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MICROBIAL AND RHIZOSPHERE MARKERS OF AIR POLLUTION INDUCED STRESS R.K. Antibus A.E. Linkins III Department of Biology Clarkson University Potsdam, N.Y. 13676 ABSTRACT The rhizosphere is a soil region of intense biological activity and differs significantly from bulk soil in terms of numbers and types of microorganisms. The structural and functional diversity of the rhizosphere is maintained by input of root derived carbon sources. Rhizosphere activity has been shown to exert either positive or negative effects on plant growth through effects on nutrient availability, production of growth regulators or phytotoxic substances, or by suppression of pathogens. Rhizosphere structure and activity has been throughly studied in crop plants grown in agricultural soils; much less is known about rhizospheres of mature trees in forest soils. Research approaches tend to emphasize either: l ~ the isolation, enumeration and identification of rhizosphere species, or 2) the characterization of rhizosphere activities or products. Advantages and disadvantages of the use of such approaches as biomarkers are discussed. Rhizosphere studies under natural conditions are greatly complicated by the high spatial and temporal variability found in soil properties and root development. Air pollutants might influence rhizosphere organisms by: 1 ) affecting plant carbon fixation thus altering carbon availability in the rhizosphere, or 2) through direct effects on soil chemical or physical properties. Research results, obtained largely with potted plants, are available to support both of the above mechanisms. However, the paucity of information does not allow for generalizations about potential rhizosphere biomarkers of pollution induced stress. Long-term data on the occurrence of fruitbodies of ectomycorrhizal fungi in Europe suggest that air pollution may be involved in reducing the species diversity and abundance of these endorhizosphere organisms. Data on acid phosphatase production by field-collected ectomycorrhizae suggest that different fungi may have different functional roles relative to host nutrition. Air pollution induced changes in species composition of tree ectomycorrhizae could potentially affect soil nutrient cycles and tree growth. INTRODUCTION The rhizosphere is considered to be that zone of the soil environment influenced by plant roots. It is widely believed that this zone will be variable in extent and be directly influenced by root physiology and by soil environmental factors. Available evidence suggests that plants and rhizosphere organisms function in an interdependent fashion.

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234 Rhizosphere organisms depend on plants for a continuous supply of reduced carbon and are recognized to play a significant role in nutrient cycling, thus exerting an influence on plant growth. Air pollutants or other stresses which affect carbon fixation may influence rhizosphere populations through an effect on carbon supply; alternatively rhizosphere populations may be influenced by direct effects of air pollutants on the soil environment. Changes in rhizosphere structure or function would in turn affect nutrient cycling and exert a feedback effect on plant growth. Much of what is presently known about rhizosphere structure and function has been obtained by using crop plants grown in agricultural soils and caution should be used in extrapolating these results to forest ecosystems. RHIZOSPHERE STRUCTURE AND MAINTENANCE Numerous studies have shown that bacterial numbers are greatly increased in rhizosphere soils. Dilution plate counts indicate that the ratio of bacterial numbers in rhizosphere compared to nonrhizosphere soil varies from 10:1 - 50:1 (Richards 1987~. Numbers of fungi are also increased in rhizosphere compared to nonrhizosphere soil; however, the magnitude of this increase is often smaller than observed for bacteria. Comparison of rhizosphere and nonrhizosphere soils indicate that significant qualitative shifts occur in the bacterial and fungal species detected (Gerhardson and Clarholm 1986~. Rhizosphere species composition is influenced by numerous factors, including plant species and genotype, plant nutrient status, presence and type of mycorrhizae, soil type, soil moisture, light supply and other factors. The continued maintenance of a "normal" rhizosphere is mediated by the release of a wide variety of organic carbon compounds. Available data, obtained from crops and tree seedlings, suggest that 40-50 oh of the net carbon fixed may be exuded or rapidly released to the rhizosphere (Perry et al. 1987), more complex carbon compounds may enter the rhizosphere more slowly resulting from root aging. The rhizosphere contains a diverse array of metabolic substrates such as exudates, secretions, plant mucilages, mucigel, and lysates (Rovira et al. 1979~. The diversity and complexity of released compounds is likely to be an important factor contributing to the high species diversity of rhizosphere microorganisms. Attempts to describe the rhizosphere have emphasized the spatial locations of organisms within the root zone. Whipps and Lynch ( 1986) recognized three regions supporting microbial growth: endorhizosphere organisms live within the root, rhizoplane organisms live on the root surface, and ectorhizosphere organisms inhabit a zone around the root. The terms mycorrhizosphere and mycosphere have also been applied to the zones associated with mycorrhizae and fungal hyphae respectively. Although such regions and their component species may be difficult to characterize operationally, such a classification has heuristic value. Microorganisms can be envisioned as existing along a gradient in terms of plant and soil influences. Endorhizosphere species are in contact with the plant and have direct access to reduced carbon. Organisms in distal portions of the ectorhizosphere will be more directly influenced by soil factors. We would expect organisms to show metabolic adaptations to the resources available in their surroundings. Our inability to grow vesicular-arbuscular (VA) fungi in pure culture and the limited capacities for complex carbohydrate utilization demonstrated by ectomycorrhizal (ECM) fungi suggest that endorhizosphere species are adapted to root supplied carbon (Harley and Smith 1983~. Rhizosphere bacterial isolates demonstrate growth and amino acid utilization patterns suggesting adaptation to root products. Air pollutants affecting tree carbon fixation or allocation patterns have potential to influence rhizosphere organisms; however, our knowledge of these effects in forest species is limited.

