Assessment of Allelopathy Among Microbes and Plants - ACS

Chapter 45

Assessment of Allelopathy Among Microbes and Plants L. F. Elliott and H. H. Cheng

Downloaded by UNIV LAVAL on July 12, 2016 | http://pubs.acs.org Publication Date: January 8, 1987 | doi: 10.1021/bk-1987-0330.ch045

Agricultural Research Service, U.S. Department of Agriculture, and Washington State University, Department of Agronomy and Soils, Pullman, WA 99164

Allelopathic effects of microbes on plants, whether due to direct production of toxins by the microbes or to toxic molecules produced during microbial decomposition of organic residues, have been difficult to prove. The problem can be related to difficulties in characterizing and incorporating environmental factors regulating the allelopathic relationship such as soil water, and temperature. The need to follow production of allelopathic compounds and mechanisms of synthesis, fate of the allelochemicals in the soil, their uptake by and specific damage to the plant, and reisolation of the allelochemicals or their breakdown products in the plant makes the task of establishing allelopathic mechanisms difficult. Yet, complete knowledge of all these processes is essential for assessment of allelopathy among microbes and plants. Two cases are presented to examine the allelopathic potential of toxins from decomposing crop residues and the role of microbial root colonizers that produce toxins. There are numerous reports describing the allelopathic (phytotoxic) effects of microbial products on crop growth, particularly in conjunction with heavy residues from the previous crop (1-5). The cause of the reduced crop growth has been attributed to the production of a variety of toxic compounds such as phenolic acids, shortchain fatty acids, patulin, and many others (6-9). These compounds may be produced directly or indirectly during the microbial decomposition of organic residues under varying environmental conditions, such as when the soil remains wet over an extended period of time. As moisture becomes more limiting to a cropping system, microbialassociated allelopathic problems generally decrease (10). Allelopathic problems have been especially troublesome with conservation tillage systems (6,7,9). An example is the reduced growth of winter wheat when i t is direct-drilled into stubble (Figure 1). In the heavy residues (left), the plants grew poorly, 0097-6156/87/0330-0504$06.00/0 © 1987 American Chemical Society

Waller; Allelochemicals: Role in Agriculture and Forestry ACS Symposium Series; American Chemical Society: Washington, DC, 1987.


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Among Microbes

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but where residues were low ( r i g h t ) , the plants grew very w e l l . Conservation t i l l a g e practices are defined here as d i r e c t - d r i l l i n g of seeds into the surface residues of previous crops ( n o - t i l l ) or as shallow incorporation of crop residue into the s o i l with a s i g n i f i cant portion s t i l l remaining on the s o i l surface (stubble-mulch). The purpose of maintaining residues at or near the s o i l surface i s to protect the s o i l from water and wind erosion. Conservation t i l lage cropping practices are e s s e n t i a l for protection of erodible croplands, for maintenance of s o i l p r o d u c t i v i t y , and for reducing o f f - s i t e damage that leads to deposition of s o i l on land away from the land where erosion occurred. Unfortunately, common conservation t i l l a g e practices are not always compatible with e f f i c i e n t crop production practices and often r e s u l t i n poor crop growth (6,7). In many cases the poor crop growth has been attributed to phytotoxicity (allelopathy) caused by the production of toxic chemicals during microbial decomposition of residues (4,11,12,13). Other problems appear to be associated with microbes that are carried on residues and then colonize plant roots, causing reduction i n plant growth (14,15). While some of these organisms appear to be minor pathogens, those mentioned by E l l i o t t and Lynch (15) i n h i b i t winter wheat growth by colonizing the root surface and producing a toxin that adversely affects the plant without r e a d i l y v i s i b l e root damage (16,17). The d i f f i c u l t y i n a l l e l o p a t h i c studies has been to l i n k the ^ allelochemicals d i r e c t l y with the plant growth problems. Before the r o l e of crop residue, s o i l management, or other practices i n a l l e l o pathic problems can be evaluated, a d i r e c t l i n k must be established between the source or production of the chemicals and plant damage. Plant damage may be caused by the chemicals produced from residue decomposition or from the microorganisms residing i n the residues. Chemicals Crop Residue

