Allelopathic Effects on Mycorrhizae - American Chemical Society

C h a p t e r 17

Allelopathic Effects on Mycorrhizae Influence on Structure and Dynamics of Forest Ecosystems David A. Perry and Carolyn Choquette

Downloaded by UNIV OF NEW SOUTH WALES on April 11, 2016 | http://pubs.acs.org Publication Date: January 8, 1987 | doi: 10.1021/bk-1987-0330.ch017

Department of Forest Science, Oregon State University, Corvallis, OR 97331-5704

Ectomycorrhizal species differ in their sensitivity to allelochemicals originating in litter and soil organic material. This phenomenon produces a successional change in mycorrhizal species as ecosystems rebuild litter layers following disturbance, and possibly acts to structure rooting zones in such a way that competition among higher plants is decreased. Mycorrhizae alter foliage chemistry, and thus potentially form a closed loop in which they both act on, and are acted upon by, system biochemistry. A mycorrhiza (literally, fungus-root) is a symbiotic association between a fungus and a plant. Mycorrhizae occur most frequently on plant roots, but may be found on any tissue involved in uptake of elements from soil. Mycorrhizae, formed by numerous fungi in the orders Phycomycetes, Basidiomycetes, and Ascomycetes, can be divided into two broad groups: those that penetrate host cells (endomycorrhizae) and those that do not (ectomycorrhizae). A few fungal species defy this neat classification, penetrating the cells of one host but not those of another. Among the endomycorrhizae, the most common are those that, because of distinctive structures produced by the fungus, are called vesicular-arbuscular mycorrhizae (VAM). VAM are Phycomycetes of the family Endogonaceae, and may occur on trees, shrubs, or herbs, and in any plant phyla (1). Ectomycorrhizae (EM), formed by numerous species of Basidiomycetes, Ascomycetes, and Phycomycetes, are distributed less widely in the Plant Kingdom than VAM. Although EM have been reported on herbs, principal hosts are trees and woody shrubs, particularly Gytnnosperms and Angiosperms of the families Betulaceae and Fagaceae (1). Most of the important commercial tree species of the temperate zone are ectomycorrhizal. Despite their relatively narrow host range, EM fungi are highly diverse. At least 5000 species of fungi form EM, compared to fewer than 30 forming VAM (2). 0097-6156/87/0330-0185$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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ALLELOCHEMICALS: ROLE IN AGRICULTURE AND FORESTRY

Over 90 percent of the roughly 200 plant families so far investigated form mycorrhizae and for many the relationship i s obligate (3). Mycorrhizae d i r e c t l y benefit host plants by increasing water and nutrient ( p a r t i c u l a r l y phosphorus) uptake, increasing the l i f e t i m e of feeder roots, and protecting against root pathogens. The ecological role of mycorrhizae i s i n general poorly understood, but they are l i k e l y to mediate competitive r e l a t i o n s between higher plants (4-6), a l t e r plant p a l a t a b i l i t y to herbivores (5, 7^), and influence the physical structure of s o i l s (8). The l a t t e r point i s p a r t i c u l a r l y important i n s o i l s with low clay content, i n which v i r t u a l l y a l l aggregation and consequently water-holding capacity and porosity may r e s u l t from the a c t i v i t y of mycorrhizae and associated rhizophere organisms ( e . g . , 9, 10). For most of the world's plants mycorrhizae are the primary interface between p h y s i o l o g i c a l l y active areas of the root and the external environment. Hence i t i s l i k e l y that many, perhaps most, allelochemical interactions involving higher plant roots are mediated by the fungal symbiont. Herein we b r i e f l y review past research dealing with a l l e l o p a t h i c effects on mycorrhizae, and discuss how i n t e r a c t i o n between mycorrhizae and chemicals may influence s t r u c t u r a l and functional aspects of ecosystems. Most studies to date have dealt with EM i n forest ecosystems, and t h i s i s where our discussion w i l l focus. A l l e l o p a t h i c Effects on Mycorrhizae A l l e l o p a t h i c effects on mycorrhizae have been known for 40 years. Melin (11) demonstrated that EM were i n h i b i t e d by ethanol-soluble, heat-stable, substances contained i n l i t t e r of Scots pine (Pinus s y l v e s t r i s ) and various deciduous tree species. Since then various workers have shown i n h i b i t i o n of EM by organic matter or water-soluble extracts from l i t t e r or roots (12-19). EM may also be i n h i b i t e d by some Streptomyces species (20). Mikola (21) found that the degree of i n h i b i t i o n of EM by leaf and l i t t e r leachates varied with concentration: low concentrations actually stimulated growth of Cenococcum Reophilum and Lactarius tomintosus. A l l e l o p a t h i c effects on EM vary not only with concentration, but are highly s p e c i f i c to fungal species and nature of the allelochemical as w e l l . Tan and Nopamornbodi (22) found that several f u l v i c acids and s o i l extracts stimulated growth of P i s o l i t h u s t i n c t o r i u s , a fungus that i s also i n h i b i t e d by leachates from a number of l i t t e r s . Rose et a l (2_3), studying the influence of water-soluble leachates from various types of l i t t e r on growth of four EM fungi, found a highly s i g n i f i c a n t i n t e r a c t i o n between EM species, l i t t e r type, and concentration. A l l e l o p a t h i c effects on EM may produce s t r i k i n g changes i n plant communities. Widespread f a i l u r e of Sitka spruce (Picea sitchensis) plantations i n Scotland was attributed to i n h i b i t i o n of spruce EM by substances leaching from heather (Calluna vulgaris) roots and/or raw humus (12). In Finland, unidentified substances leached from reindeer lichen (Cladina sp.) i n h i b i t EM formation on various tree species (24). Trees growing i n the absence of lichen cover may be up to 20 times as large as trees growing with lichen (25). In other cases effects are more subtle, with allelopaths