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235 RHIZOSPHERE FUNCTIONS Rhizosphere organisms may exert either positive or negative effects on plant growth. These effects are determined by the rhizosphere's capacity to: 1 ) influence nutrient availability, 2) produce plant growth regulators or phytotoxic compounds, or 3) suppress pathogenic organisms. A complex set of microbial interactions determines the structure of the rhizosphere community, these include: antagonism, commensalism, parasitism, and predation. Bacteria may exhibit inhibitory or stimulatory effects on the formation of mycorrhizal associations, which in turn affect plant growth and mineral nutrition (Bowen and Theodorou 1979~. Formation of various types of mycorrhizae can subsequently produce quantitative and qualitative alterations in rhizosphere bacteria and fungi (Katzoelson et al. 1962, Meyer and Linderman 1986~. These changes observed in rhizosphere composition may be mediated by a diverse array of metabolites produced by rhizosphere organisms (Lynch 1987~. Nye and Tinker (1977) listed the mechanisms by which rhizosphere organisms might influence plant nutrient availability, including alterations in root morphological and physiological properties, effects on phase equilibria of soil nutrients, effects of soil chemical composition and organic matter mineralization, direct transfer of nutrients, and competition for soil nutrients. Potentially favorable effects on root morphology and respiration have been obtained with several rhizosphere bacteria on crop plants (Hades and Okon 1987~. Work with vesicular-arbuscular suggests that the increased surface area provided satisfactory explanation for observed increases in phosphate. Under natural conditions, however, the organisms such as nitrogen fixers and hyphal _ composition and nutrient cycling (Coleman 1985~. species under controlled conditions by extramatrical hyphae provides a uptake of immobile nutrients like situation becomes more complex and Brazers will influence rhizo~nh~r~ Some workers have suggested that root and rhizosphere phosphatases and phosphate solubilizing bacteria may contribute to P nutrition under field conditions. Recent studies (Tarafdar and Jungk 1987, Kroehler and Linkins 1988) suggest that root surface and rhizosphere phosphatase activities will hydrolyze organic phosphorus forms at rates sufficient to meet plant needs. These studies do not imply a necessary role for rhizosphere organisms, however. Ectomycorrhizae are the most common form of mycorrhizae on many important temperate tree species and can increase the uptake of macronutrients (Harley and Smith 1983~. Ectomycorrhizal fungi alter root morphology, and control the movement of nutrients from rhizosphere to plant by surrounding plant roots with a fungal sheath. Phosphatases produced by ECMs are active against a variety of organic phosphate sources found in forest soils (Bartlett and Lewis 1973) and likely play key roles in phosphorus cycling. We have shown that ECMs formed by different fungi exhibit different levels of phosphatase activity (Antibus et al. 1981~. Activity appears to vary seasonally for a given host-fungus combination (Antibus and Linkins, unpublished data), and we feel that phosphatase activity reflects the general physiological activity of ECMs at given times. Further research could determine the efficacy of using phosphatases or other enzyme assays as general indicators of root and rhizosphere activity. It may also be possible to use ratios of enzymes such as the ratio of acid alkaline phosphatases to determine the relative contributions of bacteria to rhizosphere enzyme activity. EXPERIMENTAL APPROACHES Rhizosphere workers usually attempt either to dissect the rhizosphere and study the workings of its components or to examine the physiology of the intact zone. Studies of the former type emphasize isolation, quantification and identification of rhizosphere organisms, whereas the latter type emphasize the measurement of specific rhizosphere

