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3.4 Soil-borne plant pathogens

Soils contain diverse communities of microscopic organisms that are capable of damaging plants. A detrimental interaction between a soil organism and a plant is often highly specific. For example, a fungus that causes root-rot of wheat may have no effect on the roots of another plant growing in the same soil. Highly specialised interactions between soil organisms and plants can kill seedlings and even adult trees. Many organisms target younger plants but others appear as problems at later stages in the life of the plant. Other pathogens are able to cause disease in many different plant species.

The soil organisms that have the potential to be plant pathogens include fungi, bacteria, viruses, nematodes and protozoa. Some pathogens of the above ground parts of plants (leaves, stems) survive in the soil at various stages in their life cycles. Therefore, a soil phase of a plant pathogen may be important, even if the organism does not infect roots.

In spite of the potential for severe damage to be inflicted on plants by soil organisms, most plants do not display serious symptoms of disease. Disease usually occurs when conditions are particularly unfavourable, or when a soil organism is accidentally introduced where a highly susceptible plant species occurs. Intensive production in agriculture, horticulture or forestry increases the opportunities for diseases to develop compared with undisturbed natural ecosystems. Planting of similar plant species together in monoculture increases the probability of disease outbreak. In contrast, the damage caused by the fungus Phytophthora cinnamomi in many different plant species in diverse natural ecosystems in Australia demonstrates the damage that can be caused by a pathogen that infects the roots of many unrelated plants.

Some plant pathogens depend on their host plant for survival and are unable to complete their life cycle without infecting their host plant. Biotrophic organisms of this type are often difficult to grow in laboratory media.

Disease-causing microorganisms and soil animals are a natural component of the soil community. The organisms are normally present in relatively low numbers. An outbreak of disease commonly follows either an increase in the abundance of the pathogen or a change in the susceptibility of the host to the pathogen. Important questions are:

• Why do outbreaks of disease occur?

• What are the soil conditions that allow disease to develop or that suppress disease?

• What are the soil conditions that suppress disease?

• How do management practices influence the soil as a habitat for plant pathogens?

• How do plant pathogens survive in the absence of their specific host plant?

What is plant disease?

Plant disease is the result of a complex interaction between the host plant, the pathogen and the environmental conditions including those in the soil. Soil conditions that influence the development of disease are pH, moisture, oxygen, and nutrients. In addition, other soil organisms interact with the pathogen. The level of this interaction is also influenced by soil conditions, which affects the growth and activity of the non-pathogenic organisms. Consequently, whenever the soil environment changes, there is potential for either a positive or negative influence on soil-borne plant pathogens.

Plant disease reduces plant survival and productivity, but the symptoms of plant disease are often difficult to recognise. One reason for this is that they are not necessarily the same in plants of different ages. The amount of a potential pathogen in a soil and the environmental conditions can also alter the symptoms displayed by a plant. Furthermore, symptoms may be related to infection by more than one organism. Interactions between organisms can produce symptoms that are not the same as those that occur when each type of organism is present alone. Similar symptoms can be caused by different pathogens and furthermore, the symptoms of some pathogens resemble those of various nutrient deficiencies. Therefore, it is not always easy to identify a pathogen responsible for a disease simply from the symptoms on the plant. A great deal of experience and knowledge of the range of symptoms produced by different pathogens and knowledge of symptoms of nutrient deficiency is essential for an accurate identification of most pathogens.

Examples of major soil-borne plant diseases:

(i) Disease caused by Phytophthora cinnamomi

Phytophthora cinnamomi causes a serious disease that threatens forests and other ecosystems especially in south-eastern and south-western Australia (Shea et al. 1984). Hundreds of different plant species are killed by this introduced pathogen. Vehicles are often responsible for the widespread distribution of the pathogen by disturbing and transporting infected soil. There is no simple solution to Phytophthora disease in the forest. Quarantine methods have been introduced to limit the spread of the fungus and cleaning of vehicles is mandatory.

P. cinnamomi and related fungi also cause disease of horticultural plants such as azalea, pineapple and avocado. In horticultural systems, organic mulches have been used to stimulate the community of soil organisms and reduce the negative impact of the pathogens.

(ii) Take-all Disease of Wheat

Take-all disease is caused by the fungus Gaeumannomyces graminis var. tritici (Cook 2003). This pathogen infects the vascular tissue of wheat roots and restricts the transport of water and nutrients within the plant. Severely infected plants have stunted root systems. In addition to root rot, a severe symptom is ‘white heads’ which occurs if plants survive seedling damage and grow to maturity. Such plants form seed heads with poor grain development that are characteristically white. The fungus survives in the soil on decaying plant material and relies on this material as a carbon source to sustain it until it is able to infect new roots in the following wheat crop or alternate hosts.