Plant Damage ^Microorganisms or microbial toxins

Two cases w i l l be presented to i l l u s t r a t e the d i f f i c u l t y i n establ i s h i n g allelopathy and i n l i n k i n g the agent to poor crop growth. S p e c i f i c a l l y , the role of phenolic acids and the r o l e of t o x i n producing pseudomonads colonizing wheat roots w i l l be examined. Other cases concerning the d i r e c t and i n d i r e c t effects of a l l e l o chemicals such as acetic acid produced during crop residue decompos i t i o n are presented i n t h i s symposium by J . M. Lynch. The emphasis of t h i s discussion w i l l not be a review of existing l i t e r a t u r e , but on establishing a conceptual framework for a r e a l i s t i c assessment of the a l l e l o p a t h i c phenomena and the r o l e and fate of allelochemicals i n the s o i l . Phenolic Acids Phenolic acids have been implicated i n a l l e l o p a t h i c problems for some time (1,5). There i s s u f f i c i e n t evidence i n the l i t e r a t u r e to



506

ALLELOCHEMICALS: ROLE IN AGRICULTURE AND FORESTRY

b u i l d a strong linkage between phenolic acids and plant damage observed under conservation t i l l a g e . Evidence for considering the phenolic acids as allelochemicals can be summarized i n the following sequence of observations: (a) Plant damage i s observed i n the presence of heavy crop residues i n the f i e l d , such as under the conditions of conservation t i l l a g e ; (b) phenolic acids are produced during the decomposition of crop residues; (c) phenolic acids are found i n s o i l extracts; and (d) phenolic acids can cause plant damage. A number of phenolic acids have been i d e n t i f i e d i n the s o i l (1.3), including f e r u l i c , jp-coumaric, v a n i l l i c , s y r i n g i c , and _p-hydroxybenzoic acids. I n h i b i t i o n of plant growth by these and other phenolic acids has been demonstrated i n nutrient solution studies (e.g. 18.19). However, when the effects of phenolic acids on seed germination and seedling growth were tested i n s o i l , no i n h i b i t i o n was observed even when the amounts of phenolic acids applied were much greater than the amounts normally detectable i n the s o i l (20). This lack of observed allelopathy i n the presence of phenolic acids i n s o i l could have been due to several reasons. Phenolic acids may not be a problem i n s o i l or may only be a problem i n s o i l s where they are not inactivated. Inactivation could be chemical or b i o l o g i c a l . Phenolic acid allelopathy may only be a problem when portions of the seedling or plant are i n intimate contact with the decomposing residues and the chemicals are transferred d i r e c t l y from the residue to the plant with limited or no contact with s o i l . Direct evidence l i n k i n g phenolic acids and phytotoxicity under f i e l d conditions or simulated f i e l d conditions has been d i f f i c u l t to obtain. One problem i s that much of our information on the effect of phenolic acids i s based on extracts from plant material. As Fisher (21) has pointed out: " I t seems u n l i k e l y that the a l l e l o p a t h i c chemicals that may be extracted from plant material are actually those that reach the host plant, yet nearly a l l our information on a l l e l o p a t h i c compounds i s derived from extracts that have never been exposed to the soil.** To prove a d i r e c t linkage between phenolic acids and plant damage, information i s needed on the dynamics of phenolic acid production, the processes regulating t h e i r presence i n s o i l s o l u t i o n , and the mechanism of t h e i r uptake by the plant. An assessment of the rates and duration of phenolic acid production from a residue i s an important f i r s t step. Laboratory and f i e l d studies for assessing the dynamics of phenolic acid production must include considerations of the nature of the residue, s o i l properties, nutrient status of the system, microbial biomass i n t e r r e l a t i o n s h i p s , temperature, moisture, residue placement i n or on the s o i l , and other factors that relate to the f i e l d . S o i l properties i n the f i e l d are e s p e c i a l l y important when organic residues are incorporated. When s o i l s are wet, such as those with more than -0.02 MPa water p o t e n t i a l , oxygen d i f f u s i o n i s impeded and anaerobic conditions p r e v a i l , especially i n s o i l s that are high i n clay content. Under these circumstances, microbial byproducts change dramatically and one r e s u l t , for example, i s an increase i n the production of phenolic acids. Phenolic acid production i s also affected by temperature (22) and s o i l f e r t i l i t y status (23). While the C : N r a t i o of an organic residue may influence the rate of i t s decomposition and, hence, the rate of phenolic acid production, the