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236 activities or products. Both approaches are valid, but are subject to numerous limitations and drawbacks. Techniques employed in the dissection and study of the rhizosphere include procedures such as plate counting, enrichment cultures, end-point dilutions, direct visualization and many others. These have the advantage of allowing identification of specific organisms or groups of organisms. However, the selective nature of isolation techniques has led to severe criticisms (Brock 1987~. Direct visualization procedures overcome some of these limitations but often do not allow identification. The use of fluorescent antibodies may permit identification, but requires increased technical expertise. Another technically complex but potentially useful method to study populations of specific rhizosphere bacteria involves the use of specific DNA probes (Holben et al. 1988~. Biomass estimates suffer from difficulties in separating live and dead organisms, or from an inability to separate various specific groups of organisms. The use of biochemical markers specific to certain species or functional groups may allow the in situ estimation of rhizosphere organisms (Pace et al. 1986~. One such study has been conducted with rhizosphere bacteria under greenhouse conditions (Tumid et al. 1985~. The application of specific biochemical markers requires a thorough knowledge of biochemistry, technical expertise and elaborate equipment. Workers attempting to understand the physiological aspects of the rhizosphere have examined such processes as nitrogen fixation or enzyme activities in the root and surrounding soil. A disadvantage of these studies is that the key organisms involved in the process of interest are usually not identified. These techniques may thus fail to detect perturbation-induced population shifts which buffer against physiological change. Enzyme studies offer the advantage of studying processes, such as nutrient mineralization, which are crucial to plant growth. The procedures are sensitive and assays are easy to perform using commonly available equipment. Because enzyme assays are integrated measures, they demonstrate less variability than microbial counts (Burns 1978~; however, they may also demonstrate time delays in response to perturbations. Rhizosphere characteristics change over extremely short distances making study of this soil region difficult. In addition to methodological difficulties mentioned, interpretation of results under natural conditions is complicated by a high amount of spatial and temporal variability in root growth and soil properties. AIR POLLUTION EFFECTS Air pollutants might affect rhizosphere activity by plant mediated effects or through direct effects on the soil environment. Using pine seedlings Luxmoore et al. (1986) showed that carbon dioxide enrichment resulted in plant-induced decreases in rhizosphere pH and increased solubility of certain cations. Firestone et al. (1984) found the effects of simulated acid precipitation on rhizosphere composition resulted from an influence on root characteristics rather than changes in soil properties. In this study solubilization of cations by acid precipitation was an important factor affecting bulk soil microorganisms, and various pollutants can, under controlled conditions, affect bulk soil microbiology, soil processes and enzyme acitivities (Wilke 1987~. Dighton et al. (1986) found numbers of root tips and types of ECMs formed on Pinus sylvestris were affected when seedlings were grown in soils previously exposed to artificial acid rain for 5 years. Evidence based on production of fruitbodies of known ECM fungi strongly suggests that the mycorrhizal fungus flora of the Netherlands has changed in the last 80 years. It has been suggested that fruitbody productivity has decreased because of air pollution-induced stress of the host species Pinus sylvestris (Termorshuizen and Schaffers 1987), and that ECM species

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237 frequency and diversity have been reduced through air pollution induced changes in soil chemistry (Arnolds 1988~. The latter study indicates that some species may have been lost completely from the fungal flora. These data, and work by Haselwandter et al. ( 1988) on radiocaesium accumulation in fruitbodies, suggest that the occurrence of ECM fungi may provide a valuable and easily obtained record of the effects of air pollution on the endorhizosphere of ECM tree species. Unfortunately, little data of a mycosociological nature are available for North American forests. Our work (Fig. 1 ) shows that naturally occurring ECM morpho-types formed by several species of ECM fungi produce significantly different acid phosphatase activities and may exert differential influences on organic phosphorus mineralization. Data on fruitbody occurrence suggest that ECM populations in Europe have changed; a concomitant shift in mycorrhizal root tips would likely influence enzyme production and rhizosphere composition. Shifts in the relative abundance of these morpho-types, whether due to air pollution effects on trees or soils, could affect phosphorus cycling and other soil processes. Alternatively, changes in soil properties might result in ecotypic differentiation. Woolhouse ( 1969) showed that ecotypes of plants growing on metal-contaminated soils produced acid phosphatases differing in susceptibility to cation inhibition; the development of such changes in ECM fungi might serve as a marker of air pollution-induced changes in forest soils. 130 A, 110 =~_ 90 o 3 70 50 30 10 ~ oWR - ~YB - C G 1 1 2 3 4 5 6 7 8 Time (hrs) Figure 1. Acid phosphatase activity of field-collected Douglas fir ectomycorrhizal morphotypes: WR - white rhizomorph producer, YB - yellow brown smooth type and CG- Cenococcum geophilum. Assays were conducted at 25C in pH 5.0 citrate buffer. Values are means with standard deviation bars (n=5~.