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a l t e r i n g EM composition rather than causing outright f a i l u r e of EM formation. Schoeneberger and Perry (19) found that leachates from the l i t t e r of an Oregon forest reduced formation of a single EM type on Douglas-fir (Pseudotsuga menziesii), while EM of Western hemlock (Tsuga heterophylla) were unaffected. L i t t e r from a nearby, very s i m i l a r , forest had no effect. This d i s p a r i t y i n r e s u l t s i s not unusual; while most studies have found that organic material i n h i b i t s EM, some find just the opposite—stimulation of EM by organic material (26, 27). Such differences are probably due largely to the highly s p e c i f i c nature of the allelopath-EM r e l a t i o n s h i p , although p h y s i o l o g i c a l vigor of the a l l e l o p a t h producing plant also plays a role (12). Our work has consistently shown that trees of a given species form different proportions of EM types depending on whether they are grown i n s o i l s from undisturbed forest or from clearcuts, and that the r e l a t i v e frequency of types formed i n the l a t t e r depends on whether logging slash was burned or not. More research i s needed, but the most l i k e l y explanation f o r these observations i s that s o i l s from plant communities i n different stages of succession, or that have experienced different types of disturbance, vary i n t h e i r c h a r a c t e r i s t i c chemical signature, and t h i s i n turn influences the type of EM forming on seedlings. Apparently a variety of chemical compounds i n h i b i t EM. Olsen et. a l . (15) i d e n t i f i e d benzoic acid and catechol as the EM i n h i b i t o r s present i n aspen leaves (Populus tremula). They also showed that fungi decomposing wood and l i t t e r were less sensitive to these compounds than EM, and speculated that t h i s may be due to greater production of e x t r a c e l l u l a r phenol oxidases by the decomposer groups. Harley and Smith (1) suggest that the d i f f e r e n t i a l s u s c e p t i b i l i t y to allelochemicals that occur among EM species may be related to production of phenol oxidases. Melin and Krupa (28) found i n h i b i t i o n of EM by several mono- and sesquiterpenes present i n Scots pine (Pinus s y l v e s t r i s ) roots, although the two fungi they tested differed i n t h e i r response to i n d i v i d u a l compounds. Relatively l i t t l e work has been done on a l l e l o p a t h i c effects on VAM. Tobiessen and Werner (29) found reduced VAM formation i n hardwood tree seedlings growing under pines, and spores of VAM fungi are absent from s o i l beneath l i v i n g ponderosa pines, although they are abundant under dead trees (30). Members of the nonmycorrhizal family Cruciferae sometimes i n h i b i t VAM formation i n associated plants though t h i s doesn't always happen (31-34). Influence on Succession Temperate forests are characterized by periodic catastrophic disturbance. Often t h i s i s due to f i r e , but various other agents such as wind and volcanic eruption also are responsible. Disturbance may influence the allelochemical environment i n various ways. Living biomass i s reduced, and f i r e reduces or eliminates l i t t e r and humus layers as w e l l . Hence we should expect the t o t a l production of allelochemicals to be lowered following disturbance. As succession proceeds and t o t a l biomass and l i t t e r layers r e b u i l d ,



