Diseases of roots and crowns
L.L. Singleton

Soil-borne disease pathogens of cereals are associated with the invasion of crown and root tissues and their diminished capacity for efficient nutrient and water uptake. In wheat soils, soil-borne pathogens are widely distributed and can cause economic losses in yield. When they are present, soil-borne pathogens negatively influence wheat root growth and development from planting through harvest. In temperate climates, severe pre- and post- emergence damping-off during the first and second week after planting that would require replanting is not a common problem. In most years, soil-borne pathogen damage is less obvious, and disease signs and symptoms do not appear until the latter stages of crop maturity. These effects are manifested in moderate to severe root rot areas after heading when white-headed patches begin to appear. The premature senescence of wheat heads after head emergence from the boot is evident as 'whiteheads' which are partially filled with immature kernels as a result of the damage to the crown and root tissues of the plant caused by root rot pathogens. The white-headed areas in a field can consist of a small percent up to 50 percent or greater. In either case, the whiteheads are representative of the level of grain yield loss. Usually when root rot is present, the level of whitehead occurrence will be greater in years when rainfall is limited and temperatures are high at heading.

With root pathogens, root health becomes a major consideration as emphasized by Bolley in 1913 with the following quote: "When a valuable fertilizer is present and the roots are dead by disease, the wheat plant cannot make use of it. If the roots are healthy, they can make use of it." Thus, Bolley had recognized the importance of a healthy root system. As a result, in root rot-prone areas, the following components of wheat production are stressed: (i) use of a balanced fertility programme; and (ii) good soil preparation and weed and insect control practices. However, it must be recognized that the effectiveness of these practices will be diminished depending on the incidence and severity of the root rot pathogens that are present.

MEASURING ROOT ROT DISEASE EFFECTS

Root pathogens can limit cereal production in many environments (Saari, 1985; Weise, 1987). Recognition of the role of soil-borne pathogens as a factor in limiting wheat production potential in most areas will always be a problem because of the more highly visible foliar pathogen symptomology. Because root and crown rot pathogens attack roots that are growing in soil, demonstrations of their presence and quantification involves more complicated procedures than the simple visual observations needed to detect and quantify the presence of foliar pathogens.

Various procedures are available for elucidating soil-borne disease effects (Wilhelm, 1966; Bland, 1992). Regardless of the methodology, the following should be considered: (i) Does a significant root rot disease problem occur in an area? (ii) What kind of losses are being encountered? and (iii) Which pathogens are involved? Thus, various indirect and direct strategies can be undertaken to answer these questions about a suspect root rot disease situation. The following are presented as examples and are not meant to exclude the use of other approaches.

Indirect approaches

Historically, the importance of soil-borne diseases came about with the development of soil fumigation techniques for the control of Phylloxera on grapes in France (Wilhelm, 1966). These techniques and more recently selective fungicides can be quite useful for indirectly characterizing soil-borne disease problems in an area.

Two advantages of soil fumigation are: (i) it provides information about the importance of soil-borne disease pathogens in an area; and (ii) it provides an estimate of yield potential for a given environment in the absence of the biological components of the soil.

Disadvantages of soil fumigation include: (i) possible overestimation of the contribution of soil-borne pathogens to yield suppression because it also controls weeds, nematodes and other pests; and (ii) it is not an economical control measure for soil-borne pathogens of wheat.

Advantages for selective fungicides are: (i) the effects are specific using ridomil, imazalil and other types of fungicides with well-defined spectra of activity; (ii) they can be used in the form of seed treatment, granular broadcast or in furrow treatment; (iii) they may inexpensively provide an indicator as to the types of pathogens present in a soil environment because of the specificity of their action; and (iv) they may provide preliminary data for economic chemical control for some pathogens. Disadvantages include possible underestimation of total effects of the soil-borne pathogens in an area because of the narrow spectrum of activity, and such fungicides may lead to an increase in damage caused by pathogens outside the spectrum of activity.

