that convincingly establish that growth-promoting substances of microbial origin occur in the rhizo- sphere, speculation persists that such compounds are synthesized in the vicin- ity of roots and affect crop yields. Vanous bacterial fertilizers have been marketed at different times, but commercial preparations known as azotobacterin and phosphobacterin have received the most attention. Azotobacterin is composed of cells of Azoto- bacter chroococcum, a bacterium able, under some conditions, to fix atmos- pheric nitrogen. Phosphobacterin contains the bacterium Bacillus mega- terium var. phosphaticum, which mineralizes organic phosphorus compounds. Russian scientists think that growth of these bacteria in soil will supply plants with nitrogen and phosphorus, but this has not been proved. Treated plants are favorably affected, but growth is not increased by more than 10 percent. Moreover, the effect is said to be due not to nitrogen fixation or phosphorus solubilization, but to plant hormones. Since the benefits are minimal and depend on conditions difficult to con- trol in the field, and the results are unpredictable, bacterial fertilizers are not recommended for general use. Although the potential benefits of inoculating bacteria have not yet been fully explored, it is questionable how much additional exploration may be warranted. Present evidence is insufficient to justify the use of inoculants, other than rhizobia for legumes, to increase crop yields, improve plant quality, or control disease. A beneficial effect is even less likely when the microorga- nism used as inoculum is a normal inhabitant of soil. The British soil micro- biologist S. D. Garrett (1956) has described this problem as follows: [Such] attempts to boost the population of an antagonistic organism by inoculation alone have been doomed to failure from their inception, because

SOIL MICROBES IN PLANT HEALTH AND NUTRITION 51 they are in flagrant contradiction to the ecological axiom that population is a reflection of the habitat, and that any change due to plant introduction without change of the habitat must be a transient one. Mycorrhizal Fungi Most plants, both wild and cultivated, have roots infected with fungi Mat increase nutrient and water uptake and may also protect the root from cer- tain diseases. These infected roots are called mycorrhizae. Although the mycorrhizal fungi probably increase uptake of all the essential elements, they are usually most important in improving phosphorus nutrition. Phosphate is generally present in the soil in low concentrations and it is also highly im- mobile. Strands of fungal hyphae grow out from mycorrhizae and greatly increase the volume of soil from which phosphorus is obtained. So mycor- rhizal plants, in general, can grow and thrive in soils much lower in phosphate and other essential nutrients than a comparable nonmycorrhizal plant. Many plants are so dependent on mycorrhizal fungi for nutrient uptake that they may starve if these fungi are absent. There are a number of types of mycor- rhizae. The two that occur on the most economically important crops, the endomycorrhizae and the ectomycorrhizae, are discussed below. Endomycorrhizae of Crop Plants and Forest Trees Endomycorrhizae of the vesicular-arbuscular (VA) type occur on nearly all crop plants (plants in a few families such as the Cn~ciferae [cabbage, mustard, etc.] and Chenopodiaceae [beets, spinach, etc.] may be nonmycor- rhizal). They also occur on many trees in temperate regions and on the majority of tree species native to the subtropics and tropics. VA mycorrhizal fungi are present in almost all soils and they are not host-specific. Thus, the same fungus producing VA mycorrhizae on trees will form mycorrhizae on plants after land is cleared and planted to agricultural crops. The mycorrhizal condition is normal for most plants, and absence or scarcity of mycorrhizal fungi can greatly limit plant growth (Figure 3. 14. Introduction of mycorrhizal fungi to soil environments lacking or with low populations of such organisms, such as biocide-treated soils, can enhance plant growth. VA mycorrhizae are particularly important for many legumes in that they stimulate nodulation by Rhizobium' thereby increasing nitrogen fixation. Improved phosphorus nutri- tion of the mycorrhizal legume is responsible for increased nodulation. VA mycorrhizal fungi survive in soil as resting spores. They obtain their food from the plant roots and they are unable to grow independently in soil. It is unlikely that they obtain much, if any, organic nutrient from soil. VA fungi have not been grown in pure culture, which presents an obstacle to artificial inoculation. However, these fungi produce the largest spores of