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allelochemicals should become an increasingly important factor i n the ecosystem. There are l i k e l y to be q u a l i t a t i v e as well as quantitative changes i n allelochemicals during succession. Incomplete combustion of organic matter produces various polynuclear aromatic hydrocarbons, many of which are mutagens, carcinogens, or protocarcinogens (35). F i r e dramatically a l t e r s the microflora of forest s o i l s , increasing the r a t i o of bacteria to fungi and a l t e r i n g the proportion of Streptomycetes spp. that i n h i b i t root pathogens or mycorrhizal fungi (20). Concentrations of hydroxymate siderophores (HS), an important class of iron chelators, are reduced by disturbance, p a r t i c u l a r l y f i r e (36_). Because iron oxides play a role i n the breakdown of phenolic compounds (H. H. Chang, personal communication), lower levels of HS may well influence allelochemical i n t e r a c t i o n s . F i n a l l y the change i n plant species that defines a successional sequence undoubtedly produces temporal differences i n the nature of allelochemicals. The diverse nature of mycorrhizal response to allelochemicals suggests that the changing biochemical environment during succession may drive a successional sequence of mycorrhizal fungi. It i s well established that a sequence of mycorrhizal species occurs on a given tree as i t matures (37^, 38), and i n one case t h i s has been linked to the buildup of l i t t e r around trees (39). S e n s i t i v i t y of mycorrhizal species to l i t t e r leachates correlates well with what we know about t h e i r ecological r o l e . For example, Rose et a l (23) found that growth of P i s o l i t h u s t i n c t o r i u s i n pure culture was i n h i b i t e d by a wide range of l i t t e r types, while that of Cenococcum seophilum was stimulated. The former species i s a rapid grower that greatly aids survival and growth of trees on highly disturbed s i t e s such as mine spoils while the l a t t e r has c h a r a c t e r i s t i c s , such as an a b i l i t y to infect roots of plants grown under low l i g h t , that make i t p a r t i c u l a r l y suited for mature forest conditions. It i s d i f f i c u l t to avoid concluding that P. t i n c t o r i u s i s an early successional fungus, adapted to the low allelochemical environment of recently disturbed s i t e s , while Ç. geophilum i s a late successional species that t h r i v e s , and perhaps even depends, on allelochemicals. In our studies we find that, where more than one mycorrhizal fungus occurs i n the system, disturbance invariably results i n a s h i f t i n the proportion of types that are formed on tree seedlings (5, 19, 40). For example, i n high-elevation forests growing on g r a n i t i c s o i l s i n southern Oregon, two mycorrhizal types predominate on Douglas-fir seedlings, an unidentified species that we c a l l "brown," and Rhizoposon v i n i c o l o r . Ninety-five percent of the mycorrhizae on seedlings grown i n s o i l s from mature forests are "brown". When seedlings are grown under the same conditions, but with s o i l from an adjacent clearcut i n which logging slash had been burned (standard p r a c t i c e ) , the proportion changes to 22% "brown" and 68% R. v i n i c o l o r . Evidence suggests that t h i s change i s at least p a r t i a l l y related to destruction of the upper s o i l layers, which contain a large proportion of organic matter. When Rose e t . a l . (23) added l i t t e r leachates to Douglas-fir seedlings grown i n s o i l containing both R. v i n i c o l o r and "brown," colonization of roots by R. v i n i c o l o r was inhibited while "brown" was either



