Agronomy Journal 93:79-84 (2001)
© 2001 American Society of Agronomy
ALLELOPATHY SYMPOSIUM
Soil
Environmental Effects on Allelochemical Activity
Inderjit
Dep. of Botany, Panjab Univ., Chandigarh 160014, India
Corresponding author (allelopathy{at}satyam.net.in)
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ABSTRACT
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To exert phytotoxic effects on other plant species, chemicals may have to move to the roots of the target plant through the soil. However, during movement, abiotic (physical and chemical) and biotic (microbial) soil barriers can limit the phytotoxicity of chemicals in terms of quality and quantity required to cause injury. Organic matter, reactive mineral surfaces, ion exchange capacity, inorganic ions, and abiotic and biotic factors of soil environment significantly influence allelochemical activity. In this article, the significance of soil in laboratory and field studies on allelochemical interference is discussed.
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INTRODUCTION
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SOIL is a living biological system that provides habitat for microorganisms, e.g., bacteria, fungi, actinomyctes, algae, and protozoa (Wild, 1996). In many cases, allelochemicals move through soil and they may be transformed during movement, metabolized by soil microbes, or bound to soil organic matter. Microbes may toxify or detoxify allelochemicals after entry into soil. Many studies on allelopathy, however, do not involve soil or involve an artificial soil substrate (Inderjit and Dakshini, 1995). Not enough attention is paid to soil ecology in laboratory and field studies on allelopathy. While arguing the role of allelochemicals in plant–plant interactions, the dynamic nature of soil should not be overlooked. Because allelochemicals are present in every plant, their presence per se does not necessarily demonstrate the occurrence of allelopathic interference in nature (Heisey, 1990). Abiotic and biotic soil factors tranform allelochemicals, for example, phenolics to nontoxic phenolic polymers (Huang et al., 1999; Inderjit et al., 1999a). Controlled studies involving soil or artificial soil might help to understand a particular mechanism, but certainly will be of limited help to argue the occurrence of allelopathy in nature.
Root exudates play an important role in community structure by influencing (i) growth and establishment of plant species (allelopathy), (ii) availablity of soil inorganic ions, and (iii) soil microbial ecology (Inderjit and Weston, 2000). Several techniques have been proposed and tested to study the effects of root exudates (Inderjit et al., 1999b). Tang and Young (1982) proposed a method to collect allelopathic compounds from the undisturbed root system of bigalta limpograss [Hemarthria altissima (Poir.) Stapf & C.E. Hubb.]. Stolon cuttings of bigalta limpograss were washed and treated with 5% (v/v) Clorox (sodium hypochlorite) before planting in the pots. The pots were filled with crushed basaltic rocks and sand/rock mixtures (2:1, v/v). The soils from the rhizosphere of bigalta limograss were not selected as a medium in the study, and this might have significantly influenced the collection of allelochemicals. Studies conducted without involving soil may not reproduce soil conditions that influence expression of allelochemicals in nature.
The soil zones penetrated by fine roots and held together by mucilage (a polysacchride composed of hexose and pentose sugars and uronic acids) is called the rootsheath (Fig. 1a)
. Numerous tiny fine roots, present on the main root, coat surrounding soil with mucilage and modify the soil in contact (McCully, 1999). Cryo-SEM sections (Fig. 1b) show the root and the thickness of the rhizosheath (McCully, 1999). Figure 1c shows a 50-µm wide root surrounded by mucilage, and soil held tightly together by the contraction of mucilage (McCully, 1999). In many situations, root exudates must pass through the rhizosheath and then travel through soil to reach roots of the target plant. Therefore, in the process of allelochemical transport, physical, chemical, and biological soil barriers limits the phytotoxicity of allelochemicals in many situations (Schmidt and Ley, 1999). Due to root exudation of amino acids and carbohydrates and decortication of the root, the rhizosphere (root–soil interface) has higher microbial activity compared with bulk soil (Cunningham et al., 1996). Not only the allelochemicals, but many synthetic herbicides and pesticides, are degraded in this soil zone with higher microbial activity (Anderson and Coats, 1995). However, rhizosphere effects depend on the diffusion of root exudates away from the roots, their diffusion properties, and moisture levels of the soil (Bowen and Rovira, 1999). In this article, the significance of soils in the expression of phytotoxicity is discussed.
