Written by Tessa R. Grasswitz, Cornell University
Advances in molecular research techniques are providing new insights into the complex interactions that can occur between soil organisms, plants, and the above- or below-ground organisms that feed on plants—including insect pests and pathogens. This review briefly examines some of these interactions and their possible impact on plant health.
Soil ‘feed-back loops’
The living components of the soil include large numbers of fungi, bacteria, protozoa, nematodes, larger invertebrates (such as earthworms and soil-dwelling insects), and plant roots. The composition and activity of the soil community (particularly the microbial fraction) is heavily influenced by chemicals released from plant roots, either in the form of dead cells and other debris, or as root ‘exudates’. The latter may include a wide variety of carbon-rich compounds including various sugars, amino acids, fatty acids, phenolics, and many others.
The composition of root exudates varies not only with plant species, but also at different times, and under different conditions; plant age, nutritional status, and environmental stressors (such as drought or attack by insect pests or pathogens) can all affect root exudate composition. It has been estimated that, depending on circumstances, as much as 10 to 50% of plant photosynthetic production may be released from roots into the soil at various times.
Root exudates alter soil chemistry, facilitate the formation of soil aggregates, and serve as nutrients for soil microorganisms in the zone immediately adjacent to the roots (the ‘rhizosphere’). As a result, the microbial community in the rhizosphere differs in composition from that in the surrounding soil, although both may contain plant pathogens together with beneficial species that can protect plants from pathogens, and additional species that affect plant growth and health in other ways.
The activities of the microbial community in the rhizosphere can, in turn, influence the compounds released from roots, setting up complex feed-back loops between plants and their associated soil communities. These interactions can affect the plant’s susceptibility or resistance to pests and diseases in various ways: not least by affecting the plant’s nutritional status.
Direct and indirect effects of root exudates on plant nutrition
Root exudates can influence plant nutrition both directly and indirectly. In phosphorous-deficient soils, for example, some plants release enzymes from the roots that liberate phosphorous from soil organic compounds, increasing phosphorous availability and uptake by the plant. Similarly, organic acids in root exudates can help release phosphorous from insoluble phosphates of calcium, iron or aluminium.
More indirectly, the root exudates of some plants can affect growth by inhibiting the germination and development of potential competitors: cereal rye, for example, releases several compounds via its roots that inhibit the germination and growth of various weed seeds. There are many other examples of such allelopathic interactions between different plants.
More subtly, plant nutrition can be influenced by the formation of symbiotic relationships with soil microorganisms that are attracted or stimulated by root exudates. The nitrogen-fixing rhizobia bacteria associated with legume roots, for example, are attracted by root exudates that contain specific organic acids, amino acids, and small organic compounds known as flavonoids. Different legume species release different flavonoids, allowing specific strains of rhizobia to selectively colonize their own specific host plants.
In a similar way, other plant-growth promoting soil bacteria and arbuscular mycorrhizae (fungi that can promote nutrient uptake by plant roots) are also attracted to the roots of their plant partners by specific components of their root exudates. The effect of these symbiotic associations can be significant: it has been estimated that, in natural systems, mycorrhizal fungi can be responsible for up to 75% of the phosphorus acquired by plants on an annual basis. Conversely, in soils with high levels of available phosphorous, root colonization by mycorrhizae is reduced.
Effects of soil microorganisms on plant pests and pathogens
Apart from their beneficial effects on plants through improved nutrition (which can enhance plant resistance to pests and diseases), beneficial soil microorganisms may affect harmful members of the soil community more directly through competition, parasitism, or other mechanisms. Species of the fungus Trichoderma, for example, produce a wide range of antibiotic substances and are capable of both out-competing certain soil pathogens and parasitizing others.
Various benign soil bacteria and non-pathogenic fungi (including species of Trichoderma and some mycorrhizae), can also “prime” the production of plants’ own natural defensive chemistry, allowing a more rapid and vigorous response to subsequent attacks by pathogenic bacteria, fungi and/or viruses. Depending on the species involved, this ‘induced systemic resistance’ (ISR) can result in increased levels of plant defence not only against soil-borne pathogens, but also to some foliar pathogens and leaf-feeding insects.
The complex nature of soil interactions: root exudates and defence against invertebrate pests
Plant defence against pest attack can be stimulated in very intricate and subtle ways. For example, in plants as different as corn and citrus trees, wounding by the larvae of root-feeding beetles causes the plants to release characteristic compounds in their root exudates; these compounds in turn attract parasitic soil-dwelling nematodes that attack (and eventually kill) the root-feeding insect larvae.
Other recent research has shown that when attacked by spider mites, bean plants release specific chemicals into the soil that can be detected by nearby roots of other (uninfested) plants of the same species; in response, these healthy plants release volatile compounds from their leaves that attract predatory mites: a pre-emptive recruitment of naturally occurring biological control agents promoted and directed via soil-borne chemicals.
Other aspects of soil-mediated interactions
The examples above illustrate the complex nature of possible interactions between plants, soil communities, and other plant-associated species. These subtle interactions can even extend to pollinators. Symbiotic associations with mycorrhizae, for example, can influence the number and size of flowers produced by their plant partners, and can modify pollinator behavior by triggering changes in nectar and pollen production.
It is important to keep in mind that the same root exudates that can attract and stimulate beneficial soil organisms can have similar effects on less desirable members of the soil community, including plant pathogens, root-feeding insects and even some parasitic weeds. The outcome (for plants) of the resultant below-ground interactions will depend on the balance of species involved, their relative population sizes, and the magnitude of their individual effects on each other and on the plants. These factors in turn will be influenced by the physical and chemical characteristics of the soil, and by various management practices.
A healthy soil is a very dynamic ecosystem: soil communities can change rapidly in response to biological and environmental disturbances. For example, heavy rainfall after a period of drought can result in sequential changes in the composition of soil microbial communities within minutes or days. At longer time-scales, soil community structure can differ markedly at different seasons, and over more extended periods.
As a result of our increased understanding of soil/plant interactions, a growing number of commercial products based on soil organisms are becoming available, and various strategies are being proposed for manipulating soil biology in agricultural systems. While an increased appreciation of the biological components of soil is both welcome and long overdue, we need to fully consider the complexity of the interactions involved. Consider this: there is evidence to suggest that, in some cases, selective plant breeding under optimum conditions (e.g. with routine use of fertilizers and crop protectants) may have selected for crop cultivars with a reduced ability to form symbiotic relationships with mycorrhizal fungi and beneficial soil bacteria. As a result, these cultivars have, in effect, become much more dependent on external inputs than are their ‘wild’ relatives. The ‘law of unintended consequences’ applies to soil biology as much as to any other system.
- On-line NRCS presentation: Improving soil health in orchards, vineyards, and groves. A 1-hour overview of how to improve soil health even in extreme conditions. Covers soil biology, approaches and benefits (including effects on water, salinity, fertilizer use and crop quality). Available on demand at: http://www.conservationwebinars.net/webinars/improving-soil-health-in-orchards-vineyards-and-groves/?searchterm=None
- NRCS soil biology portal: https://www.nrcs.usda.gov/wps/portal/nrcs/main/soils/health/biology/
- Cornell soil health program: https://soilhealth.cals.cornell.edu/