The Chemistry of Allelopathy - American Chemical Society

---

20 T h e Influence o f Secondary Plant C o m p o u n d s o n the Associations o f Soil M i c r o o r g a n i s m s and Plant R o o t s 1

2

R. E.HOAGLAND and R. D. WILLIAMS Downloaded by UNIV OF PITTSBURGH on June 30, 2013 | http://pubs.acs.org Publication Date: December 17, 1985 | doi: 10.1021/bk-1985-0268.ch020

1

Southern Weed Science Laboratory, Agricultural Research Service, U.S. Department of Agriculture, Stoneville, MS 38776 Southern Plains Watershed and Water Quality Laboratory, Durant, OK 74701

2

This review summarizes aspects concerning the complexity and importance of associations of soil microorganisms and plant roots in the environment. Emphasis is not on compiling a comprehensive review, but rather on problems and potential for research in this area. Allelochemical sources, synthesis, metabolism, degradation, binding in soils, and mode of action are briefly presented and discussed with regard to root-microbe interactions. Data on these areas is accessed with recommendations and suggestions for further investigation. Allelopathy includes any direct or indirect harmful effect by one plant (including microorganisms) on another through the production of chemicals that escape into the environment. Generally in allelopathic interactions among plants, a secondary compound is released from one plant through exudation, leaching or decomposition of various plant parts which directly inhibits the growth and development of another plant. Such cases have been reported in the literature and have been implicated in successional changes in the plant community and/or spatial patterning of vegetation 2^). However, these effects may be indirect rather than direct due to the dynamic nature of the soil-root interactions. One well-documented example is the inhibition of nitrogen-fixing and nitrifying microorganisms by various plants during old field succession 2), Ecological succession is the orderly process of community change and is the sequence of communities which replace one another in a given area (3). Generally, the driving force behind succession has been attributed to changes of physical factors in the habitat, availability of essential minerals, differences in seed production and dispersal, competition, or a combination of these. In addition, Rice and co-workers (as cited in I) have indicated that This chapter not subject to U.S. copyright. Published 1985, American Chemical Society

In The Chemistry of Allelopathy; Thompson, A.; ACS Symposium Series; American Chemical Society: Washington, DC, 1985.

Downloaded by UNIV OF PITTSBURGH on June 30, 2013 | http://pubs.acs.org Publication Date: December 17, 1985 | doi: 10.1021/bk-1985-0268.ch020

302

THE CHEMISTRY OF ALLELOPATHY

allelopathy may be responsible for some successional changes i n grassland communities. These studies indicated that certain species from the weedy stage of succession are i n h i b i t o r y to other species i n t h i s stage, autotoxic, and/or i n h i b i t o r y to nitrogen-fixing and n i t r i f y i n g organisms. Furthermore, since the majority of plants absorb nitrogen through t h e i r roots (usually ammonium and n i t r a t e ions) often assisted by bacteria and mycorrhizal fungi, possible a l l e l o p a t h i c e f f e c t s on these processes could have a s i g n i f i c a n t impact on plant growth. Recent compilations of aspects of nitrogen i n s o i l s (4) and nitrogen f i x a t i o n i n plants (5) demonstrate the importance and complexity of nitrogen c y c l i n g . The objective of t h i s paper is to examine the relationship between the root and i t s ' natural microflora, as well as to discuss possible mediation of the p o t e n t i a l a l l e l o p a t h i c interactions by the microflora. Rhizosphere As the root system develops i n the soil, the soil micro-environment is altered, and organic and inorganic compounds exuded from roots stimulate growth and a c t i v i t y of various soil microorganisms p a r t i c u l a r l y bacteria and fungi. The zone of soil i n which the microflora is influenced by the plant root is termed the rhizosphere. Microbial a c t i v i t y is greater i n rhizosphere than non-rhizosphere s o i l s and the microflora i n the rhizosphere d i f f e r s quantitatively and q u a l i t a t i v e l y from that of the non-rhizospheric soil. Bacteria and fungi associated with the rhizosphere may be either attached to the surface of the root (rhizoplane) or present i n the soil surrounding the root. Mycorrhizal fungi not only grow on the root surface but also penetrate the root cortex and develop a symbiotic relationship with the host plant. Papavizas and Davey (6) demonstrated that b a c t e r i a l and fungal numbers decreased with increased distance from blue lupine roots and that some fungi, p a r t i c u l a r l y Cylindrocarpon r a d i c i c o l a , were associated only with the root surface. For example, the number of bacteria per gram of soil at the root surface, 3-6 mm from.the root surface and i n a control soil was 1.59 χ 10 , 3.8 χ 10 , and 2.7 χ 10 , respectively. Transmission electron micrographs indicate that the rhizosphere is generally i n the range of 1-2 mm thick (7). Although some authors exclude the mycorrhizal associations from general discussions of the rhizosphere, we have used the term i n i t s broadest sense. Since we w i l l be unable to cover a l l the l i t e r a t u r e , we refer the reader to several general references on the rhizosphere (8-12) and on mycorrhizae (13-18). Rhizosphere i n i t i a t i o n During seed imbibition, germination

and r a d i c l e elongation, various

In The Chemistry of Allelopathy; Thompson, A.; ACS Symposium Series; American Chemical Society: Washington, DC, 1985.

Downloaded by UNIV OF PITTSBURGH on June 30, 2013 | http://pubs.acs.org Publication Date: December 17, 1985 | doi: 10.1021/bk-1985-0268.ch020

20.

HOAGLAND AND

WILLIAMS

Soil

Microorganisms-Plant

Root Associations

303

organic compounds such as sugars and amino acids are exuded. These compounds stimulate the germination and growth of b a c t e r i a l and fungal spores. I n i t i a t i o n of the rhizosphere begins as early as seed germination. Further rhizosphere development takes place as the root elongates, but not a l l areas of the root stimulate m i c r o f l o r a l development equally. The area just behind the root cap is the most active part of the root and contributes s i g n i f i c a n t l y to mycorrhizal formation. Early rhizosphere establishment is demonstrated i n 2-3 day-old wheat plants when there is a s h i f t towards a population of amino acid requiring bacteria (19). Maximum a c t i v i t y and numbers of rhizosphere microorganisms correlated with maximum vegetative plant development (20-22). Once established, the rhizosphere remains q u a l i t a t i v e l y s i m i l a r , but quantitatively increases from seedling stage to maturity (23). After maturity the b a c t e r i a l population reverts to a population similar to that i n non-rhizospheric s o i l s . Rhizospheric organisms Bacteria and fungi are stimulated by root growth and are found i n the rhizosphere. Generally amino acid-requiring bacteria comprise a higher proportion of the rhizosphere microflora than the general soil microflora, and the rhizosphere contains a higher proportion of bacteria with simple n u t r i t i o n a l requirements than soil distant from the plant root (24). Various p h y s i o l o g i c a l b a c t e r i a l groups (motile forms, chromagenic forms, ammonifiers, d e n i t r i f i e r s , g e l a t i n l i q u i f i e r s and aerobic cellulose-decomposing forms) are present i n greater numbers i n the rhizosphere than the general soil, whereas other groups ( n i t r i f y i n g forms, anaerobic cellulose-decomposing forms and nitrogen-fixing anaerobes) are fewer i n number (12). Rhizobium, Azotobacter and Psuedomonas are b a c t e r i a l genera common to the rhizosphere. Although numerous genera of fungi may be associated with plant roots, only a r e s t r i c t e d number appear to be isolated from apparently healthy roots with high frequency, i . e . Fusarium, Cylindrocarpon, Rhizoctonia, Glicladium and M o r t i e r e l l a (12). In nature, most plant roots are invaded by fungi and transformed into mycorrhizae or "fungus roots" (25). The host plant and fungus form a symbiotic relationship whereby nutrients absorbed from the soil by the fungus are released into the host c e l l and the mycorrhizal fungus obtains nutrients from the host. Mycorrhiza formation is complex and depends on the dynamic interaction of the host plant, fungus and soil. Once formed, mycorrhizae have a profound influence on growth and development of the host plant (26-28). There are three d i s t i n c t types of mycorrhizae, but the vesicular-arbuscular mycorrhiza is found on more plant species than

In The Chemistry of Allelopathy; Thompson, A.; ACS Symposium Series; American Chemical Society: Washington, DC, 1985.

304

THE CHEMISTRY OF ALLELOPATHY

any other type (29). It occurs i n the bryophytes, pteridophytes and spermatophytes, and is of p a r t i c u l a r interest because i t is found on many economically important agronomic and h o r t i c u l t u r a l species. Vesicular-arbuscular mycorrhizae have been reported to enhance: absorption of nutrients such a phosphorus (30-37), sulfur (38, 39), zinc (40), s i l i c o n (32), potassium (41), calcium (42) and copper (42); s a l t (43) and drought tolerance (43); and nodulation (44-46). The increase i n nodulation may be due to an increase i n the n u t r i t i o n a l l e v e l of the plant ( p a r t i c u l a r l y with regard to phosphorus) and to o v e r a l l better growth dynamics of mycorrhizal versus non-mycorrhizal plants (47).