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238 A review of available literature indicates that air pollutants can affect structure and function of tree rhizospheres. These effects may relate to changes in root supplied carbon or changes in soil environment. Too few data are available to suggest that any particular rhizosphere organisms or functions may serve as a simple biomarker of pollution induced stress. We suggest that the measure of root and rhizosphere enzyme activities can provide a simple and useful approach to the study of air pollution effects on rhizosphere physiology. be interpreted in terms of tree growth. However, such information on the function of rhizosphere organisms is crucial if we are to understand the significance of air pollution effects on the occurrence of rhizosphere organisms. More data will be needed before rhizosphere physiology can SUMMARY - The rhizosphere is an area of intense biological activity driven by root-derived carbon. - Rhizosphere activity may exert positive or negative influences on plant growth through effects on nutrient availability, production of growth regulators or phytotoxic substances, or by suppression of pathogens. Most of what is known about rhizosphere effects comes from studies of crop plants in agricultural soils. - Air pollutants might influence rhizosphere structure or function by effects on plant carbon fixation or allocation, or by direct effects on the soil environment. Evidence to support both mechanisms is available. - Rhizosphere studies usually emphasize either: 1 ) isolation, enumeration and identification of component species, or 2) the characterization of activities or products. The former approach would allow detection of air pollution-induced shifts in key rhizosphere organisms, whereas the latter would detect shifts in important rhizosphere processes. Advantages and limitations of these approaches are discussed. -Potentially useful approaches to rhizosphere study using techniques from molecular biology are appearing; however, these often require technical expertise and sophisticated equipment. - The study of the response of the rhizosphere under natural conditions is complicated by great spatial and temporal variability in soil properties and root development. - Occurrence and composition of ectomycorrhizal fruitbodies could potentially serve as a biomarker in forests of ECM trees. Studies of ECM fruitbody occurrence in the Netherlands suggest that air pollution has reduced the frequency and diversity of these endorhizosphere organisms. -ECMs formed by different fungi on a single tree species can demonstrate significantly different acid phosphatase activities. Shifts in ECM species composition in relation to air pollution could potentially affect forest soil nutrient cycles.