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r e a d i l y available C and Ν content of the residue may have a more d i r e c t bearing on the decomposition rate (24). Most studies have been aimed at the i d e n t i f i c a t i o n of the various phenolic acids produced; however, more attention w i l l now be needed to assess how much and for how long a period these phenolic acids are produced and how changing environmental and f i e l d conditions affect production of these compounds. Once the phenolic acids are produced and present i n the e n v i ronment, p h y s i c a l , chemical, and microbiological interactions w i l l occur. These processes and reaction rates should be defined. The phenolic acids i n s o i l solution can be adsorbed onto s o i l p a r t i c l e s . However, one should examine t h i s adsorption process with care. Adsorption processes have often been characterized by using a batch e q u i l i b r a t i o n method. Many such studies did not examine whether the adsorption process was reversible. The adsorption of many phenolic acids i s actually much more complicated than that depicted by the batch e q u i l i b r a t i o n method. A number of binding mechanisms may be involved, including hydrogen bonding, ligand exchange, and complex formation. These compounds can also react chemically with s o i l constituents. For instance, recent studies (25) have demonstrated that Fe and Mn oxides can r e a d i l y oxidize phenolic acids and cause t h e i r immobilization i n s o i l . This reaction cannot be r e a d i l y reversed. In addition to chemical reactions, microorganisms can degrade phenolic acids to CO2 and H2O or p a r t i a l l y degrade them to meta b o l i c products that may also be a l l e l o p a t h i c (26). More important than the mode of degradation of these compounds are the environ mental and s o i l conditions under which these compounds are degraded. Factors such as s o i l properties, nutrient status, microbial biomass, temperature, and moisture affect the dynamics of decomposition. In addition to the processes of degradation, processes that transport the compounds from the s i t e of production, such as leaching by water or v o l a t i l i z a t i o n into the atmosphere, w i l l also affect the concen t r a t i o n of these phenolic acids i n s o i l s o l u t i o n . The rate of move ment and transformation of phenolic acids i n the s o i l w i l l determine what influence these compounds have on the vegetation i n the vicinity. The mere presence of phenolic acids i n s o i l solution under conditions that have resulted i n allelopathy does not conclusively prove that these compounds are the causative agents. Commonly, a l l e l o p a t h i c studies involving phenolic acids have focused either on i s o l a t i n g the acids from areas of poor plant growth i n the f i e l d by using rigorous extractants or on observing plant growth i n h i b i t i o n i n the presence or absence of phenolic acids added to a growth medium. These approaches do not indicate how the plant i s damaged or i f the added or extracted compounds are taken up by the plant. I t i s necessary to provide evidence that these compounds are taken up by the plants and that damage to the plants can be d i r e c t l y associated with the presence of these compounds i n plant tissues or organs. Tracer-labeled phenolic acids can best serve these i n v e s t i gations. Several c r u c i a l questions must be answered i n order to derive a r e a l i s t i c assessment of plant damage and, furthermore, to devise means to a l l e v i a t e such damage i n the f i e l d . For instance, does damage occur at or on the root surface, or i s the chemical(s)