Downloaded by UNIV OF PITTSBURGH on June 30, 2013 | http://pubs.acs.org Publication Date: December 17, 1985 | doi: 10.1021/bk-1985-0268.ch020

Factors Influencing Rhizosphere Formation Some factors which influence the development of rhizosphere organisms are: plant species, plant age, root exudates, nutrient pool, soil type, soil moisture, soil temperature and pH. B a s i c a l l y any condition which a l t e r s root exudation (quantitatively or q u a l i t a t i v e l y ) of the host plant can a l t e r the nature of the rhizosphere. For example high l i g h t i n t e n s i t y and temperature can increase root exudation, p a r t i c u l a r l y during the f i r s t few weeks of growth (48). Increases i n t o t a l b a c t e r i a l number, glucose fermenting forms, and ammonifiers were detected on wheat roots grown under high l i g h t i n t e n s i t y (49). In a s i m i l a r study fungi development was not affected by l i g h t i n t e n s i t y (50). These studies suggest that increased root exudation (caused by increased l i g h t intensity) promotes b a c t e r i a l growth to a greater degree than fungal growth. Furthermore, t h i s indicates how one environmental parameter s i g n i f i c a n t l y influences the relationship between host exudation patterns and microbial interactions. Nature of Exudate and Factors Influencing Exudation One major factor influencing rhizosphere development is the root exudate. Rovira and Davey (8) compiled a l i s t of compounds occurring i n wheat root exudates which are t y p i c a l l y found i n exudates i n general. Several sugars (glucose, fructose, ribose, e t c . ) , amino acids (most of the commonly occurring amino a c i d s ) , organic acids (oxalic, c i t r i c , g l y c o l i c , e t c . ) , nucleotides, flavonones, and enzymes (invertase, amylase, protease) have been i d e n t i f i e d (8). Several phenolic acids such as c a f f e i c , f e r u l i c and cinnamic acids have also been reported to exude from plant roots and have been implicated as allelochemicals (1). Most of the compounds exuded are simple organic compounds of r e l a t i v e l y low molecular weight. The nature of the compounds i n the exudate can be altered by b i o t i c and a b i o t i c factors experienced by the plant. Factors involved i n quantitative or q u a l i t a t i v e changes i n exudates are:

In The Chemistry of Allelopathy; Thompson, A.; ACS Symposium Series; American Chemical Society: Washington, DC, 1985.

Downloaded by UNIV OF PITTSBURGH on June 30, 2013 | http://pubs.acs.org Publication Date: December 17, 1985 | doi: 10.1021/bk-1985-0268.ch020

20.

HOAGLAND AND

WILLIAMS

Soil

Microorganisms-Plant

Root Associations

305

plant species, plant age, plant n u t r i t i o n , l i g h t quality and quantity, temperature, soil moisture, soil type, soil pH, f o l i a r sprays ( a g r i c u l t u r a l chemicals) and microorganisms (51, 52). These are generally the same factors that influence rhizosphere microorganisms. Exudates may be grouped according to t h e i r mobility through the soil as d i f f u s i b l e - v o l a t i l e , diffusible-water soluble and nondiffusible compounds (8). Most of the techniques used to study root exudates y i e l d information only on the diffusible-water soluble compounds. However, C-labeling techniques indicate that for every unit of carbon exuded as water-soluble material, 3 to 5 units are released as non-water soluble components (mucilage and root cap c e l l s ) and 8 to 10 units as v o l a t i l e material (8). Based on t h i s , Rovira and Davey (8) stress that (a) under natural conditions many of the simple compounds w i l l be quickly adsorbed or modified by microflora, and (b) techniques used l a r g e l y ignore the v o l a t i l e materials and water insoluble materials that may far exceed the soluble compounds under natural conditions. The majority of the allelochemicals i d e n t i f i e d are water soluble, or p a r t i a l l y water soluble, and of r e l a t i v e l y low molecular weight. Also only a few v o l a t i l e compounds have been suggested as i n h i b i t o r s i n allelopathy studies (see for example 53-56). Influence of Rhizosphere Organisms on Plants The nature of exudates plays a key role i n rhizosphere development and i n turn rhizosphere organisms have either a d i r e c t or i n d i r e c t e f f e c t on the host plant's growth and development. Rhizosphere organisms can: a l t e r root morphology; change phase e q u i l i b r i a of soil; enhance nutrient a v a i l a b i l i t y to the plant; change the chemical composition of soil p a r t i c i p a t i n g i n symbiotic processes; and p h y s i c a l l y block root surfaces (52). Rhizosphere organisms can affect exudation by: a l t e r i n g root c e l l permeability or root metabolism; p r e f e r e n t i a l l y u t i l i z i n g certain exudate components; or, excreting toxins (52). It is clear that the process(es) involved i n root-rhizosphere interactions are both complex and dynamic. A l l nutrients and/or compounds a plant obtains from the soil must pass through the rhizosphere and be subjected to b i o l o g i c a l and chemical transformation i n t h i s zone. Studies of toxic compounds i n the soil should include processes of the rhizosphere. An allelochemical exuded by a plant could be altered (detoxified or enhanced) by the rhizosphere of the exuding or target plant. A l t e r n a t i v e l y , allelochemicals may have indirect e f f e c t s on the target species by influencing i t s rhizosphere. Modification of Exudates by the Rhizosphere Modification of chemicals by the rhizosphere has been followed i n

In The Chemistry of Allelopathy; Thompson, A.; ACS Symposium Series; American Chemical Society: Washington, DC, 1985.

306

THE CHEMISTRY OF ALLELOPATHY

studies using CO^. For example, Martin (57) studied water-soluble compounds exuded by roots of wheat, clover and ^ ryegrass grown i n sandy soil, ^ | t e r labeling the shoots with C0 . Differences i n the amounts of C-labeled material i n the leachate occurred among species, but i n t h i s near natural nonsterile environment, exudates were mainly compounds of high molecular weight, i . e . 45% had molecular weights above 10,000 and 70% were above 1,000. Under s t e r i l e conditions, the bulk of soluble exudates released by roots consists of low molecular weight compounds. This indicates that these low molecular weight compounds are r e a d i l y u t i l i z e d by microorganisms i n the rhizosphere, and are subsequently transformed into more complex forms. Downloaded by UNIV OF PITTSBURGH on June 30, 2013 | http://pubs.acs.org Publication Date: December 17, 1985 | doi: 10.1021/bk-1985-0268.ch020

2

Synthesis and Sources of Allelochemicals from Plants The term allelochemical applies to phytotoxic substances that cause growth i n h i b i t i o n (58). These compounds are generally composed of by-products of main plant biochemical pathways, i . e . , secondary plant compounds (59). Rice (1) has designated 14 allelochemical categories based on chemical properties and metabolic pathways. Moreland et a l . (60) and Moje (61) have reviewed major allelochemicals and t h e i r roles i n plant interactions. The most thoroughly studied and perhaps the most important allelochemicals are those derived from the shikimate biosynthetic pathway (Fig. 1) (62). The most important chemical groups i n t h i s regard are: phenolic acids and t h e i r derivatives, terpenoids and steroids, coumarins, flavonoids, alkaloids and cyanohydrins, and tannins Ç1 ). These compounds are generally water soluble and can be leached from l i v i n g and decaying plant tissues; exuded from roots; and some compounds are v o l a t i l e and can d i f f u s e from roots and leaves. There are numerous reports of allelopathy i n the l i t e r a t u r e , but often the i d e n t i t y of the allelochemical(s) is unknown. There are, however, many cases where s p e c i f i c compounds or groups of compounds have been implicated as a l l e l o p a t h i c agents. Table 1 summarizes some examples of sources and i d e n t i t i e s of allelochemicals that d i r e c t l y i n h i b i t plant growth. These secondary compounds have been implicated as a driving force i n ecological succession (1). Allelochemicals Implicated i n Affects on Rhizosphere and/or Root-microbial Association The bulk of the allelopathy l i t e r a t u r e has dealt with d i r e c t toxic effects on other plants. However, as developed i n t h i s review, i t is obvious that allelochemicals may have a major impact on plant root-microbial interactions. Such interactions could lead to growth i n h i b i t i o n i n the microorganisms (or i n roots) and a f f e c t other factors of the root-microbe association r e s u l t i n g i n e f f e c t s

In The Chemistry of Allelopathy; Thompson, A.; ACS Symposium Series; American Chemical Society: Washington, DC, 1985.

Soil

HOAGLAND AND WILLIAMS

Microorganisms-Plant

y\

Root Associations

TANNINS

G A L L I C ACID SINAPIC FERULIC

ACID ISOFLAVONOIDS

Î Downloaded by UNIV OF PITTSBURGH on June 30, 2013 | http://pubs.acs.org Publication Date: December 17, 1985 | doi: 10.1021/bk-1985-0268.ch020

CHLOROGENIC

ACID

.