52 MICROBIAL PROCESSES FIGURE 3.1 Endomycorrhizal (left) and nonmycorrhizal (right) peanut plants (ground- nuts). (Photograph courtesy of J. W. Gerdemann) any known fungi, some being 0.5 mm or more in diameter. The spores can be easily extracted from the soil with sieves and then propagated on the roots of living plants. The infected roots can also be used for inoculation. Heavily infected palm roots collected in the wild have been used as a source of inoculum. If field-collected inoculum is used, it is important that it be free of dangerous pathogens. There are situations in which inoculation with VA fungi is highly bene- ficial. If soil is treated with steam or fumigants to kill pathogens, VA fungi are also killed, and considerable time is required for them to become reestab- lished naturally. The nutrient deficiencies and associated stunting that often result may be prevented by inoculating the soil with VA fungi rather than by applying excessive rates of fertilizer. The greatest opportunity for the use of VA fungi is in soils low in available phosphorus, which includes many untreated soils in tropical regions. There is evidence as well that many of these soils also contain less than the optimum number of spores of VA fungi. In such soils inoculation may enable the use of inexpensive rock phosphate fertilizer instead of the more expensive super and triple phosphates. The major obstacle to greater use of VA fungi is the difficulty in obtaining inoculum. However, there are several commercial companies interested in producing pure inoculum, and it may become available in the near future. We are now at the stage where different species of VA fungi should be tested on

SOIL MICROBES IN PLANT HEALTH AND NUTRITION 53 crop plants and forest trees and their effects on growth compared in the field in untreated soils and in soils that have been sterilized. Ectomycorrhizae of Forest Trees Ectomycorrhiza is the second most common type of mycorrhizae. It occurs on roots of pine, spruce, fir, larch, hemlock, willow, poplar, hickory, pecan, oak, birch, beech, and eucalyptus (Figure 3.2). The fungi that form ectomycorrhizae produce mushrooms and puffballs as their reproductive structures (fruit bodies). In North America there are more than 2,100 species of ectomycorrhizal fungi. The fungi are spread in nature by millions of micro- scopic spores, finer than dust, which are released from fruiting bodies and moved great distances by winds. Many forest trees, such as pines, cannot grow beyond the first year with- out an appreciable number of ectomycorrhizae. Ectomycorrhizae benefit trees by: increasing nutrient and water absorption from soil; increasing the tolerance of the tree to drought and extremes of soil conditions (acid levels, toxins, etc.~; increasing the length of the feeder root system; and protecting the fine feeder roots from certain harmful soil fungi. Ectomycorrhizal fungi cannot grow and reproduce unless they are in asso- ciation with the roots of a tree host. These fungi obtain all their essential FIGURE 3.2 Examples of pine ectomycorrhizae. Each different ectomycorrhiza is formed by a different species of fungus. Each main root is approximately 3 cm long. (Photograph courtesy of J. W. Gerdemann)