The take-all fungus is a major root disease world-wide and is estimated to cause millions of dollars in lost wheat yield each year. The main method for control is by crop rotation with non-host plants and removal of weeds that may act as alternate hosts. There has been little success in breeding for resistance in wheat to the fungus Gaeumannomyces graminis var. tritici. Under some conditions, soils become naturally suppressive to the fungus. This has been observed in long-term monocultures of wheat. Reduced disease is likely to be due to changes in activity of other soil microorganisms.

(iv) Crown Gall

Crown gall occurs on many genera of plants and is characterised by the formation of root tumours caused by the bacterium Agrobacterium tumefaciens. The bacteria infect the root and induce plant cells to divide; a tumour-like swelling is formed that contains infected cells around its outer surface. Bacterial DNA is transferred to the host plant (see Viss et al. 2003).

(v) Root Knot Nematode Disease

Root knot nematodes cause disease on hundreds of plant species, especially horticultural species, in warmer climatic zones (see Trudgill and Blok 2001). Species of nematodes in the genus Meloidogone induce the formation of numerous galls throughout the root system. The damaged roots also have malfunctioning root tips which reduce root growth, resulting in considerable yield losses.

How is the source of plant disease identified?

The fundamental approach to identifying the organism or organisms responsible for a disease is to follow the protocol known as Koch’s Postulates (McIntyre and Sands 1977):

Step 1. Visual inspection of the plant to identify signs of the presence of a pathogen and symptoms on the host (observed without the aid of a microscope.

Step 2. Observation of the diseased portion of the plant using a microscope.

Step 3. Isolation and purification of the pathogen (growth of the organism on artificial media).

Step 4. Inoculation of plants of the same type with organisms isolated from the diseased plant to observe symptoms of disease, for comparison with the original observations in Step 1.

The purpose of using Koch’s Postulates is to identify the organism responsible for disease in a rigorous manner. This is the first step in working out how to overcome the problem. Not all organisms can be isolated from plants and grown in culture and for many diseases it is difficult to identify the responsible organism.

Once a potential pathogen has been identified, a variety of procedures can be used to determine the conditions under which the disease is likely to be most severe. An example of this approach was used to identify the causal organism of brown spot and root rot of lupin in Western Australia as described below.

Case Study: Pleiochaeta Root Rot of Lupin

The pathogen responsible for a serious root disease of lupin in Western Australia was not immediately identified when it was first detected. In fact, several species of fungi were commonly reported from diseased lupin roots, including species of Fusarium, Pythium, Rhizoctonia and Pleiochaeta further hindering the control of the disease.

The protocol used by Sweetingham (1989 & 1991) to identify the causal pathogen was to

Observe and describe the disease symptoms and occurrence in the field.

Identify the fungi isolated from diseased roots. More than 10 species of fungi were isolated, but none were clearly identified as the possible pathogen.

Perform pathogenicity tests to identify the degree of disease caused by each fungus when it was present by itself on lupin roots. Some fungi were more pathogenic than others, but none of the fungi, when present alone, was distinctly more pathogenic than any other.

Test the effect of selected fungicides on the presence of different fungi and on the extent of disease using field soil. This technique was most successful in identifying the likely cause of the root rot.

The use of fungicides that targeted the major fungi present in soil where disease was observed demonstrated that Pleiochaeta was the most likely pathogen (Sweetingham 1989). The fungicides Ridomil, Benlate, Rovral and a mixture of all three were used. Ridomil eliminated Pythium without causing a major decline in the disease rating of roots. Benlate had little effect on Pythium, but reduced Pleiochaeta and Fusarium in the roots leading to a reduced disease rating. Rovral eliminated Pleiochaeta but left Furarium and Pythium and these roots had a much reduced disease rating. This set of fungicide treatments was successful in discriminating among the fungi that were present in the diseased roots.

This case study illustrates the complexity involved in identifying the causal agent of root disease, especially when more than one fungus may be involved. It cannot be presumed that the presence of an organism implicates it as a causal agent of disease. Non-pathogenic fungi often enter damaged roots and therefore a number of organisms may be present in diseased roots without being responsible for the disease.

How are disease-causing organisms dispersed?

Disease occurs under the following conditions:

(i) if there are enough infective hyphae, spores or other fungal structures such as sclerotia of a pathogen present in the soil,

(ii) if there is a suitable environment for growth of the organisms, and

(iii) if the plant is susceptible to infection.

If the organism is present in low numbers, it may have little impact on the plant. If soil conditions are suitable for the multiplication of the pathogen, there will be a greater chance of disease if other factors are also appropriate for disease development. In general, the more organisms present, the more severe the disease (Sweetingham 1991), but plant and soil conditions are also important.

The hyphae of some fungal pathogens can grow long distances through the soil. For example, hyphae of the fungus Armillaria extend many metres horizontally in soil and simultaneously infect the roots of several plants. Some fungi, for example species of Phytophthora, form narrow and short hyphae that do not spread the fungus through the soil. Often these fungi are disseminated in water or in soil during erosion and by other mechanisms including transport of soil on vehicles or footwear.