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unaffected or stimulated. Comparison of s o i l s between mature forest and disturbed s i t e s suggests at least one mechanism by which t h i s change i n fungus occurs. The former i s characterized by a heavily organic surface layer 20 to 30 cm deep, overlying a sandy mineral zone. The boundary between the two i s quite d i s t i n c t , and i s emphasized by a predominance of roots and hyphae i n the upper zone. Bioassays show that "brown" i s the predominant mycorrhizal fungus i n t h i s organic layer. The clearcut s o i l , although i t s t o t a l carbon content d i f f e r s l i t t l e from the forest, has no coherent surface organic layer; t e x t u r a l l y i t s surface i s very s i m i l a r to the s o i l that i s found at depth i n the forest. R. v i n i c o l o r " i s i t s predominant mycorrhizal fungus (at least for D o u g l a s - f i r ) . Apparently, the buildup of the organic layer over time i n these forests r e s u l t s i n a p a r t i t i o n i n g of the two fungal species, the a l l e l o c h e m i c a l - i n s e n s i t i v e "brown" occupying the organic layers and the s e n s i t i v e R. v i n i c o l o r the lower mineral layers. Logging and f i r e destroys the organic layer, leaving R. v i n i c o l o r i n the mineral s o i l to serve as the primary fungus colonizing roots of invading tree seedlings. As l i t t e r and humus layers r e b u i l d , "brown" becomes the dominant mycorrhizae-former, at least i n the top 20 to 30 cm of s o i l . Empirical evidence suggests that, i n at least some cases, a l l e l o c h e m i c a l - i n s e n s i t i v e mycorrhizal fungi p r e f e r e n t i a l l y colonize late-successional trees. In pure culture experiments Cenococcum geophilum, which i s stimulated by l i t t e r leachates, r e a d i l y forms mycorrhizae both with early-successional Douglas-fir and late-successional western hemlock (41). However when these tree species are grown i n s o i l from either disturbed areas or mature forest, Ç. geophilum forms a much higher proportion of the t o t a l mycorrhizae of western hemlock than of Douglas-fir (19). This raises the i n t r i g u i n g p o s s i b i l i t y that the s h i f t i n mycorrhizal fungi that occurs during succession f a c i l i t a t e s change in higher plants. Effects on Rooting Structure and Interactions Among Plants Studies discussed e a r l i e r c l e a r l y show that a l l e l o p a t h i c influences on mycorrhizae may a l t e r the structure of communities by i n h i b i t i n g one or more plant species. The d i v e r s i t y of response to allelochemicals among mycorrhizal species suggests that rooting pattern may also be influenced by the biochemical background of soils. Such s t r u c t u r i n g , rather than increasing the l e v e l of interference among i n d i v i d u a l plants, could produce the opposite e f f e c t , d i s t r i b u t i n g roots throughout the s o i l volume and hence decreasing competition among individuals for water and nutrients. Such patterning would be strongest where plant species grown together tend to form different mycorrhizal types. For example, i n a mixture of Douglas-fir and Western hemlock the former, with a r e l a t i v e l y high percentage of a l l e l o c h e m i c a l - s e n s i t i v e mycorrhizae such as Rhizopogon v i n i c o l o r , would tend to root i n lower s o i l layers, while hemlock, with i t s a l l e l o c h e m i c a l - i n s e n s i t i v e symbiont Cenococcum geophilum, would root i n or close to surface organic layers. Because a single tree species may form several types of mycorrhizae that d i f f e r i n s e n s i t i v i t y to allelochemicals, t h i s



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mechanism of root dispersion and subsequent decrease in belowground competition could occur i n monospecific stands as w e l l . In order to test these ideas, we are growing Douglas-fir and ponderosa pine (Pinus ponderosa) in a Replacement Series. In t h i s standard design the t o t a l number of individuals i n a pot remains constant (12 in our case) while the proportion of each species varies. Our experiment actually involves four Replacement Series, one i n unpasteurized s o i l , one i n pasteurized s o i l i n which no mycorrhizae were added, one i n pasteurized s o i l with a s p e c i e s - s p e c i f i c mycorrhiza synthesized on each tree species (RhizopORon v i n i c o l o r on Douglas-fir and RhizopORon oechorubens on ponderosa pine), and one with four mycorrhizae i n the system, the two RhizoppRons plus the two generalists Laccaria laccata and Hebeloma crustiforme. S o i l s are from a mixed Douglas-fir ponderosa pine forest in southwestern Oregon. A and Β s o i l layers, plus l i t t e r , were l i f t e d separately i n the f i e l d and reconstructed in the pots to simulate natural conditions as c l o s e l y as possible. Five r e p l i c a t i o n s are being grown in a greenhouse with pots rotated weekly so that a l l treatments cycle p e r i o d i c a l l y through a l l bench locations. This experiment i s i n progress; however i n i t i a l results c l e a r l y show that interference between seedlings of the two tree species i s altered by addition of mycorrhizae to the system. Six months after being transplanted into the same pots, height growth of ponderosa pine i s suppressed by Douglas-fir in the absence of mycorrhizae (Figure l a ) . When each tree has i t s own mycorrhizal symbiont, however, t h i s trend i s reversed, ponderosa pine increasing in height with increasing proportions of Douglas-fir in the mix (Figure l b ) . Growth of Douglas-fir i s lower in unpasteurized than in pasteurized s o i l (Figure Id); In previous experiments we have found that Douglas-fir growth may be either i n h i b i t e d or stimulated by s t e r i l i z a t i o n , depending on s o i l type and disturbance h i s t o r y , and that t h i s may vary from one year to the next in a single s o i l (20, 42). Reinoculation of pasteurized s o i l indicates that t h i s i s not an a r t i f a c t of pasteurization. In contrast to Douglas-fir, ponderosa pine, when grown only with other ponderosa pine, performs at least as well in unpasteurized as in pasteurized s o i l . However, the presence of Douglas-fir has a much more depressing effect on pine height growth i n unpasteurized than in pasteurized s o i l . Reduced height growth of Douglas-fir may indicate greater root growth, and t h i s could create more competition between the two tree species, however t h i s i s pure speculation—at t h i s point we cannot explain why responses are so different between pasteurized and nonpasteurized s o i l . I n i t i a l results of the experiment support the hypothesis that mycorrhizal d i v e r s i t y influences interactions between plants. Isotope labeling now i n progress w i l l t e l l us whether this i s due to different rooting patterns, and future experiments w i l l s p e c i f i c a l l y address the role of allelochemical d i v e r s i t y on rooting pattern. Our r e s u l t s in nonpasteurized s o i l s simply emphasize what every s o i l b i o l o g i s t knows - patterns occurring i n nature are complex and include interactions among numerous organisms. There i s l i t t l e question that the belowground dynamic