^

ACID

FLAVONOIDS

CAFFEIC

ACID

CHALCONES

• J.-CINNAMATE (g)

TRYPTOPHAN

£-COUMAR > AMMONIA

PHENYLALANINE

^

^

«

Τ

ATE

@

TYROSINE

^

®

0

PREPHENATE

t® t® t® t®

CHORISMATE

SHIKIMATE

I®

3-DEOXY-D-ARABINO-HEPTULOSONATE

-7-P

® ERYTHROSE

4 4PP

—

—

S

A\

PMOSPHOENOL

PYRUVATE

Figure 1. Schematic outline of various products and associated enzymes from the shikimate and phenolic pathways i n plants (and some microorganisms). Enzymes: (1) 3-deoxy-2-oxo-D-arabinoheptulosate-7-phosphate synthase; (2) 5-dehydroquinate synthase; (3) shikimate dehydrogenase; (4) shikimate kinase; (5) 5-enolpyruvylshikimate-3-phosphate synthase; (6) chorismate synthase; (7) chorismate mutase; (8) prephenate dehydrogenase; (9) tyrosine aminotransferase; (10) prephenate dehydratase; (11) phenylalanine aminotransferase; (12) anthranilate synthase; (13) tryptophan synthase; (14) phenylalanine ammonia-lyase; (15) tyrosine ammonia-lyase; and (16) polyphenol oxidase, (From ACS Symposium Series No. 181, 1982) (62).

In The Chemistry of Allelopathy; Thompson, A.; ACS Symposium Series; American Chemical Society: Washington, DC, 1985.

307

In The Chemistry of Allelopathy; Thompson, A.; ACS Symposium Series; American Chemical Society: Washington, DC, 1985.

- water

Method of Isolation Extraction - ethanol

Tripsacum laxum, dried leaves

Panicum maximum, dried leaves Paspalum plicatulum, dried leaves Polygonum orientale, roots, stems, leaves Rumex crispus, leaves Setaria sphacelata, dried leaves Sorghum halepense, leaves, rhizomes

Kochia scoparia, leaves

Helianthus annuus, root

E r i c a arborea, leaves

Phenolics F e r u l i c acid, other phenolics Chlorogenic, £-coumaric acids, £-hydroxybenzaldehyde F e r u l i c acid, other phenolics

Phenolics Phenolics Chlorogenic and c a f f e i c acids Chlorogenic and c a f f e i c acids F e r u l i c and coumaric acids Phenylheptatriyne V a n i l l i c , j>-hydroxybenzoic, o-hydroxyphenylacetic acids Phenolics - f e r u l i c acid Phenolics - p-coumaric acid F e r u l i c acid and other phenolics Chlorogenic, isochlorogenic and s u l f o s a l i c y l i c acids S a l i c y l i c acid, scopoletin, p-hydroxybenzaldehyde Chlorogenic, isochlorogenic acids; scopoletin F e r u l i c acid, myricetin, quercitin o-Hydroxyphenylacetic acid F e r u l i c acid, other phenolics Flavone glycosides

Abutilon theophrasti, leaves Agropyron s m i t h i i , l i t t e r Ambrosia a r t e m i s i f o l i a , shoots Aster pilosus, shoots Avena fatua, dead l i t t e r Bidens p i l o s a , leaves Brachiaria mutica, dried leaves

Chloris gayana Cynodon dactylon, dried leaves D i g i t a r i a decumbens, dried leaves D i g i t a r i a sanguinalis, whole plant

Chemical Class F e r u l i c acid and other phenolics F e r u l i c acid and other phenolics

Sources and Identity of Allelochemicals from Higher Plants

Species and Tissue Cyperus esculentus, tubers and leaves Cyperus rotundus, tubers and leaves

Table I.

Downloaded by UNIV OF PITTSBURGH on June 30, 2013 | http://pubs.acs.org Publication Date: December 17, 1985 | doi: 10.1021/bk-1985-0268.ch020

74

84 74 85, 86

74 74 83

82

79-81

78

75 74 74 76, 77

66, 67 68 69 69 70, 71 72, 73 74

Reference 63, 64 64, 65

3

r r m r Ο

>

Ο τι

H

g

m π 33 m

In The Chemistry of Allelopathy; Thompson, A.; ACS Symposium Series; American Chemical Society: Washington, DC, 1985. 85^, 86

63, 64 90 75, 89 91-93 94 95 96 90_ 97-101 j33, 64 102 103

F e r u l i c acid, other phenolics Scopolamine, hyoscyamine Phenolic glucosides, f a t t y acids Phenolics Quercitin, f e r u l i c a c i d , others Xanthotoxin, (furanocoumarin) Phenolics Scopolamine, hyoscyamine Acetic, butyric acids F e r u l i c acid, other phenolics Terpenes, camphor, pinene, Various v o l a t i l e s

Cyperus esculentus Datura stramonium Polygonum aviculare

Pteredium aquilinum Salsola k a l i

Ammi majus

AbutiIon theophrasti Datura stramonium

Agropyron repens Cyperus esculentus

Artemisia tridentata Salvia leucophylla

Leachates - leaves

- fronds

- fruits

- seeds

- roots and rhizomes

V o l a t i l e s - leaves

7_5, 89

88

Chlorogenic, £-coumaric acids; p-hydroxybenzaldehyde

- root and rhizome

Polygonum aviculare

Hemarthria a l t i s s i m a

Sorghum halepense,

69^ 87^ 79-81

Chlorogenic and c a f f e i c acids Oxalic acid Chlorogenic, isochlorogenic acids; scopoletin Cinnamic and benzoic acids and derivatives Phenolic glucosides, f a t t y acids

Exudates - root

Ambrosia a r t e m i s i f o l i a Chenopodium album Helianthus annuus

Downloaded by UNIV OF PITTSBURGH on June 30, 2013 | http://pubs.acs.org Publication Date: December 17, 1985 | doi: 10.1021/bk-1985-0268.ch020

Downloaded by UNIV OF PITTSBURGH on June 30, 2013 | http://pubs.acs.org Publication Date: December 17, 1985 | doi: 10.1021/bk-1985-0268.ch020

310

THE CHEMISTRY OF ALLELOPATHY

interpreted as d i r e c t a l l e l o p a t h i c e f f e c t s . Most of the a l l e l o p a t h i c l i t e r a t u r e disregards the rhizosphere i n t e r a c t i o n with plant roots even though some studies suggest the importance of d i r e c t e f f e c t s of allelochemicals on soil microorganisms (Table 2). Many varied plant sources contain components that a f f e c t rhizosphere bacteria and fungi. In contrast to numerous examples of d i r e c t e f f e c t s of allelopathy (of which Table 1 is only a small fraction) there are limited examples of i n d i r e c t e f f e c t s (presented i n Table 2, which comprises most of the major reports i n t h i s area). Here most of the work is from Rice's laboratory and deals with interactions of allelochemicals and plant growth with regard to growth of nitrogen-fixing and n i t r i f y i n g bacteria, nodulation (nodule mass and number), and hemoglobin content of nodules. Also presented are other important examples of interactions, i . e . growth of plants i n the presence of f r e e - l i v i n g bacteria (104), e f f e c t s of rhizosphere fungi and bacteria on Rhizobium growth (106, 133, 134), e f f e c t s of mycelial extracts of fungi on Rhizobium growth and on nodulation and growth of soybean (121), and root exudate e f f e c t s on mycorrhizal fungi growth (122, 132). Elkan (135) found that root extracts of a hybrid between a nodulating and non-nodulating soybean caused reduced nodule weight, t o t a l dry weight, and t o t a l nitrogen per plant i n the nodulating variety of soybean, and did not i n h i b i t R. japonicum growth. Azotobacter cultures caused increased growth i n several plant species, probably due to production of plant growth regulators, i . e . IAA, GA, and cytokinins (136). Schenck and Stotzky (137) showed that unidentified v o l a t i l e s from several germinating seeds promoted growth of soil bacteria and fungi. Menzies and G i l b e r t (138) showed that exposure of s o i l s to a l f a l f a , corn and other plants caused an increase i n r e s p i r a t i o n rate of the soil microflora, followed by increased b a c t e r i a l and fungal growth. Studies of e f f e c t s of rhizosphere fungi on seed germination and root growth of leguminous weed seedlings indicated that culture f i l t r a t e s of some rhizosphere fungi i n h i b i t e d germination i n some species, but increased germination of others (139). As stated e a r l i e r , mycorrhizae enhance nutrient absorption. Greater soil e x p l o i t a t i o n by mycorrhizal roots as a means of increasing phosphate uptake is well established. The normal phosphate depletion zone around non-mycorrhizal roots is 1-2 mm, but an endomycorrhizal root symbiont increased t h i s zone to 7 cm (140). This a b i l i t y to increase the n u t r i t i o n a l l e v e l ( p a r t i c u l a r l y with regard to phosphorus), and subsequently the o v e r a l l better growth dynamics of the mycorrhizal plant has been suggested as the reason for the s a l t (43) and drought (44—46) tolerance and increased nodulation (47) observed i n mycorrhizal associations. Another i n t e r e s t i n g aspect of t h i s enhanced nutrient uptake is the possible e f f e c t of mycorrhizae on competitive a b i l i t y between two plant species. Under some conditions, mycorrhizal

In The Chemistry of Allelopathy; Thompson, A.; ACS Symposium Series; American Chemical Society: Washington, DC, 1985.

In The Chemistry of Allelopathy; Thompson, A.; ACS Symposium Series; American Chemical Society: Washington, DC, 1985.