54 MICROBIAL PROCESSES sugars, vitamins, amino acids, and other foods from their hosts. It is unlikely that these fungi as a group are directly involved in any significant decomposi- tion of forest litter. Certain forest trees, then, must have ectomycorrhizae to survive and grow, and the ectomycorrhizal fungi need their tree hosts to exist. This means that the introduction of tree species as exotics into regions where the appropriate mycorrhizal fungi are absent must be accompanied by the introduction of their natural ectomycorrhizal fungi. In the past, this introduction has been accomplished mainly by using soil collected from under healthy trees with ectomycorrhizae, which is mixed into the upper layer of soil in nurseries. The seedlings planted in this soil usually form abundant ectomycorrhizae in one growing season, and they are then transplanted to the field. Unfortunately, this method is not without risk, since pathogens can be present in the intro- duced soils and cause serious damage to the trees. The logistics of transport- ing large volumes of soil great distances is an added problem. By far the most biologically sound method of correcting an ectomycorrhizal deficiency is by the use of pure cultures of selected species of ectomycorrhizal fungi. In recent years, techniques have been devised to inoculate soil with pure vegetative and spore cultures of Pisolithus tir~ctorius in the United States and to introduce spore cultures of Rhizopogon luteolus onto pine seed and into soil in Australia. These two puffball-producing fungi form ectomycorrhizae on many commercially important forest trees. Currently, research is being done in the United States on the use of a commercially produced vegetative inoculum of P. tinctorius, which should be available at economical prices on the world market in the next few years. Thus far, P. tinctorius appears to enhance growth more than other ectomycorrhizal fungi, and it can be used to tailor-make seedlings to improve the performance of trees even in areas where other ectomycorrhizal fungi are present. Pines with Pisolithus ectomycorrhizae formed in nurseries and planted in forest sites in the southern United States have not only survived, but have grown to twice the heights of comparable pines with naturally occurring ectomycorrhizae. On sites where it is difficult to establish pines, such as those created by strip-mining for coal, the only trees capable of growing are often those that have been inoculated with Pisolithus. The selection and use of specific ectomycorrhizal fungi may well determine whether a productive forest becomes established. The most obvious research need on ectomycorrhizae in developing coun- tries is to determine whether appropriate ectomycorrhizal fungi are present prior to the establishment of forests of introduced species. If such forests are already established or are accessible, then fruit bodies of ectomycorrhizal fungi can be collected and the spores harvested. The puffball fungi usually produce an abundance of easily extractable spores. For example, one fruit body of P. tinctorius may contain 75 grams of spores, and there are more

SOIL MICROBES IN PLANT HEALTH AND NUTRITION 55 than one billion spores in a gram. Spores of P. tinctor~us when kept dry and cool have been stored for more than 4 years without losing their ability to form ectomycorrhizae. The spores can be mixed into nursery soil and the seed of the desired tree species planted. Moderate levels of fertility and at least 2-4 percent organic matter should be maintained in the soil. Usually, the seedlings will have adequate ectomycorrhizae in 6-7 months after seed germination. The production of vegetative cultures of ectomycorrhizal fungi requires aseptic culture technique. This means that the substrate on which the fungi are grown must be sterilized, usually by autoclaving, and maintained free of other microbial contamination for at least several weeks, or until the fungus has produced sufficient growth to overcome contamination. After it has been leached with water, this inoculum can then be added to soil. Some species of ectomycorrhizal fungi are more beneficial to tree growth and development under different soil conditions than others. It is important to select and test different species to determine which are best suited to specific locations. Biological Control of Soil-Borne Pathogens Microorganisms that cause root diseases are sometimes suppressed by other microorganisms in the soil. In many instances disease-causing organisms may be present, but because of naturally occurring biological control, little or no disease results. The prevalence of pathogens may be reduced by crop rotation using a non-host crop, which often starves the pathogen and prevents it from reproducing. It is also possible to increase the level of organisms that are antagonistic to soil-borne plant pathogens. This is generally done not by adding antagonistic microorganisms directly to the soil, but by the use of various organic amend- ments such as manure or plant residues. These amendments provide a source of food for soil-borne microorganisms that can inhibit the development of plant pathogens. Research is needed in order to exploit more fully the use of various forms of organic matter to enhance this biological control of soil- borne pathogens. There have been many attempts to control pathogens in soil by the addi- tion of specific microorganisms. In general, these attempts have failed to increase the level of naturally occurring biological control. For example, soil contains species of fungi that trap and feed on plant parasitic nematodes (Figure 3.39. However, application of additional nematode-trapping fungi failed to protect plants under field conditions. It is likely that unless the soil is altered in some way, it naturally contains the maximum number of nema- tode-trapping fungi that it can support. There is, however, hope that we may