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239 REFERENCES Antibus, R.K., J.G. Croxdale, O.K. Miller, and A.E. Linkins. 1981. Ectomycorrhizal fungi of Salix rotundifolia Trautv. III. The surface phosphatase activities of resynthesized mycorrhizal complexes. Can. J. Bot. 59:2458-2465. Arnolds, E. 1988. The changing macromycete flora in the Netherlands. Trans. Br. Mycol. Soc. 90:391-406. Bartlett, E.M., and D.H. Lewis. 1973. Surface phosphatase activity of mycorrhizal roots of beech. Soil Biol. Biochem. 5:249-257. Bowen, G.D., and C. Theodorou. 1979. Interactions between bacteria and ectomycorrhizal fungi. Soil Biol. Biochem. 11:119- 126. Brock, T.D. 1987. The study of microorganisms in situ: progress and problems. Pp. 1 - 17 in Ecology of microbial communities, M. Fletcher, T.R.G. Gray and J.G. Jones~eds.~. Cambridge University Press, Cambridge. Burns, R.G. 1978. Enzyme activity in soil some theoretical and practical considerations. Pp. 295-340 in Soil enzymes, R.G. Burns (ed.~. Academic Press, New York. Coleman, D.C. 1985. Through a ped darkly: an ecological assessment of root-soil- microbial-faunal interactions. Pp. 1 -21 in Ecological interactions in soil, A.H. Fitter (ed.~. Blackwell, Oxford. pp. 1-21. Dighton, J., R.A. Skeffington, and K.A. Brown. 1986. The effects of sulfuric acid (pH 3) on roots and mycorrhizas of Pin?vs sylvestris. Pp. 739-743 in Physiological and genetical aspects of mycorrhizae, V. Gianinazzi-Pearson and S. Gianinazzi (eds.~. INRA, Versailles. pp. 739-743. Firestone, M.K., J.G. McColl, K.S. Killham, and P.D. Brooks. 1984. Microbial response to acid deposition and effects on plant productivity. Pp. 51 -63 in Direct and indirect effects of acid deposition on vegetation. R.A. Linthurst. Butterworth, Stoneham, MA. Gerhardson, B., and M. Clarholm. 1986. Microbial communities on plant roots. Pp. 19-34 in Microbial communities in soil, V. Jensen, A. Kjoller and L.H. Sorensen (eds.~. Elsevier, New York. Hadas, R., and Y. Okon. 1987. Effect of Azospirillum brasilense inoculation on root morphology and respiration in tomato seedlings. Biol. Fertil. Soils 5:241 -247. Harley, J.L., and S.E. Smith. 1983. Mycorrhizal symbiosis. Academic Press, New York. Haselwandter, K., M. Berreck, and P. Brunner. 1988. Fungi as bioindicators of radiocaesium contamination: pre- and post- Chernobyl activities. Trans. Br. Mycol. Soc. 90:171-174. Holben, W.E., J.K. Jansson, B.K. Chelm, and J.M. Tiedje. 1988. DNA probe method for the detection of specific microorganisms in the soil bacterial community. Appl. Environ. Microbiol. 54:703-711.

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240 Katznelson, H., mycorrhizal 40:377-382. J.W. Rouatt, and E.A. Peterson. 1962. The rhizosphere effect of and non-mycorrhizal roots of yellow birch seedlings. Can. I. Bot. Kroehler, C.J., and A.E. Linkins. 1988. The root surface phosphatases of Eriophorum vaginatum: Effects of temperature, pH, substrate concentration and inorganic phosphorus. Plant Soil 105:3-10. Luxmoore, R.J., E.G. O'Neill, J.M. Ellis, and H.H. Rogers. 1986. Nutrient uptake and growth responses of Virginia pine to elevated atmospheric carbon dioxide. J. Environ. Qual. 15:244-251. Lynch, J.M. 1987. Biological control within microbial communities of the rhizosphere. Pp. 55-82 in Ecology of microbial communities, M. Fletcher, T.R.G. Gray and J.G. Jones (easy. Cambridge University Press, Cambridge. Meyer, J.L., and R.G. Linderman. 1986. Selective influence on populations of rhizosphere or rhizoplane bacteria and actinomycetes by mycorrhizas formed by Glomus fasiculatum. Soil Biol. Biochem. 18:191-196. Nye, P.H., and P.B. Tinker. 1977. Solute movement in the soil-plant system. Blackwell, Oxford. Pace, N.R., D.A. Stahl, D.~. Lane, and G.J. Olsen. 1986. The analysis of natural microbial populations by ribosomal RNA sequences. Pp 1-55 in Advances in microbial ecology. Vol. 9, K.C. Marshall (ed.~. Plenum Press, New York. Perry, D.A., R. Molina, and M.P. Amaranthus. 1987. Mycorrhizae, mycorrhizospheres, and reforestation: current knowledge and research needs. Can. J. For. Res. 17:929-940. Richards, B.N. 1987. The microbiology of terrestrial ecosystems. Longman, Essex. Rovira, A.D., R.C. Foster, and J.K. Martin. 1979. Origin, nature and nomenclature of the organic materials in the rhizosphere. Pp. 1-4 in The soil-root interface, I.L. Harley anc! R.S. Russell (eds.~. Academic Press, New York. Tarafdar, J.C., and ~ A. Jungk. 1987. Phosphatase activity in the rhizosphere and its relation to the clepletion of soil organic phosphorus. Biol. Fertil. Soils 3:199-204. Termorshuizen, A.~., and A.P. Schaffers. 1987. Occurrence of carpophores of ectomycorrhizal fungi in selected stands of Pinus sylvestris in the Netherlands in relation to stand vitality and air pollution. Plant Soil 104:209-217. Tunlid, A., B.H. Baird, M.B. Trexler, S. Olsen, R.H. Findlay, and D.C. White. 1985. Determination of phospholipid ester-linked fatty acids and poly beta- hydroxybutyrate for estimation of bacterial biomass and activity in the rhizosphere of the rape plant Brassica napus L. Can J. Microbiol. 31:1113-1119. Whipps, J.M., and J.M. Lynch. 1986. The influence of the rhizosphere on crop productivity. Pp. 187-244 in Advances in microbial ecology, Vol. 9, K.C. Marshall (ed.~. Plenum Press, New York.