Source 2

Tissue-isolation H 0-leaf wash

At r i p l e x c o n f e r t i f o l i a , Eurotia lanata, Artemisia tridentata

A r i s t i d a adscensionis

107, H)8

inhib'd. growth of NO" & NH, Λ J -ϊ ^ oxidizers

red'd. growth, nodulation & 109 acetylene red*η i n Alnus crispa inhib'd. n i t r i f i c a t i o n 110

106

105

104

Reference

antagonistic and stim. to R. japonicum

stim'd. r a d i c l e elongation i n presence of ^ - f i x . bacteria inhib'd. R. japonicum growth

Effect

Table I I . Continued on next page

0

111 red'd n i t r i f i c a t i o n caffeic, chlorogenic acids, tannins inhib'd. Rhizobium& Azotobacter 112-114 extracts & leachates nodulation roots, shoots, l i t t e r inhib'd. N - f i x a t i o n 115 I^O-extract, leaves

Identity

Sources and Action of Secondary Plant Compounds on Root - Rhizosphere Interactions

non-nodulating roots Cassia f i s t u l a , £. occiden-, t a l i s , Leucaena leucocephala. and root extracts fungi and bacteria T r i f o l i u m alexandrinum of T^. alexandrinum Hyparrhenia f i l i p e n d u l a , root extracts Cynodon dactylon, Rhynchelytrum repens, Sporobolus pyramidalis, Eragrostis curvula, Themeda triandra, Pennisetum purpureum H^O-extracts of a l l Populus balsamifera plant parts extracts & leachates Abries balsamea, Populus of leaves and buds balsamifera extracts-needles, Pinus ponderosa bark

Species Camelina sativa

Table I I .

Downloaded by UNIV OF PITTSBURGH on June 30, 2013 | http://pubs.acs.org Publication Date: December 17, 1985 | doi: 10.1021/bk-1985-0268.ch020

In The Chemistry of Allelopathy; Thompson, A.; ACS Symposium Series; American Chemical Society: Washington, DC, 1985. inhib' d. R japonicum; Τ. v e r i d i inhib'd. nodulation & M. vesiculosis inc'd nodule no. inhib'd. mycorrhizal fungi growth

inhib'd. Nitrosomonas, Nitrobacter; 123-131 red'd nodule size & no.; red'd hemoglobin i n nodules

inhib'd. mycorrhizal fungal growth

sugarphenolic complexes, tannins benzoic acid, catechol

straw soil

decomposing

extracts of

mycelial exudates

root leachate

extracts, exudates, leachates of plants & soil

H^O-extracts,

Soils

Trichoderma v i r i d e , Rhizopus nigricans, Mucor vesiculosis

Calluna vulgaris

Various plant species, ex. Ambrosia e l a t i r , Euphorbia c o r r o l l a t e r , Helianthus annuus

Populus tremula

leaves

humic & f u l v i c acids

phenolics

inhib'd. E. c o l i , B a c i l l u s s u b t i l i s ; Staph, aureus, Strep, haemolyticus toxic i n lettuce & r i c e seed bioassays; mungbean root assay stim'd plant growth & nodule mass; dec'd nodule no.

Oryza sativa

2

132

122

121

120

119

118

117

Trachypogon plumosus

acid endproducts

116

Reference

growing w. Azotobacter H 0-extract, roots

inhib'd. Rhizoctonia growth, inc'd pigmentation i n mycelium, dec'd saprophytic a c t i v i t y inhib'd. A. chroococcum

Effect

Pseudomonas spp.

?

Identity

Tissue-isolation v o l a t i l e s f r . plant residues

Source

(Continued)

Species Various plant species

Table I I .

Downloaded by UNIV OF PITTSBURGH on June 30, 2013 | http://pubs.acs.org Publication Date: December 17, 1985 | doi: 10.1021/bk-1985-0268.ch020

Downloaded by UNIV OF PITTSBURGH on June 30, 2013 | http://pubs.acs.org Publication Date: December 17, 1985 | doi: 10.1021/bk-1985-0268.ch020

20.

HOAGLAND AND WILLIAMS

Soil

Microorganisms-Plant

Root Associations

313

plants have been more competitive than non-mycorrhizal plants (141, 142). Although there is no doubt as to the importance of mycorrhizae i n nutrient absorption, reviews on ion uptake have generally not considered i t . Hatling et a l . (143) made t h i s same point more than 10 years ago. In addition, although phenolic acids i n h i b i t phosphate (144, 145) and potassium (146) uptake, no work has examined the e f f e c t s of these compounds on nutrient absorption of mycorrhizal associations. Since soil microorganisms produce the bulk of the v o l a t i l e compounds emitted from soil, which are known to i n h i b i t or stimulate fungal development (147-148), t h i s group of compounds from microbial sources should receive more attention. If mycorrhizae are s i t e s of action f o r allelochemicals, t h i s is an important indirect aspect of a l l e l o p a t h i c i n t e r a c t i o n among plants. I n h i b i t i o n of mycorrhizal formation or a reduction i n the e f f i c i e n c y of mycorrhizal association would reduce the nutrient l e v e l of the mycorrhizal plant and subsequently i t s competitiveness, stress tolerance or nodulation. Although allelochemicals have been implicated i n the reduction of nodulation and nodule s i z e , possible mycorrhizal involvement has not been examined. This is a d i f f i c u l t area of research but one that w i l l provide better understanding of t h i s complex s i t u a t i o n . N i t r i f i c a t i o n i n the Rhizosphere C o n f l i c t i n g reports on the question of n i t r i f i c a t i o n i n the rhizosphere e x i s t . Goring and Clark (149) found that nitrogen was immobilized i n the rhizosphere giving an apparent i n h i b i t i o n of n i t r i f i c a t i o n , but there was a rapid accumulation of n i t r a t e a f t e r removal of the roots from the rhizosphere. Other workers found that exudates d i d not i n h i b i t n i t r i f i c a t i o n by pure cultures of n i t r i f y i n g bacteria and that the number of Nitrosomonas and Nitrobacter increased i n the rhizosphere (150). This is contrary to Rice's r e s u l t s (Table 2) i n which root extracts of several plants inhibited n i t r i f i c a t i o n i n pure cultures and i n soil. Moore and Waid (151) eliminated immobilization and d e n i t r i f i c a t i o n as possible causes f o r low content of n i t r a t e and confirmed an e a r l i e r report (152) that i n h i b i t i o n of n i t r i f i c a t i o n by grass roots was responsible f o r low levels of n i t r a t e i n permanent grassland s o i l s . Munro (107, 108) found that root extracts from Hyparrhenia f i l i p e n d u l a and several other species inhibited the growth of n i t r a t e - and ammonia-oxidizing bacteria. Contrary to t h i s , Purchase (153, 154), using root washings of H. f i l i p e n d u l a , found no evidence of t o x i c i t y to Nitrobacter and Nitrosomonas. Since Nitrobacter is more sensitive to phosphorus deficiency than Nitrosomonas, and because phosphorus deficiency is s u f f i c i e n t l y severe i n some s o i l s to r e s t r i c t growth, i t s a b i l i t y to compete f o r nitrogen is diminished. I n h i b i t i o n was found i n the root extract

In The Chemistry of Allelopathy; Thompson, A.; ACS Symposium Series; American Chemical Society: Washington, DC, 1985.

314

THE CHEMISTRY OF ALLELOPATHY

where the concentration of the allelochemical(s) may have been greater than i n the root wash. This l a t e r controversy points out a major problem i n much of the allelopathy l i t e r a t u r e , i . e . the lack of i d e n t i f i c a t i o n and q u a n t i f i c a t i o n of toxic components.

Downloaded by UNIV OF PITTSBURGH on June 30, 2013 | http://pubs.acs.org Publication Date: December 17, 1985 | doi: 10.1021/bk-1985-0268.ch020

Allelochemical Concentration i n

Soil

Allelochemical complexes, pool size, and turnover i n s o i l s . Many chemicals occur i n s o i l s that have been released from l i v i n g and decaying plant tissues and soil microorganisms. Generally these consist of nearly a l l of the common amino acids, common sugars, a l i p h a t i c acids, nucleotides, some enzymes, and various benzoic and phenolic acids and their derivatives (8). L i t t l e information is available on concentration levels of many of these components. Reports (155, 156) indicate that free amino acid levels seldom exceed 2 ug/g soil, but these levels can be 7-fold higher i n _^ rhi^osphere s o i l s . This is a concentration range of about 10 to 10 M. Most of the phytotoxic compounds isolated from plants and s o i l s are the phenolic acids and t h e i r derivatives (157, 158). Aromatic amino acids are precursors of phenolic and benzoic acids i n plants, and some microorganisms and soil microbes readily metabolize these l a t t e r compounds to various products (159, 160). Free phenolic acids can occur i n the soil solution but only f e r u l i c , £-hydroxybenzoic, £-coumaric, and v a n i l l i c acids are commonly found, and at amounts less than O.01% of the t o t a l soil organic matter (158, 161, 162). These four phenolic acids are readily u t i l i z e d by soil microorganisms (163-165). There is l i t t l e d i r e c t evidence (or research) r e l a t i n g the effects of soil microbial metabolism of phenolics to phytotoxicity to higher plants (166). Recent studies do show that amelioration of phenolic phytotoxicity could be achieved with some microbes i n solution culture (167). There is s u f f i c i e n t evidence that some plants stimulate the growth of phenolic acid-degrading organisms (165), and that many soil fungi can use phenolic acids as sole carbon sources (168). This indicates that some soil microbes can exert t h e i r maximal effect on phenolic acid metabolism during plant growth. Maximal levels for £-coumaric and f e r u l i c acids of 30.0 and 6.5 pmol/l^O g of soil ha^e been reported (158) and concentrations of 4 χ 10 M and 3 χ 10 M, respectively, for these two acids i n other s o i l s ( 1 6 1 ) O t h e r gtudies indicate a similar concentration range of 2.3 χ 10 to 10 M for £-hydroxybenzoic, v a n i l l i c and £-coumaric acids (169). These levels may be too low to have direct measurable a l l e l o p a t h i c e f f e c t s on plants i n greenhouse or growth chamber studies (non-rhizosphere s o i l s , low microbial population). However, i n f i e l d rhizosphere s o i l s (high microbial population) these levels could be s u f f i c i e n t to influence microbial growth

In The Chemistry of Allelopathy; Thompson, A.; ACS Symposium Series; American Chemical Society: Washington, DC, 1985.