56 MICROBIAL PROCESSES FIGURE 3.3 A nematode-trapping fungus, Dactylella drechsleri, which captures prey on adhesive knobs. (Photograph courtesy of D. Pramer) be on the verge of a major advance in controlling soil-borne pathogens by adding specific microorganisms or by altering the rhizosphere environment. There are a few examples where disease has been reduced by applying a hypovirulent strain or a mutant strain of a pathogen that is incapable of producing disease. Such strains may prevent development of the pathogenic strains. A nonpathogenic strain of the crown gall bacterium will thus protect plants from attack by a pathogenic strain. In soil, most pathogenic fungi must pass through the rhizosphere or must live within this zone. Their success in colonizing or infecting plant roots depends upon their ability to compete with other rhizosphere microorgan- isms. The chemical and microbiological environment in this zone may be altered slightly, but significantly, to effect changes in the inoculum potential of pathogens, either by selections of plant genotypes that produce such changes or by careful regulation of nitrif~cation in soil. Research on biological control should be highly encouraged, for it could provide an alternative means of disease control to the use of expensive and often dangerous pesticides. References and Suggested Readings Alexander, M. 1977. Introduction to soil microbiology. 2nd Edition. New York: John Wiley and Sons.

SOIL MICROBES IN PLANT HEALTH AND NUTRITION 57 . 1974. Microbial ecology. New York: John Wiley and Sons. Baker, K. F., and Cook, R. J. 1974. Biological control of plant pathogens. San Francisco: W. H. Freeman and Company. Barber, D. A., and Martin, I. K. 1976. The release of organic substances by cereal roots into soil. The New Phytologist 76:6 9-80. Barber, D. S. 1968. Microorganisms and the inorganic nutrition of higher plants. Annual Review of Plan t Physiology 19: 71-8 8. Barron, G. L. 1977. The nematode-destroying fungi. Topics in mycobiology No. 1. Guelph, Ontario: Canadian Biological Publications Ltd. Brown, M. E. 1974. Seed and root bacterization. Annual Review of Phytopathology 1 2:1 81-197. ; Hornby, D.; and Pearson, V. 1973. Microbial populations and nitrogen in soil growing consecutive cereal crops infected with take-all. Journal of Soil Science 24(3): 296-3 1 0. Carson, E. W. 1974. The plant root and its environment. Charlottesville: The University Press of Virginia. Cook, R. J. 1977. Management of the associated microbiota. In Plant disease: an ad- vanced treatise in how disease is managed. J. G. Horsfall and E. B. Cowling, eds., pp. 145-166. New York: Academic Press. . 1976. Interaction of soil-borne plant pathogens and other microorganisms: an introduction. Soil Biology and Biochemistry 8:267. Doetsch, R. N., and Cook, T. M. 1976. Introduction to bacteria and their ecobiology. Baltimore, Maryland: University Park Press. Garrett, S. D. 1956. Biology of root-infecting fungi. p. 11. New York: Cambridge Uni- versity Press. 1970. Pathogenic root-infecting fungi. Cambridge, England: Cambridge Univer- sity Press. Gerdemann, J. W. 1975. Vesicular-arbuscular mycorrhizae. In The development and function of roots. J. G. Torrey and D. T. Clarkson, eds., pp. 575-591. New York: Academic Press. Gray, T. P., and D. Parkinson. 1968. The ecology of soil bacteria. Liverpool: Liverpool University Press. , and Williams, S. T. 1975. Soil microorganisms. New York: Longman. Harley, J. L. 1979. Proceedings of the soil-root interface symposium: London: Academic Press. Henis, Y., and Chet, I. 1975. Microbiological control of plant pathogens. Advances in A pplied Microbiology 19: 85 . Hornby, D. 1978. Microbial antagonisms in the rhizosphere. Annals of Applied Biology 89 :97-1 00. Joshi, M. M., and Hollis, J. P. 1977. Interactions of Beggiatoa and rice plants: detoxifica- tion of hydrogen sulfide in the rice rhizosphere. Science 197:179-180. Kleinschmidt, G. D., and Gerdemann, J. W. 1972. Stunting of citrus seedlings in fumi- gated nursery soils related to the absence of endomycorrhizae. Phytopathology 62: 1447-1453. Krasilnikov, N. A. 1958. Soil microorganisms and higher plants. Moscow: Academy of Sciences USSR. English translation, by Y. Halperin, 1961. Jerusalem: Israel Program for Scientific Translations, Ltd. Marks, G. C., and Kozlowski, T. T. 1973. Ectomycorrhizoe: their ecology and physiol- ogy. New York: Academic Press. Marx, D. H. 1977. The role of mycorrhizae in forest production. In Proceedings of the TAPPI (Technical Association of the Pulp and Paper IndustryJ Annual Meeting, February 14-16, 1977, held in Atlanta, Georgia, pp. 151-161. Atlanta: TAPPI. Mosse, B. 1977. Plant growth responses to vesicular-arbuscular mycorrhiza: X. Responses of stylosanthes and maize to inoculation in unsterile soils. New Phytologist 7 8 :277-288. 1977. The role of mycorrhiza in 1eguMe ~utritiol1 OI1 marginal soils. In Exploiting the legume-rhizobium symbiosis in tropical agriculture: Proceedings of a workshop,