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P a s t e u r i z e d s o i l w i t h no added m y c o r r h i z a e P a s t e u r i z e d s o i l w i t h two m y c o r r h i z a l s p e c i e s added P a s t e u r i z e d s o i l w i t h f o u r m y c o r r h i z a l s p e c i e s added Unpasteurized soil


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i s strongly influenced by allelochemicals, although the task of unraveling mechanisms i s l i k e l y to be a long one.


The Ecological Demon The d i v e r s i t y of response to allelochemicals that exists within the community of mycorrhizal fungi has considerable implication for structure and functioning of t e r r e s t r i a l ecosystems. The repertoire of behaviors available to a given plant i s greatly enhanced i f i t forms different mycorrhizal types, as i s that of plant populations and communities forming a variety of mycorrhizae. The fungi translate information contained i n allelochemicals into pattern within the ecosystem, and i n t h i s sense are reminiscent of James Clerk Maxwell's imaginary Demon, which could sort fast molecules from slow and thus impose structure on a gas. This allelochemically driven information processing a b i l i t y suggests that mycorrhizae, l i k e Maxwell's Demon, may play a far more important role i n the ecosystem than indicated by t h e i r biomass or energy use. Among the many questions remaining i s the degree to which mycorrhizal fungi themselves influence the allelochemical background of a system. It i s well known that mycorrhizae a l t e r the chemistry of plant roots. Preliminary work i n our laboratory shows that they influence leaf chemistry as w e l l , producing a s h i f t away from common monoterpenes toward unidentified compounds that may be d i - or sesquiterpenes ( 5 ) . The effect that such s h i f t s may have on herbivory, decomposition and allelochemical interactions i s not known. Mycorrhizae have been shown to retard l i t t e r decomposition (43), an effect that could a l t e r the production of allelochemicals, p a r t i c u l a r l y those that r e s u l t from microbial activity. It seems almost certain that mycorrhizal fungi are active participants i n , rather than passive prisoners of, the allelochemical dynamics of ecosystems. Applications i n Forestry and Agriculture Because of t h e i r role as interfaces between plant roots and the s o i l environment, mycorrhizae have the p o t e n t i a l to contribute s i g n i f i c a n t l y to the success or f a i l u r e of agroecosystems. Selection of the proper fungal symbiont may reduce a l l e l o p a t h i c effects of weeds or of one crop plant on another i n mixed-species systems. C u l t i v a t i o n of mycorrhizal d i v e r s i t y and selection of s p e c i f i c host-fungal combinations could enhance exploitation of s o i l resources. Genetic selection for allelochemical-tolerant s t r a i n s of mycorrhizal fungi i s probably f e a s i b l e . Before mycorrhizae can become a s i g n i f i c a n t management t o o l , however, much research i s needed on the basic biology and ecology of t h e i r i n t e r a c t i o n with allelochemics, and how t h i s influences community development. Acknowledgments This research was supported by National Science foundation grant, no. BSR-8400403.


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