20.

HOAGLAND AND WILLIAMS

Soil

Microorganisms-Plant

Root Associations

315

Downloaded by UNIV OF PITTSBURGH on June 30, 2013 | http://pubs.acs.org Publication Date: December 17, 1985 | doi: 10.1021/bk-1985-0268.ch020

(positively or negatively) r e s u l t i n g i n an indirect effect v i a a l t e r a t i o n of mycorrhizal-root associations. Complexing of various compounds commonly occurs i n soil, transforming low molecular weight materials into high molecular weight polymers. Phenolic acids are intermediates i n the formation of l i g n i n s and humic substances (170) and are also important i n s t a b i l i z i n g nitrogen i n organic forms i n s o i l s (171). Associated higher molecular weight compounds ( i . e . aggregates, polymers of phenols) can a l t e r the concentration of low molecular weight phenolics i n the rhizosphere (160, 172). One proposed scheme of such polymerization consists of condensation of amino acids with phenolic compounds and sugars to y i e l d complex polymers (Fig. 2) (173). Phenolic Binding and A v a i l a b i l i t y i n S o i l s . Low molecular weight phenolic and polymeric phenolic complexes occur i n s o i l s and can be bound to soil p a r t i c u l a t e s . Wang et a l . (174) have shown that clay minerals can act c a t a l y t i c a l l y to influence phenolic polymerization. These polymers can then form clay-organic complexes r e s u l t i n g i n reduced a v a i l a b i l i t y of these materials to plant roots and thus decreased phyto|oxic o r g l J ^ l o p a t h i c potential. Soil mineral content ( i . e . A l or Fe * ) also has a great influence on absorption of phenolics and is implicated i n reducing phytotoxicity, increasing b i o t i c degradation, and i n c a t a l y t i c a l l y transforming these compounds into humic materials (175). The common low molecular weight phenolics have varying a f f i n i t i e s for s o i l s depending on soil type and phenolic structure (175, 176). Phenolics (especially polyphenolics) exuded from plants or produced during decomposition can be rapidly leached from the soil surface, become bound, and contribute to humus formation (174). Phenolic acid t o x i c i t y is also dependent on soil nutrient status, especially with regard to nitrogen and phosphorus levels (177). Since l i g n i n s are polymers of phenolics and are major plant constituents with resistance to microbial decomposition, they are the primary source of phenolic units for humic acid synthesis (178, 179). Once transformed, these humic acids become further resistant to microbial attack and can become bound to s o i l s (180); form interactions with other high molecular weight phenolic compounds (ex. l i g n i n s , f u l v i c acids) and with clays (181); and influence the biodégradation of other organic substrates i n s o i l s (182, 183). Some compounds, i . e . benzoic and cinnamic acids are not protected against biodégradation to a high degree by linkage and/or absorption on soil constituents such as clay or humus (184), hence they may have a rapid turnover rate i n s o i l s . Incorporation of some xenobiotics (herbicides) into soil humus-complexes occurs v i a pathways analogous to those for incorporation of naturally occurring phenolic and benzoic acids and do indeed involve phenolic and humus-like constituents +

In The Chemistry of Allelopathy; Thompson, A.; ACS Symposium Series; American Chemical Society: Washington, DC, 1985.

Downloaded by UNIV OF PITTSBURGH on June 30, 2013 | http://pubs.acs.org Publication Date: December 17, 1985 | doi: 10.1021/bk-1985-0268.ch020

316

THE CHEMISTRY OF ALLELOPATHY

(Figure 3) (173). Although these complexes are resistant to degradation and re-entry into the rhizosphere, some microorganisms and other microfauna can cause degradation of these complexes with potential phytotoxicity (185, 186). This concept is pertinent to t h i s discussion i n that xenobiotics and/or bound naturally occurring phenolics could be p o t e n t i a l pools of toxic compounds or allelochemics. I f these compounds are released from bound complexes, they may not only a f f e c t plants d i r e c t l y , but also a f f e c t rhizosphere organisms and microbial-root interactions. The nature and t o x i c i t y of these humus-bound residues is unresolved as is whether these polymeric substances are p o t e n t i a l l y b e n e f i c i a l or harmful. Although there is considerably more information on degradation and transformation of p o t e n t i a l allelochemicals than presented here, t h i s b r i e f presentation points to the importance of further research i n this area. Biochemical Sites and Modes of Action of Allelochemicals There are numerous reported e f f e c t s of various allelochemicals (phenolics) on plants, but r e l a t i v e l y l i t t l e work on e f f e c t s of these compounds on microorganisms. Even though some reports deal with physiological and biochemical e f f e c t s on these systems, most are concerned only with t o x i c i t y studies ( i . e . growth i n h i b i t i o n ) and don't consider possible s i t e s of action, or mode and mechanisms of action, especially at the molecular l e v e l . Allelochemical mode of action has been reviewed Q, 2_, 60^, 187) , and although mode of action studies have increased since 1966, there is a general void i n this allelochemical research area. Possible s i t e s of action f o r allelochemicals should be quite s i m i l a r , i f not i d e n t i c a l to those of herbicides. For plants these include e f f e c t s on: c e l l walls, membranes, major organelles (mitochondrion, chloroplast, nucleus, nucleolus, e t c . ) , major processes ( c e l l d i v i s i o n , photosynthesis, r e s p i r a t i o n , protein synthesis, lipid synthesis, etc.) and on key enzymes. For mode of action studies of allelochemicals on microorganisms most of these also apply. When the intimate associations of microorganisms with roots is considered, other important possible s i t e s of action of allelochemicals (and herbicides) are apparent. These are: biochemical and physiological action on mycorrhizal binding, i n f e c t i o n processes of nodulating bacteria, nodulation development, and important alterations of key enzyme a c t i v i t i e s associated with these processes. Allelochemical research i n these areas is woefully lacking. Summary and Conclusions To further c l a r i f y the actual r o l e , impact, and expression of a l l e l o p a t h i c phenomena i n natural environments, much more research

In The Chemistry of Allelopathy; Thompson, A.; ACS Symposium Series; American Chemical Society: Washington, DC, 1985.

Soil

HOAGLAND AND WILLIAMS

ALDOSE SUGAR

Microorganisms-Plant

AMINO

N-SUBSTITUTED GLYCOSYLAMINE

COMPOUND '

AMADORI

Root Associations

REARRANGEMENT

A

1-AMINO-I-DEOXY-2-KETOSE (1,2-ENOL F O R M )

DEHYDRATION

Downloaded by UNIV OF PITTSBURGH on June 30, 2013 | http://pubs.acs.org Publication Date: December 17, 1985 | doi: 10.1021/bk-1985-0268.ch020

• « -AMINO

ι

STRECKER DEGRADATION

ALDEHYDE

ACID

FRAGMENTATION

;

RE D U C T O N E S DEHYDROREDUCTONES FURFURALS

ι

FISSION PRODUCTS (ACETOL, DIACETYL, PYRUVALDEHYDE, ETC.)

I

I

I

AMINO

AMINO

COMP'D

COMP'D

i

i

JBSW^^JITROGENO^

Figure 2. Scheme f o r formation of nitrogenous polymers i n s o i l s by condensation of amino acids with polyphenols and sugars. (From ACS Symposium Series No. 29, 1976) (173).

PHENOXYALKANOIC ACIDS

PHENOLIC

PHENYLCARBAMATES PHENYL UREAS

CONSTITUENTS

AMINES

0

ENZYMATIC

NH

• ENZYMATIC

?

CHEMICAL .

-C'O'5 FtOM O.M

HUMIC-LIKE SUBSTANCES ' Environmental Quality

Figure 3. Proposed chemical reactions leading to s t a b i l i z a t i o n of phenylamide, phenylcarbamate and phenylurea pesticides i n soils. (From ACS Symposium Series No. 29, 1976) (173).

In The Chemistry of Allelopathy; Thompson, A.; ACS Symposium Series; American Chemical Society: Washington, DC, 1985.