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taken into the plant? What are the uptake kinetics? Are the effects of different phenolic acids, when present together, additive or synergistic? Evidence has shown that the effects of short-chain fatty acids on plants are synergistic (27). Moreover, are the breakdown products of phenolic acids toxic to the plant and, i f so, what are the uptake rates, uptake mechanisms, and modes of action of these metabolites? Knowledge of how these chemicals are taken up by the plant and the mechanism of action w i l l help i n designing f i e l d studies to demonstrate how phenolic acids i n s o i l solution and plant damage are linked. The requirements for establishing d i r e c t linkage between phenolic acids and plant damage can be depicted i n a flow diagram (Figure 2). This diagram provides a conceptual framework of the relationships among the input factors and processes affecting the outcome. Before phenolic acids can be linked to plant damage, the whole gamut of processes from production to transformations and uptake must be assessed under proper conditions of temperature, moisture, s o i l conditions, nutrient status, and microbial a c t i v i t i e s . When such a mechanistic model i s i n place, allelopathy can then be predicted by measurement of a few key factors. A l l e l o p a t h i c Wheat Root Colonizers Bacteria that are not considered true pathogens but do cause d e t r i mental changes i n the plant when they colonize the roots are receiving attention. In t h e i r work with deleterious rhizobacteria isolated from sugar beets i n the f i e l d , Suslow and Schroth (14) found that these organisms reduced sugar beet seed germination, caused root d i s t o r t i o n s and root lesions, reduced root elongation, increased i n f e c t i o n by r o o t - c o l o n i z i n g fungi, and s i g n i f i c a n t l y decreased root growth. But d i r e c t evidence for b a c t e r i a l a n t i b i o s i s on plant roots was s t i l l lacking (28). More recently, Fredrickson and E l l i o t t (16,17) established that nonfluorescent bacteria of the genus Pseudomonas could s i g n i f i c a n t l y reduce winter wheat root and shoot growth through the production of a t o x i n . These studies showed the relationship was indeed a l l e l o p a t h i c , according to Molisch*s d e f i n i t i o n as quoted by Rice (29), where allelopathy i s defined as biochemical interactions between a l l types of plants, including microorganisms. The i n h i b i t o r y organisms were isolated from the rhizoplane of winter wheat plants growing i n the f i e l d . The pseudomonads are aggressive root colonizers that can be found on wheat plant roots i n high numbers and appear to be associated with heavy residues from the previous crop (15). Some isolates are so i n h i b i t o r y that winter wheat root growth i s nearly prevented i n laboratory bioassay (Figure 3). Other studies showed that the pseudomonads inhibited the growth of Escherichia c o l i C - l a (Figure 4) (16). However, i t was found l a t e r that the i n h i b i t i o n of root growth and of E . c o l i C - l a did not always correlate (30). Presumably, t h i s i s because we do not understand the factors affecting toxin production i n culture media. The i n h i b i t i o n of winter wheat root growth and of E. c o l i C - l a could be reversed by J.-methionine; however, when root exudates from winter wheat c u l t i v a r s that showed d i f f e r e n t i a l resistance to the toxin were examined, no differences i n 1-methionine exudation patterns



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Figure 1. Growth of winter wheat n o - t i l l seeded i n heavy residues ( l e f t ) i n comparison with that seeded i n low residues ( r i g h t ) .

Inputs

Outcome

Processes

Temperature Moisture Soil Properties Nutrient Status Microbial Activities

Microbial Transformation

Plant Metabolism

Phenolic Acids, etc. in Plant

PLANT DAMAGE

Plant U p t a k e

Figure 2 . Conceptual model for assessing a l l e l o p a t h i c p o t e n t i a l of phenolic acids.



510


Figure 3. Effect of an i n h i b i t o r y pseudomonad on the growth of winter wheat seedlings (control, l e f t ; treated, r i g h t ) .

Figure 4 . I n h i b i t i o n of c o l i C - l a growth by a pseudomonad i n h i b i t o r y to winter wheat growth (cured with mitomycin C on the right).