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241 Wilke, B.M. 1987. Fluoride-induced changes in chemical properties and microbial activity of mull, moder and mor soils. Biol. Fertil. Soils 5:49-55. Woolhouse, H.W. 1969. Differences in the properties of the acid phosphatases of plant roots and their significance in the evolution of edaphic ecotypes. Pp. 357-380 in Ecological aspects of the mineral nutrition of plants, I.H. Rorison (ed.~. Blackwell, Oxford.

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240 Katznelson, H., mycorrhizal 40:377-382. J.W. Rouatt, and E.A. Peterson. 1962. The rhizosphere effect of and non-mycorrhizal roots of yellow birch seedlings. Can. I. Bot. Kroehler, C.J., and A.E. Linkins. 1988. The root surface phosphatases of Eriophorum vaginatum: Effects of temperature, pH, substrate concentration and inorganic phosphorus. Plant Soil 105:3-10. Luxmoore, R.J., E.G. O'Neill, J.M. Ellis, and H.H. Rogers. 1986. Nutrient uptake and growth responses of Virginia pine to elevated atmospheric carbon dioxide. J. Environ. Qual. 15:244-251. Lynch, J.M. 1987. Biological control within microbial communities of the rhizosphere. Pp. 55-82 in Ecology of microbial communities, M. Fletcher, T.R.G. Gray and J.G. Jones (easy. Cambridge University Press, Cambridge. Meyer, J.L., and R.G. Linderman. 1986. Selective influence on populations of rhizosphere or rhizoplane bacteria and actinomycetes by mycorrhizas formed by GIomus fasiculatum. Soil Biol. Biochem. 18:191-196. Nye, P.H., and P.B. Tinker. 1977. Solute movement in the soil-plant system. Blackwell, Oxford. Pace, N.R., D.A. Stahl, D.~. Lane, and G.J. Olsen. 1986. The analysis of natural microbial populations by ribosomal RNA sequences. Pp 1-55 in Advances in microbial ecology. Vol. 9, K.C. Marshall (ed.~. Plenum Press, New York. Perry, D.A., R. Molina, and M.P. Amaranthus. 1987. Mycorrhizae, mycorrhizospheres, and reforestation: current knowledge and research needs. Can. J. For. Res. 17:929-940. Richards, B.N. 1987. The microbiology of terrestrial ecosystems. Longman, Essex. Rovira, A.D., R.C. Foster, and J.K. Martin. 1979. Origin, nature and nomenclature of the organic materials in the rhizosphere. Pp. 1-4 in The soil-root interface, I.L. Harley anc! R.S. Russell (eds.~. Academic Press, New York. Tarafdar, J.C., and ~ A. Jungk. 1987. Phosphatase activity in the rhizosphere and its relation to the clepletion of soil organic phosphorus. Biol. Fertil. Soils 3:199-204. Termorshuizen, A.~., and A.P. Schaffers. 1987. Occurrence of carpophores of ectomycorrhizal fungi in selected stands of Pinus sylvestris in the Netherlands in relation to stand vitality and air pollution. Plant Soil 104:209-217. Tunlid, A., B.H. Baird, M.B. Trexler, S. Olsen, R.H. Findlay, and D.C. White. 1985. Determination of phospholipid ester-linked fatty acids and poly beta- hydroxybutyrate for estimation of bacterial biomass and activity in the rhizosphere of the rape plant Brassica napus L. Can J. Microbiol. 31:1113-1119. Whipps, J.M., and J.M. Lynch. 1986. The influence of the rhizosphere on crop productivity. Pp. 187-244 in Advances in microbial ecology, Vol. 9, K.C. Marshall (ed.~. Plenum Press, New York.

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The Workshop Papers Biochemical/Cell-Tissue Session

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