Downloaded by UNIV OF PITTSBURGH on June 30, 2013 | http://pubs.acs.org Publication Date: December 17, 1985 | doi: 10.1021/bk-1985-0268.ch020

318

THE CHEMISTRY OF ALLELOPATHY

and information is needed on several parameters. Highly e f f e c t i v e methods for i s o l a t i o n , i d e n t i f i c a t i o n , p u r i f i c a t i o n , and quantitation of allelochemicals (both water soluble and insoluble) i n s o i l s are available, but are not used i n most allelochemical studies. Use of these techniques is a prerequisite for needed molecular modes of action research. Determination of pool s i z e , turnover rate and degradation pathways (fate) of allelochemics i n s o i l s would also provide much insight. Effects of allelochemicals on rhizosphere microflora, and i n p a r t i c u l a r on mycorrhizae are needed. Knowledge of possible modification of root exudates by rhizosphere microflora and the biochemistry and physiology of mycorrhizal-root associations (especially on i n f e c t i o n processes, nodulation, the impact of hyphal bridge formation, etc.) could provide major breakthroughs. Since turnover of allelochemical pools, and plant and microbial growth are dynamic processes, the dynamic nature of soil and the environment should be considered for possible a l l e l o p a t h i c interactions among plants. Further a l l e l o p a t h i c research should consider the e f f e c t s of multiple allelochemicals because there are interactions of allelochemicals on both the target plant and rhizosphere organisms (188, 189). Interactions between allelochemicals and f e r t i l i t y , moisture stress and shading on plant growth should also be investigated. To accomplish these goals, the expertise of several d i s c i p l i n e s is needed; i . e . , chemistry, plant physiology, and soil microbiology. The information presented here shows that rhizosphere microorganisms play a major r o l e i n the production and metabolism of secondary plant compounds, especially phenolics. The rhizosphere contains numerous organisms that have d i r e c t and i n d i r e c t associations with major crop and weed species. Some of these associations play major roles i n plant nitrogen metabolism, nutrient uptake, and water r e l a t i o n s . Microorganisms that form associations with plant roots are sensitive and are affected by various factors (water stress, water logging, soil aeration, temperature, pH, a g r i c u l t u r a l chemicals, and naturally occurring plant materials). Studying e f f e c t s of allelochemicals i n soil only on plant roots, seed germination, etc., may not give an accurate appraisal of t o x i c i t y , s i t e of action, or mechanisms of action because of the intimate and complex nature of the rhizosphere. This complexity is further demonstrated by considering a series of 31 transfer pathways that interconnect plants, animals, soil organic matter, and soil mineral pools (190). Acknowledgment s The authors thank Ruth Jones and Doris McKenzie for t h e i r excellent assistance i n literature-searching. Judy Fava is thanked for her expert and rapid typing of the manuscript.

In The Chemistry of Allelopathy; Thompson, A.; ACS Symposium Series; American Chemical Society: Washington, DC, 1985.

Downloaded by UNIV OF PITTSBURGH on June 30, 2013 | http://pubs.acs.org Publication Date: December 17, 1985 | doi: 10.1021/bk-1985-0268.ch020

20.

HOAGLAND AND WILLIAMS

Soil Microorganisms-Plant Root Associations

319

Literature Cited 1. Rice, E. L. "Allelopathy"; Academic Press: New York, 1974. 2. Rice, E. L. Bot. Review 1979, 45, 15-109. 3. Odum, E. P. "Fundamentals of Ecology"; W. B. Saunders: Philadelphia, 1959, p. 257. 4. Stevenson, F. J. In "Nitrogen in Agricultural Soils"; Stevenson, FJ.,Ed., Am. Soc. Agronomy: Madison, Wisc., 1982; chap. 1 & 3. 5. Sprent, J. I. In "Advanced Plant Physiology"; Wilkins, M. B., Ed., Pitman Publ. Ltd: London, 1984; chap. 12. 6. Papavizas, G.C.;Davey, C. B. Plant Soil 1961, 215-236. 7. Bowen, G. D.; Rovira, A. D. Annual Rev. Phytopathol. 1976, 14, 121-144. 8. Rovira, A. D.; Davey, C. B. In "The Plant Root and Its Environment"; Carson, E.W., Ed., Univ. of Virginia Press: Charlottesville, 1974; chap. 7. 9. Bowen, G. D.; Rovira, A. D. In "Modern Methods in the Study of Microbial Ecology"; Rosswall, T., Ed.; Swedish Natural Science Research Council: Stockholm, 1973; pp. 443-450. 10. Hale, M. G.; Moore, L. D.; Griffin, G. J. In "Interactions Between Non-pathogenic Soil Microorganisms and Plants"; Dommergues, Y. R.; Kenpa, S. V., Eds., Elsevier: Amsterdam; 1978; pp. 163-203. 11. Bowen, G. D. In "Soil-Borne Plant Pathogens"; Schippers, B.; Gams, W., Eds.; Academic Press: New York, 1979; pp. 209-227. 12. Parkinson, D. In "Soil Biology"; Burges, Α.; Raw, R., Eds.; Academic Press: New York, 1967; Chap. 15. 13. Mosse, B.; Stribleny, D.P.; LeTacon, F. In "Advances in Microbial Ecology"; Alexander, M., Ed.: Plenum Press: New York, 1981; Chap. 4. 14. Moser, M.; Haselwandter, K. In "Physiological Plant Geology III": Lange,O.L.; Nobel, P. S.; Osmond, C. B.; Ziegler, H., Eds., Springer-Verlag; New York; 1983; Chap. 9. 15. Marks, G.C.;Kozlowski, T. T., Eds. "Ectomycorrhizae"; Academic Press: New York, 1973. 16. Harley, J. L. "The Biology of Mycorrhiza"; Lenard Hill: London, 1969 (334 pages). 17. Harley, J. L.; Smith, S. E. "Mycorrhizal Symbiosis"; Academic Press: New York, 1983. 18. Sanders, F. E.; Mosse, B.; Tinker, P. B., Eds. "Endomycorrhizas"; Academic Press: New York, 1975. 19. Rouatt,J.W. Can.J.Microbiol. 1959,_5,67-71. 20. Starkey, R. L. Soil Sci. 1929, 27, 319-334. 21. Starkey, R. L. Soil Sci. 1929, 27, 355-378. 22. Starkey, R. L. Soil Sci. 1929, 27, 433-444. 23. Gyllenberg, H. Can.J.Microbiol. 1957, 3, 131-134.

In The Chemistry of Allelopathy; Thompson, A.; ACS Symposium Series; American Chemical Society: Washington, DC, 1985.

Downloaded by UNIV OF PITTSBURGH on June 30, 2013 | http://pubs.acs.org Publication Date: December 17, 1985 | doi: 10.1021/bk-1985-0268.ch020

320

THE CHEMISTRY OF ALLELOPATHY

24. Lochhead, A. G.; Rouatt, J. W. Proc. Soil Sci. Soc. Am. 1955, 19 48-49. 25. Gerdemann, J. W. In "The Plant Root and Its Environment"; Carson, E. W., Ed.; Univ. of Virginia Press: Charlottesville, 1974; Chap. 8. 26. Gerdemann, J. W. In "The Development and Function of Roots"; Torrey, J. G.; Clarkson, D. T., Eds.; Academic Press: London, 1975, pp. 575-591. 27. Mosse, B. Ann. Rev. Phytopathol. 1973, 11, 171-196. 28. Hayman, D. S. Can. J. Bot. 1983, 61, 944-963. 29. Gerdemann, J. W. Ann. Rev. Phytopathol. 1968, 6, 397-418. 30. Khan, A. G. New Phytol. 1972, 71, 613-619. 31. Powell, C. L.; Daniel, J. Ν. Z. J. Agric. Res. 1978, 21, 675. 32. Yost, R. S.; Fox, R. L. Agron. J. 1982, 74, 475-481. 33. Yost, R. S.; Fox, R. L. Agron. J. 1979, 71, 903-908. 34. Mosse, B. New Phytol. 1973, 72, 127-136. 35. Mosse, B. New Phytol. 1977, 78, 277-288. 36. Ross, J. P.; Gilliam, J. W. Soil Sci. Soc. Am. J. 1973, 37, 237-239. 37. Guttay, A. J. R. J. Amer. Soc. Hort. Sci. 1983, 108, 222-224. 38. Gray, L. E.; Gerdemann, J. W. Plant Soil 1973, 39, 687. 39. Rhodes, L. H.; Gerdemann, J. W. Soil Biol. Biochem. 1978, 10, 361-364. 40. McIlveen, W. D.; Spotts, R. Α.; Davis, D. D. Phytopath. 1975, 65, 645. 41. Powell, D. L. in "Endomycorrihizas"; Sanders, F. E.; Mosse, B.; Tinker, P. Β., Eds.; Academic Press: New York, 1975, pp. 461-468. 42. Ross, J. P. Phytopath. 1971, 61, 1400-1403. 43. Hiriel, M. C.; Gerdemann, J. W. Soil Sci. Soc. Am. J. 1980, 44, 654-655. 44. Safir, G. R.; Boyer, J. S.; Gerdemann, J. W. Science 1971, 172, 581-583. 45. Safir, G. R.; Boyer, J. S.; Gerdemann, J. W. Plant Physiol. 1972, 49, 700-703. 46. Nelsen, C. E.; Safir, G. R. Planta 1982, 154, 407-413. 47. Green, Ν. E.; Smith, M. D.; Beavis, W. D.; Aldon, E. F. J. Range Management 1983, 36, 576-578. 48. Rovira, A. D. Plant Soil 1956, 7, 178-194. 49. Rouatt, J. W.; Katznelson, H. Nature 1960, 186, 659-660. 50. Peterson, E. A. Can. J. Microbiol. 1961, 7, 2-6. 51. Hale, M. G.; Foy, C. L.; Shay, F. J. In "Advances in Agronomy"; Brady, N. C. Ed.; Academic Press: New York, 1971; Vol. 23, pp. 89-109. 52. Hale, M. G.; Moore, L. D. In "Advances in Agronomy", Brady, N. C. Ed., Academic Press: New York, 1979; Vol. 31, pp. 93-124.

