5.0 The Chemical Factor: Plant-Produced Toxins and Allelopathy

5.1 A Historical Perspective on Allelopathy

Allelopathy is defined as the chemical inhibition of one plant by another. This phenomenon plays a significant strategic role in plant competition and the structuring of plant communities.

The concept has a long history, with the first suggestions being credited to De Candolle in 1832. From his field observations, he noted that spurge (Euphorbia) seemed to inhibit flax, thistles inhibited oats, and rye inhibited wheat. Despite these early insights, the field of research lay dormant for nearly a century until interest was renewed by observations such as Cook’s (1921) description of wilting in potato and tomato plants grown near black walnut trees (Juglans nigra).

The first chemical identification of an allelopathic agent came from this work. Davis (1928) extracted a compound from black walnut, identified it as juglone (5-hydroxynaphthaquinone), and demonstrated its toxicity to tomato and alfalfa plants.

More modern research spurred renewed interest, including work on the “replant problem” in old peach orchards (Proebsting and Gilmore, 1940) and an investigation into growth inhibition in guayule (Parthenium argentatum), which led to the identification of trans-cinnamic acid as the inhibitor (Bonner and Galston, 1944). These historical and agricultural examples paved the way for the documentation of allelopathy as a powerful force in natural ecosystems.

5.2 Allelopathy in Natural Ecosystems: Case Studies

In natural plant communities, allelopathy can be a dominant force, determining the spacing of individuals, influencing species composition, and directing the course of ecological succession.

A classic case study comes from the California chaparral, where Muller, Muller, and Haines (1964) observed distinct vegetation-free zones around shrubs like Salvia leucophylla and Artemisia californica. They determined that these shrubs produce volatile inhibitors that prevent other plants from growing nearby. The specific volatile compounds were later identified as terpenes, including camphor and cineole (Muller and Muller, 1964). These researchers also related the production of these inhibitors by chaparral shrubs to the disappearance of herbaceous species during the fire cycle (Muller, Hanawalt, and McPherson, 1968).

Research from my own group in the old-fields of central Oklahoma suggests a different allelopathic dynamic. We have gathered evidence that the rapid disappearance of the pioneer weed stage of succession is due to self-inhibition and inhibition by other pioneer species (Abdul-Wahab and Rice, 1967; Parenti and Rice, 1969; Wilson and Rice, 1968). The dominant species of the second successional stage, triple-awn grass (Aristida oligantha), is able to invade because it is not inhibited by the pioneers and can grow well in the infertile soil.

These chemical interactions are not limited to plant-plant relationships but involve a complex community of soil microorganisms as well.

5.3 The Role of Microorganisms: Antibiotics and Toxin Mediation

The soil environment is a site of complex chemical communication involving not just higher plants, but also bacteria, fungi, and actinomycetes. Antibiotics are substances produced by microorganisms that inhibit other microorganisms. These interactions are highly relevant to plant ecology on several levels.

• Microbe vs. Microbe: Some soil bacteria can inhibit the root-nodule bacteria essential for nitrogen fixation (Konishi, 1931), while others are antagonistic to the free-living nitrogen-fixer Azotobacter (Iuzhina, 1958). On the other hand, some soil microbes can inhibit microorganisms that cause plant diseases (Cooper and Chilton, 1950).
• Microbe vs. Higher Plant: Pathogenic microorganisms often produce toxins to cause disease symptoms in host plants. Additionally, some soil microbes can convert non-inhibitory compounds released by plants into inhibitory ones (Börner, 1960).
• Higher Plant vs. Microbe: The resistance of many plants to disease may be due to their production of compounds that inhibit pathogens (Farkas and Kiraly, 1962; Hughes and Swain, 1960; Schaal and Johnson, 1955).

Antibacterial compounds are also found in seeds and fruits. One survey found such compounds in 52 different species (Ferenczy, 1956). This can aid in seedling survival; for instance, leaching inhibitors from sunflower fruits increased their rate of rotting during germination tests (Lane, 1965).

My own research has focused on the inhibition of nitrogen-fixing bacteria by plants common in early succession. Many of these low-nitrogen-requiring plants produce compounds that inhibit both symbiotic and free-living nitrogen-fixing bacteria (Rice, 1964, 1965b, 1965c). This provides a competitive advantage to the early invaders and slows the rate of succession, as the plant species that dominate later stages have higher nitrogen requirements (Rice, Penfound, and Rohrbaugh, 1960). By inhibiting the very bacteria that would enrich the soil with nitrogen, these pioneer species actively maintain the low-nutrient conditions to which they are adapted, thereby delaying their own replacement by later successional species with higher nutrient demands.

5.4 Mechanisms of Allelopathic Action

A complete understanding of allelopathy requires not only identifying the specific chemical inhibitors but also elucidating their physiological mechanisms of action on target plants.

Volatile terpenes produced by Salvia leucophylla have been shown to reduce both cell elongation and cell division in the radicles and hypocotyls of cucumber seedlings (Muller, 1965). Subsequent work demonstrated that the terpenes cineole and dipentene markedly reduce oxygen uptake in mitochondria. The inhibition appears to be localized in the Krebs cycle between succinate and malate, and it also decreases the permeability of cell membranes (Muller et al., 1969).

Most of the inhibitors my research group has identified from old-field species are phenolic compounds. These include: chlorogenic acid, p-coumaric acid, ferulic acid, gallic acid, p-hydroxybenzaldehyde, isochlorogenic acid complex, scopoletin, scopolin, sulfosalicylic acid, and several tannins. The mechanisms of these compounds are varied and complex:

• Chlorogenic Acid: This compound is a strong inhibitor of several crucial enzyme systems. It has been shown to inhibit potato phosphorylase (Schwimmer, 1958), a peroxidase-catalyzed reaction (Mazelis, 1962), and indoleacetic acid (IAA) oxidase, the enzyme that breaks down the primary plant growth hormone auxin (Sondheimer and Griffin, 1960).
• p-Coumaric and Ferulic Acids: These compounds inhibit growth by disrupting auxin metabolism. Specifically, they increase the rate of decarboxylation of indoleacetic acid (IAA), thereby lowering the concentration of this critical growth hormone in the plant (Zenk and Müller, 1963; Henderson and Nitsch, 1962).
• Tannins (and Gallic Acid): These compounds are powerful inhibitors due to their strong affinity for the peptide linkages of proteins. They have been shown to cause considerable reduction of Krebs cycle succin oxidase and malic enzyme activity (Hulme and Jones, 1963). They also inhibit IAA-induced growth (Zimsmeister and Hollmuller, 1964), pectolytic enzymes (Hall, 1966), and even nodulation of heavily inoculated legumes and hemoglobin formation in the nodules (Blum and Rice, 1969). They can also form complexes with phenol oxidases, potentially rendering them inactive (Bendall and Gregory, 1963).
• Scopoletin: This inhibitor has a profound impact on photosynthesis. Treating tobacco and sunflower plants with scopoletin leads to an increase of scopoletin and its glycoside, scopolin, in their tissues. This has been shown to depress net photosynthesis to as low as 34% of control plants and correlates strongly with reduced leaf area growth (Einhellig et al., 1970).

The identification of allelochemicals and the study of their mechanisms of action is a vast and active field of research, offering crucial insights into the complex chemical web of plant-plant and plant-microbe interactions.

——————————————————————————–