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Soil in laboratory experiments
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In plant debris–soil studies, concentration-dependent effects are often stressed (Blum, 1999). However, it is important in such studies that the selected concentration of chemicals in soil should be similar to concentrations that actually exist in soil–plant systems. For example, it was reported that the concentration of phenolics increased with the amount of Pluchea lanceolata–leaf leachate added into soil (Fig. 2a) (Inderjit and Dakshini, 1994), and phenolic levels in the soil amended with large amounts of P. lanceolata leaf leachate are much greater than levels of phenolics generally observed in the P. lanceolata–infested fields (Fig. 2b) (Inderjit et al., 1996).
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Fig. 2 (a) Total phenolic content of 200 g of soil amended with 100 ml of 1:12, 1:8, and 1:4 (v/v, leaf leachate/water) leaf leachate of Pluchea lanceolata; and (b) natural soil infested with P. lanceolata from four sites (S1, S2, S3, and S4). Values for mean are significantly different from control at the levels of p < 0.05. Reproduced with permission from the editor of American Journal of Botany and National Research Council Canada. Source (Inderjit and Dakshini, 1994; Inderjit and Dakshini, 1996)
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The influence of soil texture on phytotoxic effects has been noted (Del Moral and Muller, 1970; Oleszek and Jurzysta, 1987). Because soil texture may vary considerable in different regions, soils from the same geographical area where the donor plant occurs should be utilized in controlled experiments investigating allelopathy. Inderjit and Dakshini (1994) amended soils belonging to four different textural classes (clay, sandy-loam, sand, and silty-loam) with different amounts of P. lanceolata–leaf leachate. Amounts of water-soluble phenolics in amended soil varied depending on the soil texture (Fig. 3)
. The clay-size layer silicates also play a very important role in oxidative polmerizaton of organic compounds (Huang et al., 1999). While discussing the abiotic catalytic ability of primary minerals in transformation of phenolic compounds, Huang et al. (1999) listed the sequence of catalytic ability of primary minerals as follows: tephroite > actinolite > hornblende > fayalite > augite > biotite > muscovite 
albite orthoclase microcline quartz. Clay minerology may therefore also play a vital role in the expression of allelochemical activity. In plant debris/litter–soil bioassays, growth response of target plants and phytochemical analyses of allelochemicals are typically evaluated. Less attention is paid to altered status of inorganic ions in soil amended with plant debris/litter or leachate from donor plants. It has been shown that inorganic ion status of soil amended with plant litter/debris or its leachate is altered due to nutrients in the added organic material or leachate and/or to the nutrient immobilization by microbes due to labile C in the leachates (Inderjit and Dakshini, 1994; Michelsen et al., 1995; Schmidt et al., 1997; Inderjit and Mallik, 1997; Inderjit and Foy, 1999). Analyzing amended soil for inorganic ions in addition to organic compounds may give useful information about the interaction of organic and inorganic soil components in explaining the observed growth responses (Inderjit and Dakshini, 1999).
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Fig. 3 Total phenolic content of 200 g of soil, from different textural class (clay loam, sand, silt loam, and sandy loam), amended with 100 mL of 1:12 (TS1), 1:8 (TS2), and 1:4 (TS3) (v/v, leaf leachate/water) leaf leachate of Pluchea lanceolata. Reproduced with permission from the editor of American Journal of Botany (Inderjit and Dakshini, 1994)
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Field soil
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Soils have different amounts of organic matter depending on the abiotic and biotic components of the ecosystem. Organic and inorganic acids are the byproducts of decomposition of organic matter. One such decomposition product is carbonic acid, which removes base-forming cations such as Ca2+ and Mg2+ (Brady, 1990). Soil organic matter may coat mineral surfaces (e.g., Mn2+ and Fe2+), which prevents phenolic acids from directly contacting with mineral ions and thus oxidation of phenolic acids. Cheng (1989) suggested that oxidation of organic chemicals is not directly related to content of Mn2+ and Fe2+ in the soil but depends on the extent these inorganic ions are exposed to organic chemicals. Phenolic compounds are reported to be polymerized into humic acids by Mn, Fe, Al, and Si oxides; however, Mn oxide is the most powerful catalyst (Huang et al., 1999). Reviews by Blum et al. (1999), Dalton (1999), Huang et al. (1999), Inderjit et al. (1999a), Novak et al. (1995), and Schmidt and Ley (1999) discuss the influence of abiotic and biotic soil factors on phytotoxic levels of allelochemicals. Although some studies on allelopathy have examined the effects of pH, there is a need to evaluate the effects of other soil properties such as electrical conductivity, inorganic ions, organic matter content, clay minerals, and water status.