Spores of fungi that are pathogens of leaves and stems may have a soil phase during which spores remain dormant. Once the dormancy period ceases, spores survive in the soil until conditions are appropriate for their germination and infection of a new plant. Growth of some pathogens is stimulated by the presence of roots which release exudates or emit other signals.

Spores of some soil-borne fungi are dispersed by wind. Dispersal of bacterial plant pathogens is common when soil is transported from one place to another. Some disease-causing organisms are dispersed on plant debris. Pleiochaeta setosa spores are dispersed in soil via dead organic material from the previous crop (Sweetingham 1996).

How do pathogens enter roots?

Pathogenic invasion of plant roots involves several steps. The first of these is recognition between the pathogen and the plant, which involves complex molecular mechanisms. Recognition occurs in the diffuse interface between the root and the soil created by root exudates and sloughed off root cells. This interface between soil and root may be a very suitable habitat for growth of the pathogen before it enters the root.

This initial interaction can also be the stimulus for the fungus to penetrate the plant cell wall. Some organisms produce enzymes that dissolve cell wall layers, allowing the hyphae to enter. Pathogens can also enter roots at points damaged by soil animals or other disturbances. A plant may react to the presence of a pathogen by producing chemical or physical barriers that prevent entry or confine potential pathogens to a small part of the root.

Once inside the root, pathogens occupy specific cell types. Some fungi enter the cells that conduct nutrients, carbon and water throughout the plant. If these cells are damaged, important processes that control the life of the plant are disrupted. Other fungi predominantly colonise the cortical root cells that are important in nutrient uptake from the soil.

How do roots react to pathogens?

Plants differ in their susceptibility to plant pathogens. Even cultivars of one plant species can be more or less resistant to a pathogen. Similarly, species or strains of pathogens differ in their capacity to infect a plant. Differences in the degree of disease can therefore be related to: (i) the susceptibility of the plant: (ii) the virulence of the pathogen; (iii) the stage of development of the plant; (iv) the abundance of the pathogen; and (v) the environmental conditions.

How does plant nutrition affect disease?

The nutritional status of a plant influences many of its physiological processes and this can alter the response that plants have to the presence of pathogens. Changes in the concentration of nutrients such as phosphorus in a plant can alter root and shoot growth as well as the movement of carbohydrate and other molecules within the plant. These changes have the potential to influence the development of a disease.

Fertilisers can also alter plant susceptibility to disease (Wilhelm et al. 1985). In this study, in the absence of manganese fertiliser, barley grew less well if nematodes were present in the soil than when manganese was added at sufficient levels to meet the requirements for growth of the plant This occurred even when the numbers of nematodes in both treatments were similar.

What is ‘biological control’ of plant disease?

The control of pathogens and prevention of plant disease is a natural soil biological process. Indeed, in most situations, plant disease is not strongly evident even when potentially pathogenic fungi are present in a soil. This suppressive characteristic of soil is common in natural ecosystems, but becomes less apparent with high levels of disturbance and the introduction of plant monocultures. Disturbance creates soil conditions and a high density of susceptible roots that encourages the multiplication of pathogens. Once potentially damaging organisms become present in high numbers in a soil, they may be difficult to eradicate. Management practices are required that create conditions in the soil that are not favourable to pathogens so that their growth is limitedand therefore, disease it restricted.

There are many demonstrations of the potential for soil organisms to reduce disease (Stotzky and Bollag 1996). As demonstrated in this study, when apple trees were replanted in a soil previously prone to apple replant disease, increased tree growth occurred when various strains of bacteria were added to the soil, indicating a beneficial effect (Utkhede and Li 1989). Similar effects were observed at two sites, but because different quantities of the bacteria were added in the inoculum it is difficult to compare the effectiveness of each organism.

In some environments, take-all disease of wheat has declined naturally. These areas of natural suppression of disease have been investigated extensively to determine how the pathogen is suppressed. Specific bacteria that are capable of limiting the growth of the fungus, including Pseudomonas species, have been isolated from disease suppressive soils. But it is still unclear whether these bacteria are responsible for the decline in take-all disease.

Summary Points (3.4)

• Soils contain diverse populations of organisms capable of causing plant disease. This immense range of fungal and bacterial pathogens includes organisms highly specialised in how they interact with plants.

• Plant disease occurs with different degrees of severity and more than one organism may be involved.

• Diagnosis of the causal organisms of a plant disease can be determined by applying Koch’s Postulates.

• Several approaches are usually required to identify soil-borne plant pathogens.

• The severity of disease depends on the abundance of the pathogen, which can be dependent on the soil conditions for growth and survival of the organism.

• Pathogens enter roots using highly specialised mechanisms or through wounds on the root surface.

• Plants may react to the presence of pathogens by producing molecules that protect the plant or reduce the probability of disease.

• The incidence of some plant diseases is associated with the nutritional status of the plant.

• Soils develop natural suppressiveness to plant pathogens; organisms may be introduced as ‘biological control agents’ or the activities of disease-suppressing organisms that occur naturally can be maximised.

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