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were noted (30). While the i n h i b i t o r y pseudomonads isolated from winter wheat could colonize the roots of several crops, the i n h i b i t i o n was greatest for winter and spring wheat. Winter barley, l e n t i l s , and peas were i n h i b i t e d to a lesser extent while spring barley and oats were not i n h i b i t e d by the organism (31). The culture f i l t r a t e from the organism did not cause as severe root growth i n h i b i t i o n as the organism i t s e l f (31). These examples do show that the organisms and toxin show some s p e c i f i c i t y . This may not be surprising as Woltz (32) pointed out that secreted toxins are often highly s p e c i f i c to species and c u l t i v a r s . In related studies, marked inhibitory" pseudomonads that were placed on winter wheat and barley straw i n the laboratory and i n the f i e l d colonized the straw, e s p e c i a l l y the barley straw, to the v i r t u a l exclusion of the resident b a c t e r i a l population when i n c u bated at 5 ° C The laboratory study showed that high numbers of the introduced organisms persisted throughout a 35-day study (31). Figure 5 shows the effect of treating winter wheat seeds with an i n h i b i t o r y pseudomonad before they were n o - t i l l planted into methyl bromide-fumigated Palouse s i l t loam s o i l . The plants from the treated seeds ( l e f t ) were much poorer than those from the nontreated seeds (right) (33). These studies provide a strong case for allelopathy by the pseudomonads and indicate that Koch*s postulates have been s a t i s fied. However, more work remains to be done to determine the agronomic importance of the a l l e l o p a t h i c problems associated with microorganisms. Accomplishment of t h i s objective requires that more information be gathered i n several areas. The mechanism of toxin production by the organisms and the effect of the toxin on the plant must be determined. We must know why and how the organisms colonize roots and residues so aggressively. Root exudation by the plant may have a profound influence on root colonization and toxin production. The effects of t i l l a g e , residue management p r a c t i c e s , and crop r o t a tions on the presence of these organisms and t h e i r colonization of winter wheat roots must be determined i n order to provide d i r e c t i o n for a l l e v i a t i o n of the problem. Approaches may be the development of TOX-negative inocula, r e s i s t a n t v a r i e t i e s , and better cropping systems. F i r s t , a quick bioassay must be developed to determine the presence of the i n h i b i t o r y pseudomonads. While the E. c o l i C - l a assay shows promise (16). i t frequently does not work w e l l ; at present, the slow and laborious agar tube-plant bioassay (15) must s t i l l be used for best r e s u l t s . The apparent problem i s that we are unable to control the toxin or T0X expression, because i t appears that T0X expression can be low on a r t i f i c i a l media. The toxin must be i d e n t i f i e d and genetic mechanisms c o n t r o l l i n g TOX must be defined. Then c u l t u r a l techniques can be devised to control T0X expression. This should provide a t o o l whereby a rapid inexpensive assay, such as the E. c o l i C - l a assay, w i l l be more accurate so that i t can be used to rapidly survey for the presence of these organisms on residues and on winter wheat roots i n the f i e l d . This would provide evidence for the presence of these organisms and the effect of crop r o t a t i o n , residue management, and s o i l management. It would also more e a s i l y allow the testing of TOX-negative inocula. +

+

+

+




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Figure 5. Effect of i n h i b i t o r y pseudomonads on winter wheat growth i n the f i e l d (treated seed, l e f t ; untreated seed, r i g h t ) .