The quantification of phytotoxins in actual soil infested with the suspected allelopathic plant is a very difficult task. In controlled studies, Inderjit and Mallik (1996) found a significant increase in phenolic levels in soils amended with different amounts of dwarf-laurel (Kalmia angustifolia L.) leaf litter leachates (Fig. 4a)
. However, these authors (1999) could not find any difference in the phenolic contents of soil infested with dwarf-laurel in cut and uncut black spruce [Picea mariana (Mill.) Britton et al.] forests and dwaf-laurel–free soils from uncut black spruce forests (Fig. 4b). It might be incorrect to completely rule out the ecological role of phenolics in dwaf-laurel–black spruce ecosystem, but more research is needed to understand the fate of phenolic compounds in complex boreal forest ecosystems.
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Fig. 4 (a) Total phenolic content of 200 g soil amended with four levels of leaf litter leachates of Kalmia angustifolia. A 5, 10, 15, and 25 g of K. angustifolia leaf litter was soaked in 400 mL of water to get different levels of leachate. Reproduced with permission from National Research Council Canada (Inderjit and Mallik, 1996); (b) total phenolic content of soil infested with K. angustifolia from uncut and cut black spruce forest and K. angustifolia–free soil from uncut black spruce forest. Similar letters indicate significant (p < 0.05) differences between values. Reproduced with permission from the editor of Acta Oecologia (Inderjit and Mallik, 1999)
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In most studies, influence of allelochemicals on growth and establishment of a plant species is studied. Some weed species, e.g., P. lanceolata and dwaf-laurel have the potential to make substratum unsuitable for the growth of associated species by altering soil chemical characteristics. The influence of organic compounds on soil ecology should be given attention in plant chemical interference studies. Northern crowberry (Empetrum hermaphroditum) is a dwarf ericaceous shrub dominating boreal forests of northern Sweden (Nilsson, 1994; Nilsson et al., 1998). Northern crowberry produces batatasin-III, a relatively recalcitrant phenolic, which is incorporated into humus (Gallet et al., 1999). Accumulation of batatasin and other phenolics modify soil C/N ratio and influences nutrient availability; thus playing a key role in long-term ecosystem functions (Wardle et al., 1997). Such studies illustrate the significance of soils in the expression of allelochemical activities.
More field studies on allelochemical influence to substratum components are needed to investigate the occurrence of allelochemical interference. For example, in many allelopathy studies on cropland weeds, little attention is paid to topsoil and subsoil. After plowing, the upper layer of soil (12–18 cm) is modified. Subsoil, however, is relatively less disturbed by soil tillage. The quantity and quality of allelochemicals may vary in the two soil layers. Inderjit and Dakshini (1996) reported higher levels of total phenolics in P. lanceolata–infested topsoil from a field cultivated twice a year compared with that cultivated once a year. However, such differences were not recorded in subsoils. Because the topsoil is the primary rooting zone, the effects on the topsoil will probably have the most impact on plant growth.
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Phytotoxic levels in soil
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After entering soil, allelochemicals encounter millions of soil microbes. The accumulation of chemicals at phytotoxic levels and their fate and persistence in soil are important determining factors for allelochemical interference. After entry into soil, all chemicals undergo processes such as retention, transport, and transformation, which influences their phytotoxic levels (Cheng, 1995). Dalton (1989) proposed that phenolic acids may be protected from microbial degradation by their reversible sorption onto soil particles. However, it was recently reported that reversible sorption of phenolic acids (e.g., ferulic and p-coumaric acids) on soil particles did not provide enough protection necessary to build up phytotoxic concentration in soil (Blum, 1998).