58 MICROBIAL PROCESSES University of Hawaii, August 1976, College of Tropical Agriculture Miscellaneous Publication No. 54, pp. 275-292. Honolulu: University of Hawaii. Rovira, A. D.; Newman, F. I.; Bowen, H. J.; and Campbell, R. 1974. Quantitative assess- ment of the rhizoplane microflora by direct microscopy. Soil Biology and Biochem- istry 6:211-216. Sanders, F. E.; Mosse, B.; and Tinker, P. B., eds. 1974. Endomycorrhizas: Proceedings. Symposium on Endomycorrhiza. July, 1974, University of Leeds. New York: Aca- demic Press. Shipton, P. J. 1977. Monoculture and soilborne pathogens. Annual Review of Phyto- pathology 15: 387-407. Smith, A. M. 1976. Availability of plant nutrients in reduced microsites in soil. Annual Reviewof Phytopathology 14:53-73. Tansey, M. R. 1977. Microbial facilitation of plant mineral nutrition. In Microorganisms and minerals, E. D. Weinberg, ea., pp. 343-385. New York: Marcel Dekker, Inc. United Nations Educational, Scientific, and Cultural Organization. 1969. Soil biology: review on research. Natural Resources Research, Series No. 9. Paris: United Nations Educational, Scientific, and Cultural Organization. Distributed in the United States by UNIPUB, New York. Research Contacts Rhizosphere Richard Bartha, Rhizosphere Group, Cook College, Rutgers University, New Brunswick. New Jersey 08903, U.S.A. J. P. Hollis, Department of Plant Pathology, Louisiana State University, Baton Rouge Louisiana 70803, U.S.A. A. D. Rovira, Division of Soils, CSIRO, P.O. Box 2, Glen Osmond, Adelaide, South Australia, 5064. Endomycorrhizae J. W. Gerdemann, Department of Plant Pathology, University of Illinois, Urbana, Illinois 61801, U.S.A. John A. Menge, Department of Plant Pathology, University of California, Riverside, California 92521, U.S.A. Barbara Mosse, Rothamsted Experimental Station, Harpenden, Hertshire AL5 2JQ, Eng- land T; H. Nicolson, Department of Biological Sciences, University of Dundee, Dundee, DD1 4HN, Scotland Ectomycorrhizae Donald H. Marx, Director and Chief Plant Pathologist, Institute for Mycorrhizal Re- search and Development, Forestry Sciences Laboratory, U.S. Department of Agri- culture, Carlton Street, Athens, Georgia 30602, U.S.A. Orson K. Miller, Jr., Department of Biology, Virginia Polytechnic Institute, Blacksburg, Virginia 24061, U.S.A. James M. Trappe, Forest Service, Forestry Sciences Laboratory, U.S. Department of Agriculture, 3200 Jefferson Way, Corvallis, Oregon 97331, U.S.A. Biological Control of Soil-Borne Pathogens R. James Cook, Regional Cereal Disease Research Laboratory, U.S. Department of Agri- culture, Washington State University, Pullman, Washington 99163, U.S.A. Allen Kerr, Department of Plant Pathology, Waite Agricultural Institute, University of Adelaide, Glen Osmond, Adelaide, South Australia, 5064.

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