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Research must be conducted to determine how the toxin i s taken up by the plant and what i t s effects are on the plant. Labeled toxin may be required i n i t i a l l y to determine when and i f the plant has taken up the toxin i n the f i e l d i n order to separate the a l l e lopathic effect from that caused by plant pathogens. This knowledge would a s s i s t i d e n t i f i c a t i o n of the problem i n the f i e l d as the p r e s ence of the i n h i b i t o r y pseudomonads on roots i s innocuous, because l i t t l e noticeable effect occurs on the root except the stunting and occasional root deformation. Plant color i s not normally affected. Spontaneous a n t i b i o t i c - r e s i s t a n t mutants of these organisms are suitable for i n i t i a l root colonization studies; however, transposon mutants w i l l be more suitable for detailed laboratory and f i e l d studies. This procedure i s useful for sorting out the genetic r e l a tionships of these organisms and for determining the mechanisms c o n t r o l l i n g toxin production. The effect of plant root exudation and exudation patterns on root colonization and expression of toxin production must be considered. For example, i t may be important to determine the effect of root exudates from cold-stressed plants on these organisms, since the exudates apparently f i r s t appear j u s t after the plants break winter dormancy (34). These data should provide information on root colonization p o t e n t i a l , possible stimulation or reduction of toxin production, and mechanisms of plant resistance to the organisms. Ecological studies are desirable to determine the effect of temperature and moisture on the organisms, p a r t i c u l a r l y under f i e l d conditions. These organisms appear associated with conservation t i l l a g e systems where residues remain on or near the s o i l surface. This s i t u a t i o n i s paradoxical since residues on the surface gene r a l l y remain d r i e r than when incorporated into the s o i l and bact e r i a normally thrive better under high moisture conditions. The effect of water and temperature on survival of these organisms should be tested with various crop residues and various anatomical parts of the residue. These studies should provide clues for residue management to a l l e v i a t e the problem. After these steps are accomplished, i t should be possible to survey for the organisms, to relate t h e i r abundance to management practices such as t i l l a g e and r o t a t i o n , and to develop management alternatives to reduce t h e i r impacts. Importantly, more t r i a l s of bacteria-treated seed are necessary to determine the precise agronomic importance of these organisms. E a r l i e r studies indicated that wheat c u l t i v a r s responded d i f f e r e n t l y to these organisms (15). If necessary, i t should be possible to develop r e s i s t a n t v a r i e t i e s , e s p e c i a l l y when we know the mechanisms of plant uptake and mode of action of the toxin within the plant. One b i o l o g i c a l control may be the development of a TOX-negative inoculum for seed treatment. These bacteria may act l i k e other rhizobacteria, which are known to increase plant growth, apparently by displacing nonbeneficial bacteria i n the plant rhizosphere (14). Conclusion A l l e l o p a t h i c interactions caused by chemicals produced during the decomposition of crop residues and by toxins produced by bacteria


514



growing on plant roots appear to create serious agronomic problems. However, d i r e c t proof and assessment of the importance of these problems have been d i f f i c u l t . For both cases presented here, i . e . , phenolic acids and phytotoxins produced by pseudomonads colonizing the surface of winter wheat roots, more detailed information i s s t i l l needed. For the phenolic acids, rates of production, reactions i n the s o i l , effects on the plant, and regulation by the environment must be determined and modeled. For the i n h i b i t o r y pseudomonads, mechanisms c o n t r o l l i n g degree and persistence of root colonization by these organisms should be ascertained. In addition, data on genetic mechanisms c o n t r o l l i n g toxin production and the effects on the plant are needed. Use of models w i l l be helpful i n describing these systems. Assessments of crop damage by allelopathy can be accomplished and controls can be developed only after such information i s known. Acknowledgments Joint contribution from U.S. Department of Agriculture, A g r i c u l t u r a l Research Service, Pullman, Washington, and Department of Agronomy and S o i l s , Washington State University, Pullman, i n cooperation with the College of Agriculture and Home Economics Research Center, Washington State University, S c i e n t i f i c Paper No. 7314.