In The Chemistry of Allelopathy; Thompson, A.; ACS Symposium Series; American Chemical Society: Washington, DC, 1985.

Downloaded by UNIV OF PITTSBURGH on June 30, 2013 | http://pubs.acs.org Publication Date: December 17, 1985 | doi: 10.1021/bk-1985-0268.ch020

20.

HOAGLAND AND WILLIAMS

Soil Microorganisms-Plant

Root Associations

321

53. Muller, C. H. In "Biochemical Interactions Among Plants"; National Academy of Sciences: Washington, D.C., 1971; pp. 64-71. 54. Hoffman, G. R.; Hazlett, D. L. J. Range Management 1977, 30, 134-137. 55. Weaver, T. W.; Klavich, D. Am. Midland. Nat. 1977, 97, 508-512. 56. L i l l , R. E.; Waid, J. S. Ν. Z.J.For. Sci. 1975, 5, 165-170. 57. Martin, J. P. Aust. J. Biol. Sci. 1971, 24, 1131-1142. 58. Whittaker, R. H.; Feeny, P. P. Science 1971, 171, 757-770. 59. Swain, T. Ann. Rev. Plant Physiol. 1977, 28, 479-501. 60. Moreland, D. E.; Egley, G. H.; Worsham, A. D.; Monaco, T. J. Adv. in Chemistry 1966, 53, 112-141. 61. Moje, W. In "Diagnostic Criteria for Plants & Soils"; Chapman, H. D., Ed.; Univ. Calif. Press: Berkeley, 1966, pp. 533-569. 62. Hoagland, R. E.; Duke, S. O. In "Biochemical Responses Induced by Herbicides"; Moreland, D. E.; St. John,J.B.; Hess, F. D., Eds., Amer. Chem. Soc.: Washington, D.C., 1982; pp. 175-205. 63. Drost, D.C.;Doll, J. D. Weed Sci. 1980, 28, 229-233. 64. Jangaard, N.O.;Sckerl, M. M.; Schieferstein, R. H. Weed Sci. 1971, 19, 17-20. 65. Friedman, T.; Horowitz, M. Weeds 1971, 19, 398-401. 66. Colton, C. E.; Einhellig, F. A. Amer.J.Bot. 1980, 67, 1407-1413. 67. Elmore, C. D. Weed Sci. 1980, 28, 658-660. 68. Bokhari, U. G. Ann. Bot. 1978, 42, 127-136. 69. Jackson, J. R.; Willemsen, R. W. Amer. J. Bot. 1976, 63, 1015-1023. 70. Schumacher, W.J.;Thill D.C.;Lee, G. A. J. Chem. Ecol. 1983, 9, 1235-1245. 71. Tinnin, R.O.;Muller, C. H. Bull. Torrey Bot. Club 1972, 99 287-292. 72. Bonasera,J.;Lynch,J.;Leek, M. A. Bull. Torrey Bot. Club 1979, 106, 217-222. 73. Campbell, G.; Lambert,J.D. H.; Arnason, T.; Towers, G. H. N. J. Chem. Ecol. 1982, 8, 961-972. 74. Chu, C.-H.; Young, C.-C. J. Chem. Ecol. 1975, 1, 183-193. 75. Alsaadawi, I. S.; Rice, E. L. J. Chem. Ecol. 1982, 8, 1011-1023. 76. Parenti, R. L.; Rice, E. L. Bull. Torrey Bot. Club 1969, 96, 70-78. 77. Schreiber, M. M.; Williams, J. L., Jr. Weeds 1967, 15, 80-81. 78. Ballester, Α.; Vieitez, A. M.; Vieitez, E. Bot. Gaz. 1979, 140, 433-436. 79. Irons, S. M.; Burnside, O. C. Weed Sci. 1982, 30, 372-377.

In The Chemistry of Allelopathy; Thompson, A.; ACS Symposium Series; American Chemical Society: Washington, DC, 1985.

Downloaded by UNIV OF PITTSBURGH on June 30, 2013 | http://pubs.acs.org Publication Date: December 17, 1985 | doi: 10.1021/bk-1985-0268.ch020

322

THE CHEMISTRY OF ALLELOPATHY

80. Schon, M. K.; Einhellig, F. A. Bot. Gaz. 1982, 143, 505-510. 81. Wilson, R. E.; Rice, E. L. Bull. Torrey Bot. Club 1969, 95, 432-448. 82. Lodhi, Μ. A. K. Can.J.Bot. 1979, 57, 1083-1088. 83. Datta, S.C.;Chatterjee, A. K. Flora 1980, 169, 456-465. 84. Einhellig, F. Α.; Rasmussen, J. A. Amer. Midl. Nat. 1973, 90, 79-86. 85. Abdul-Wahab, A. S.; Rice, E. L. Bull. Torrey Bot. Club 1967, 94, 486-497. 86. Lolas, P.C.; Coble, H. D. Weed Sci. 1982, 30, 589-593. 87. Caussanel,J.-P.;Kunesch, G. Z. Pflanzenphysiol. 1979, 93, 229-243. 88. Tang, C.-S.; Young, C.-S. Plant Physiol. 1982, 69, 155-160. 89. Alsaadawi, I.S.; Rice, E. L.; Karns, T. Κ. B. J. Chem. Ecol. 1983, 9, 761-775. 90. Lovett, J. V.; Levitt,J.;Duffield, A. M.; Smith, N. G. Weed Res. 1981, 21, 165-170. 91. Gliessman, S. R. Bot.J.Linn. Soc. 1976, 73, 95-104. 92. Gliessman, S. R.; Muller, C. H. J. Chem. Ecol. 1978, 4, 337-362. 93. Stewart, R. E. J. Chem. Ecol. 1975, 1, 161-169. 94. Lodhi, M. A. K. J. Chem. Ecol. 1979, 5, 429-437. 95. Friedman,J.;Rushkin, E.; Waller, G. R. J. Chem. Ecol. 1982, 8, 55-65. 96. Gressel,J.B.; Holm, L. G. Weed Res. 1964, 4, 44-53. 97. Gabor, W. E.; Veatch, C. Weed Sci. 1981, 29, 155-159. 98. Kommedahl, T.; Old, K. M.; Ohman,J.H.; Ryan, E. W. Weed Sci. 1970, 18, 29-32. 99. Oswald, H. J. Ecol. 1948, 36, 192-193. 100. Penn, D.J.;Lynch, J. M. J. Appl. Ecol. 1981, 18, 669-674. 101. Toai, T. V.; Linscott, D. L. Weed Sci. 1979, 27, 595-598. 102. Hoffman, G.R.; Hazlett, D. L. J. Range Management 1977, 30, 134-137. 103. Muller, W. H.; Hauge, R. Bull. Torrey Bot. Club 1967, 94, 182-191. 104. Lovett, J. V.; Sagar, G. R. New Phytol. 1978, 81, 617-625. 105. Ras, V. R.; Ras, N. S. S.; Mukerji, K. G. Plant & Soil 1973, 39, 449-452. 106. Husaina, Α.; Mallik, M. A. B. J. Sci. 1972, 1, 139-145. 107. Munro, P. E. J. Appl. Ecol. 1966, 3, 227-229. 108. Munro, P. E. J. Appl. Ecol. 1966, 3, 231-238. 109. Jobidon, R.; Thibault,J.-R.Amer.J.Bot. 1982, 69, 1213-1223. 110. Thibault,J.-R.;Fortin,J.-Α.;Smirnoff, W. A. Amer.J.Bot. 1982, 69, 676-679. 111. Lodhi, M. A. K.; Killingbeck, K. T. Amer.J.Bot. 1980, 67, 1423-1429. 112. Murthy, M. S.; Nagodra, T. J. Appl. Ecol. 1977, 14, 279-282.

In The Chemistry of Allelopathy; Thompson, A.; ACS Symposium Series; American Chemical Society: Washington, DC, 1985.