Allelopathy in black walnut (Juglans nigra L.) has been debated for several years (Massy, 1925; Davis, 1928). Scientists are still debating whether juglone allelo-chemicals accumulate to phytotoxic levels in soil. The bacterium Pseudomonas putida was isolated from soils beneath walnut, and this bacterium could convert juglone to 2-hydroxymuconic acid (Rettenmaier et al., 1983; Schmidt, 1988). Schmidt (1988) isolated the bacterium from soils beneath walnut, and reported that the bacterium could easily use juglone (5 hydroxy-1, 4-napthoquinone) as a C source. Schmidt (1990) stated that juglone is susceptible to biotic and abiotic degradation in soil and the likelihood that juglone persists at phytotoxic concentrations is remote. Williamson and Weidenhamer (1990), however, disagreed with the conclusion drawn by Schmidt (1988). They argued that the allelopathic potential of juglone is due to its static (i.e., existing concentration in the soil suspension) and dynamic (i.e., renewal rate) availability. Therefore, even if juglone gets degraded over a period of time, its accumulation in soil at a phytotoxic level is maintained due to its periodic replenishment.
Jose and Gillespie (1998) reported the spatio-temporal variation in soil juglone in a black walnut–corn (Zea mays L.) alley cropping system. It was found that within the tree row, juglone concentration was highest during fall. At a distance of 0.9 m from the tree row, juglone concentration was highest during spring and summer (Fig. 5)
. When data from all three seasons were pooled, these authors found a significant decrease in its concentration with increasing distance from tree row (Fig. 6)
. Juglone concentration was reduced to 20% at a distance of 4.25 m compared with within-tree row concentration. The mineral content and microbes in the soil limit the expression of allelochemicals (Schmidt and Ley, 1999). These authors suggested that chances of allelopathic interactions are higher when chemicals are released in close proximity to the target plant. There are, however, phytotoxins known to persist in soil for longer duration. Sorgoleone, an important component of root exudate from sorghum [Sorghum bicolor (L.) Moench] and other Sorghum spp., persists up to 8 wk at detectable limits after its addition into soil (Weston et al., 1999).
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Fig. 5 Spatio-temporal variation in soil juglone in a black walnut–corn alley cropping system. Juglone was quantified at 0, 0.9, 2.45, and 4.25 m (0 m represents the tree row and 4.25 m represents the middle of alley). Reproduced with permission from Kluwer Academic Press (Jose and Gillespie, 1998)
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Fig. 6 Soil juglone concentration as a function of the distance from tree row (only `no barrier' treatment is used for this analysis). Error bars represent 1 SE of the mean. Reproduced with permission from Kluwer Academic Press (Jose and Gillespie, 1998)
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In case of perennial weed species such as P. lanceolata (Inderjit, 1998), cogongrass, [Imperata cylindrica (L.) P. Beauv.] (Inderjit and Dakshini, 1991), mugwort (Artemisia vulgaris L.) (Inderjit and Foy, 1999), or purple nutsedge (Cyperus rotundus L.) (Tang et al., 1995), accumulation of allelochemicals at phytotoxic levels is possible. Even if compounds leached by these weed species are degraded in the soil, their continuous replenishment in soil is maintained due to the evergreen nature of the weed species. The mixture of allelochemicals contributed by these weeds and their degradation by-products can bring phytotoxic effects, even if an individual compounds are present at low levels in a mixture with other compounds. The amount of individual phenolic acid needed for biological activity may be lower in mixtures, and its concentration required to bring phytotoxicity decreases as the number of phenolic acids added to soil increases (Blum, 1996, 1998).
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Conclusion
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In many situations, allelochemicals after entering into soil undergo chemical, physical, and biological degradation. These influences often limit the accumulation of allelochemicals at phytotoxic levels. Phytotoxicity of allelochemicals depends on their movement, fate, and persistence in the soil. There is a need to stress the importance of studies of ecology and chemistry of soils in the laboratory and the field for investigation of allelochemical interference. More research is needed to understand the effects of organic matter, reactive mineral surfaces, ion exchange capacity, inorganic ions, and specific microbes on the availability of allelochemicals. Many researchers express their concern regarding unpredictability of laboratory bioassays for allelochemical interference in terms of explaining field pattern (Inderjit and Dakshini, 1995; Blum et al., 1999). This unpredictability will continue unless we realize the significance of soil, and pay more attention to soil in laboratory bioassays for phytotoxicity and phytochemical analysis. In the future, we need to take a more holistic approach integrating allelochemicals to various components of the substratum.
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ACKNOWLEDGMENTS
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I am grateful to professors David C. Coleman, Randy Dahlgren, and Anders Michelsen for reviewing the manuscript prior to publication. The comments made by two anonymous referees are gratefully acknowledged.
Received for publication November 30, 1999.
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TOP
ABSTRACT
INTRODUCTION