Literature Cited 1. Börner, H. Bot. Rev. 1960, 26, 393-424. 2. McCalla, T. M.; Haskins, F. A. Bacteriol. Rev. 1964, 28, 181-207. 3. Wang, T. S.; Yang, T. K.; Chuang, T. T. Soil Sci. 1967, 103, 239-49. 4. Chou, C. H.; Patrick, Z. A. J. Chem. Ecol. 1976, 2, 369-87. 5. Cheng, H. H. Proc. Seminar on Allelochemicals and Pheromones, 1982, p. 209-16. 6. Lynch, J. M. CRC Crit. Rev. Microbiol. 1977, 5, 67-107. 7. Elliott, L. F., McCalla, T. M.; Waiss, Α., Jr. In "Crop Residue Management Systems"; Oschwald, W. R., Ed.; American Society of Agronomy: Madison, Wisconsin, 1978; p. 131-46. 8. Sparling, G. P.; Vaughan, D. J. Sci. Food Agric. 1981, 32, 625-6. 9. Elliott, L. F.; Papendick, R. I.; Cochran, V. L. Proc. Sixth Manitoba-North Dakota Zero Tillage Workshop. 1984, p. 40-7. 10. McCalla, T. M.; Army, T. J. Adv. Agron. 1961, 13, 125-96. 11. McCalla, T. M.; Norstadt, F. A. Agric. Environ. 1974, 1, 153-74. 12. Cochran, V. L.; Elliott, L. F.; Papendick, R. I. Soil Sci. Soc. Am. J. 1977, 41, 903-8. 13. Harper, S. H. T.; Lynch, J. M. Plant Soil 1982, 65, 11-7. 14. Suslow, T. V.; Schroth, M. N. Phytopathology 1982, 72, 111-5. 15. Elliott, L. F.; Lynch, J. M. Soil Biol. Biochem. 1984, 16, 69-71. 16. Fredrickson, J. K.; Elliott, L. F. Plant Soil 1985, 83, 399-409.


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17. 18. 19. 20. 21. 22. 23. 24.


25. 26. 27. 28. 29. 30. 31. 32. 33. 34.

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Fredrickson, J. K.; Elliott, L. F. Soil Sci. Soc. Am. J. 1985, 49, 1172-7. Patterson, D. T. Weed Sci. 1981, 29, 53-9. Blum, U.; Dalton, B. R.; Shann, J. R. J. Chem. Ecol. 1985, 11, 619-41. Bremner, M. J.; Krogmeier, M. J. Agron. Abstr. 1984, p. 183. Fisher, R. F. In "Plant Disease: An Advanced Treatise"; Harsfall, H. G.; Cowling, Ε. B., Eds.; Academic: New York, 1979; Vol. 4, p. 313-30. Chou, C. H..; Chiang, Y.C.;Cheng, H. H. J. Chem. Ecol. 1981, 7, 741-52. Stowe, L. G.; Osborn, A. Can. J. Bot. 1980, 58, 1149-53. Reinertsen, S. Α.; Elliott, L. F.; Cochran, V. L.; Campbell, G. S. Soil Biol. Biochem. 1984, 16, 459-64. Lehmann, R. G.; Cheng, Η. H.; Harsh, J.B. Soil Sci. Soc. Am. J. 1985, (under review). Vaughan, D.; Sparling, G. P.; Ord, B. G. Soil Biol. Biochem. 1983, 15, 613-4. Wallace, J. M.; Whitehand, L. C. Soil Biol. Biochem. 1980, 12, 445-6. Suslow, T. V. In "Phytopathogenic Prokaryotes"; Mount, M. S.; Lacy, G. Η., Eds.; Academic: New York, 1982; Vol.I, p. 187-223. Rice, E. L. "Allelopathy"; Academic Press, Inc.: New York, 1984. Fredrickson, J. K.; Elliott, L. F., unpublished data. Fredrickson, J. K.: Elliott, L. F.; Engibous, J. C., unpublished data. Woltz, S. S. Ann. Rev. Phytopathol. 1978, 16, 403-30. Fredrickson, J. K.; Bolton, H.; Stroo, H.; Elliott, L. F., unpublished data. Elliott, L. F.; Lynch, J. M. Plant Soil 1985, 84, 57-65.

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Assessment of Allelopathy Among Microbes and Plants - ACS

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