Downloaded by UNIV OF PITTSBURGH on June 30, 2013 | http://pubs.acs.org Publication Date: December 17, 1985 | doi: 10.1021/bk-1985-0268.ch020

20. HOAGLAND AND WILLIAMS Soil Microorganisms-Plant Root Associations 113. Murthy, M. S.; Ravindra, R. Oecologia 1974, 16, 257-258. 114. Murthy, M. S.; Ravindra, R. Oecologia 1975, 18, 243-249. 115. Rychert, R. C.; Skujins, J. Soil Sci. Soc. Amer. Proc. 1974, 38, 768-771. 116. Lewis, J. Α.; Papauizas, G. C. Soil Sci. 1974, 118, 156-163. 117. Chan, E. C. S.; Basavanand, P.; Liivak, T. Can. J. Microbiol. 1970,16,9-16. 118. Stiven, G. Nature 1952, 170, 712-713. 119. Chou, C.-H.; Lin, T.-J.; Kao, C.-I. Bot. Bull. Acad. Sinica 1977, 18, 45-60. 120. Tan, K. H.; Tantiwiramanond, D. Soil Sci. Soc. Amer. J. 1983, 47, 1121-1124. 121. Angle, J. S.; Pugashetti, Β. K.; Wagner, G. H. Agron. J. 1981, 73, 301-306. 122. Robinson, R. K. J. Ecol. 1972, 60, 219-224. 123. Rice, E. L. Ecology 1964, 45, 824-837. 124. Rice, E. L. Physiol. Plant. 1965, 18, 255-268. 125. Rice, E. L.; Parenti, R. L. Southwest. Nat. 1967, 12, 97-103. 126. Floyd, G. L.; Rice, E. L. Bull. Torrey Bot. Club 1967, 94, 125-129. 127. Rice, E. L. Bull. Torrey Bot. Club 1968, 95, 346-358. 128. Rice, E. L. Amer. J. Bot. 1971, 58, 368-371. 129. Rice, E. L.; Pancholy, S. K. Amer. J. Bot. 1973, 60, 691-702. 130. Rice, E. L.; Pancholy, S. K. Amer. J. Bot. 1974, 61, 1095-1103. 131. Rice, E. L.; Lin, C.-Y.; Huang, C.-Y. Bot. Bull. Acad. Sinica 1980, 111-117. 132. Olsen, R. Α.; Odham, G.; Lindberg, G. Physiol. Plant. 1971, 25, 122-129. 133. Hattingh, M. J.; Louw, H. A. Can. J. Microbiol. 1969, 15, 361-364. 134. Damergi, S. M.; Johnson, H. W. Agron. J. 1966, 58, 223-224. 135. Elkan, G. H. Can. J. Microbiol. 1961, 7, 851-856. 136. Barea, J. M.; Brown, M. E. J. Appl. Bact. 1974, 37, 583-593. 137. Schenck, S.; Stotzky, G. Can. J. Microbiol. 1975, 21, 1622-1634. 138. Menzies, J. D.; Gilbert, R. G. Soil Sci. Soc. Amer. Proc. 1967, 31, 495-496. 139. Sullia, S. B. Geobios 1974, 1, 175-177. 140. Rhodes, L. H.; Gerdemann, J. W. New Phytol. 1975, 75, 555-561. 141. Crush, J. R. New Phytol. 1974, 73, 743-749. 142. Fitter, A. H. New Phytol. 1977, 79, 119-125. 143. Hatling, M. S.; Gray, L. E.; Gerdemann, J. W. Soil Sci. 1973, 116, 383-387.

In The Chemistry of Allelopathy; Thompson, A.; ACS Symposium Series; American Chemical Society: Washington, DC, 1985.

3

Downloaded by UNIV OF PITTSBURGH on June 30, 2013 | http://pubs.acs.org Publication Date: December 17, 1985 | doi: 10.1021/bk-1985-0268.ch020

324

THE CHEMISTRY OF ALLELOPATHY

144. Glass, A. D. M. Plant Physiol. 1973, 51, 1037-1041. 145. Glass, A. D. M. Phytochem. 1975, 14, 2127-2130. 146. Glass, A. D. M. J. Exp. Bot. 1974, 25, 1104-1113. 147. Hutchinson, S. A. Trans. Brit. Mycol. Soc. 1971, 57, 185-200. 148. Stotzky, G.; Schenck, S. Can. J. Microbiol. 1976, 21, 1622-1634. 149. Goring, C. A. I.; Clark, F. E. Soil Sci. Soc. Amer. Proc. 1948,13,261-266. 150. Molina, J. A. E.; Rovira, A. D. Can. J. Microbiol. 1964, 10, 249-257. 151. Moore, D. R. E.; Waid, J. S. Soil Biol. Biochem. 1971, 3., 69-83. 152. Theron, J. J. J. Agr. Sci. 1951, 41, 289-296. 153. Purchase, B. S. Plant & Soil 1974, 41, 527-539. 154. Purchase, B. S. Plant & Soil 1974, 41, 541-547. 155. Sowden, F. J. Soil Sci. 1969, 107, 364-371. 156. Sowden, F. J. Can. J. Soil Sci. 1970, 50, 227-232. 157. Borner, H. Bot. Rev. 1960, 26, 393-424. 158. Wang, T. S. C.; Yeh, K. L.; Cheng, S. Y.; Yang, T. K. In "Biochemical Interactions Among Plants"; Nat'l. Acad. Sciences: Washington, 1971; pp. 113-120. 159. Dagley, S. In "Soil Biochemistry"; McLaren, A. D.; Peterson, G. H., Eds.; Marcel Dekker: New York, 1967; pp. 289-317. 160. Turner, J. Α.; Rice, E. L. J. Chem. Ecol. 1975, 1, 41-58. 161. Whitehead, D. C. Nature, London 1964, 202, 417-418. 162. Vaughan, D.; Ord, B. G. Soil Biol. Biochem. 1980, 12, 449-450. 163. Knosel, D. Zeit. Pfanzenernahrung Bodenkunde 1959, 85, 58-66. 164. Batistic, L.; Mayaudon, J. Anns. l'Itst. Pasteur 1970, 118, 190-206. 165. Sparling, G. P.; Ord, B. G.; Vaughan, D. Soil Biol. Biochem. 1981, 13, 455-460. 166. Sparling, G. P.; Vaughan, D. J. Sci. Food Agric. 1981, 32, 625-626. 167. Vaughan, D.; Sparling, G. P.; Ord, B. G. Soil Biol. Biochem. 1983, 15, 613-614. 168. Henderson, M. E. K.; Farmer, V. C. J. Gen. Microbiol. 1955, 12, 37-46. 169. Guenzi, W. D.; McCalla, T. M. Proc. Soil Sci. Soc. Amer. 1966, 30, 214-216. 170. Haider, K.; Martin, J. P.; Filip, Z. In "Soil Biochemistry"; Paul, Ε. Α.; McLaren, Α. D., Eds.; Marcel Dekker: New York, 1975; pp. 195-224. 171. Parsons, J. W.; Tinsley, J. In "Soil Components"; Gieseking, J. Ε., Ed.; Spring-Verlag: New York, 1975; pp. 263-304.

In The Chemistry of Allelopathy; Thompson, A.; ACS Symposium Series; American Chemical Society: Washington, DC, 1985.

Downloaded by UNIV OF PITTSBURGH on June 30, 2013 | http://pubs.acs.org Publication Date: December 17, 1985 | doi: 10.1021/bk-1985-0268.ch020

20.

HOAGLAND AND WILLIAMS Soil Microorganisms-Plant Root Associations 172. Henderson, Μ. Ε. K. Pure Appl. Chem. 1963, 589-602. 173. Stevenson, F. J. In "Bound & Conjugated Pesticide Residues", Kaufman, D. D.; Still, G. G.; Paulson, G. D.; Bandai, S. Κ., Eds., Amer. Chem. Soc: Washington, D. C.; 1976; pp. 180-207. 174. Wang, T. S.C.;Li, S. W.; Ferng, Y. L. Soil Sci. 1978, 126, 15-21. 175. Hauang, P. M.; Wang, T. S.C.;Wang, M. K.; Wu, M. H.; Hsu, N. W. Soil Sci. 1977, 123, 213-219. 176. Shindo, H.; Kuwatsuka, S. Soil Sci. Plant Nutr. 1976, 22, 23-33. 177. Stowe, L. G.; Osborn, A. Can.J.Bot. 1980, 58, 1149-1153. 178. Oglesby, R. T.; Christman, R. F.; Driver, C. H. Adv. Appl. Microbiol. 1967, 9, 111-184. 179. Hurst, H. M.; Burges, N. A. In "Soil Biochemistry"; McLaren, A. D.; Peterson, G. Η., Eds.; Marcel Dekker: New York, 1967; pp. 260-286. 180. Martin, J. P.; Richards, S.J.;Haider, K. Soil Sci. Soc. Amer. Proc 1967, 31, 657-662. 181. Greenland, D. J. Soil Sci. 1971, 111, 34-41. 182. Martin, J. P.; Parsa, Α. Α.; Haider, K. J. Biol. Biochem. 1978, 40, 483-486. 183. Martin, J. P.; Haider, K. Soil Sci. Soc. Amer. J. 1976, 40, 377-380. 184. Haider, K.; Martin, J. P. Proc. Soil Sci. Soc. Amer. 1975, 39, 657-662. 185. Bollag,J.-M.;Loll, M. J. Experimentia 1983, 39, 1221-1231. 186. Kaufman, D. D.; Still, G. G.; Paulson, G. D.; Bandai, S. Κ., Eds. "Bound & Conjugated Pesticide Residues"; Amer. Chem. Soc: Washington, D. C., 1976. 187. Horsley, S. B. In "Proc. Fourth N. Amer. Forest Biology Workshop"; Wilcox, H. E.; Hamer, A. F., Eds.; State Univ. NY: Syracuse, 1977, pp. 93-136. 188. Einhellig, F. Α.; Rasmussen, J. A. J. Chem. Ecol. 1979, 5, 815-824. 189. Williams, R. D.; Hoagland, R. E. Weed Sci. 1982, 30, 206-212. 190. Frissel, M.J.,Ed. "Cycling of mineral nutrients in agricultural ecosystem". Elsevier Scientific Publ. Co: New York, 1978. RECEIVED August 10, 1984

In The Chemistry of Allelopathy; Thompson, A.; ACS Symposium Series; American Chemical Society: Washington, DC, 1985.