Direct approaches

Most soil-borne disease problems can be observed in terms of their seedling disease and mature plant effects (Weise, 1987; Zillinsky, 1983). Seedling disease problems are manifested as poor stands, which would be conspicuous within the first or second week after planting, and depending on the severity of damage as pre- and post-emergence damping-off, replanting maybe necessary. Seedling stands weakened and yellowed as a result of root rot pathogens may not respond to post-plant applications of nitrogen as a true nitrogen deficiency problem would. As a result, lack of response to additional fertilizer applications may provide more evidence that root disease pathogens may be present (Huber and Graham, 1992). Direct examination of the root and crown tissues of diseased plants and healthy plants may provide information about the reasons for these problem. Nutrient deficiency problems would be expected to occur uniformly in a field; however, soil-borne disease problems would appear as irregular and patchy areas throughout a field because of the unlikely occurrence of uniform inoculum distribution in a field.

The major mature plant effects caused by soil-borne pathogens would be variable plant height, premature death of individual scattered tillers and/or quite large irregular areas of dead plants throughout a field. Direct examination of such plants will usually provide evidence of the causal agent.

When the symptomology associated with a root disease problem has been determined, the diagnosis should be confirmed by isolating and pathogenicity testing the causal agent. There are various techniques and methodologies available for this type of work (Dhingra and Sinclair, 1985; Johnson and Curl, 1972; Singleton et al., 1992).

Two approaches to this problem will be suggested here (for more detail refer to the referenced material). The first approach is isolation directly from host tissue for pathogens, such as Fusarium spp., Bipolaris spp., Rhizoctonia spp. and Sclerotium rolfsii, using potato dextrose agar, or selective media have been developed for Fusarium spp. (Papavizas, 1967) and Bipolaris spp. (Stack, 1977).

The second approach consists of isolation from diseased host roots using a 'baiting' technique for Pythium spp. or Gaeumannomyces. Wheat seeds are planted directly into a root mass of washed field-collected roots, covered with sterile soil and allowed to grow for six to seven days. The emerging seedling roots are then carefully removed, washed thoroughly and plated directly onto cornmeal agar (1/5X, i.e. 0.20X concentration). Usually, pathogen growth from these seedlings will be quite rapid. Without this step, these pathogens may be completely masked by the direct plating of field-collected root pieces because of their inability to compete with other pathogens that may be present, such as Bipolaris and Fusarium. The next step would involve testing the isolated strains of a given pathogen to determine if they are pathogenic (Gilchrist, 1985; Singleton et al., 1992).

Yield losses

With soil-borne pathogens of cereals, there are problems connected with accurately determining disease incidence and severity and the yield loss associated with them. Root pathogen identification is more difficult compared to foliar pathogen evaluation because: (i) symptoms are not directly observable since the roots and crown tissues have to be extracted from the soil; (ii) above-ground symptomology, such as yellowing, stunting, etc., is indistinct and can be confused with nutrient deficiency problems and with soil drainage problems; and (iii) more than one pathogen can be present.

In Oklahoma, United States, hard red winter wheat (Triticum aestivum L.), a versatile and profitable crop, is grown as a cash grain crop (averaging 4.08 million tonnes) and with proper management can also serve a dual purpose in providing winter grazing for livestock (50 to 60 percent of 2.4 to 2.8 million ha). Oklahoma's production systems can be categorized as: (i) cash grain production; (ii) forage production only; and (iii) combination forage/grain production. With the latter, the producer has the option of utilizing the forage production for grazing and also taking a cash grain crop. These production options for wheat production place Oklahoma producers in a position of greater economic competitiveness.

Wheat production is not without risks because of environmental constraints imposed by variable rainfall patterns and temperature extremes. In addition to environmental risks, there are hazards associated with soil-borne pathogens, insects and weed pests. In Oklahoma, wheat root rot nematode disease research has shown that forage and grain yields are being conservatively reduced by an average of 77 percent and 16 percent in root rot-prone areas (two years and five locations, respectively; Russell and Singleton, unpublished data). Thus, grain and forage production is not just simply environmentally limited, but is also affected by soil-borne fungi and nematode pathogens. Therefore, effective measures for soil-borne disease control are of critical importance.

MAJOR ROOT ROT DISEASES

In Oklahoma, soil-borne pathogens encompass a complex of soil-borne fungi and nematodes as pathogens. These soil-borne pathogens attack plant tissues associated with the roots and crown of the wheat plant. The ultimate result is the destruction of root and crown tissues that interferes with soil water and nutrient utilization. The most severe damage by these pathogens occurs in association with forage and grain production systems where early September planting is necessary. The following fungal pathogens are important components in the Oklahoma root rot disease complex.

Common root rot

Common root rot is caused by Bipolaris sorokiniana Sac. in Sorok. (syn. Helminthos-porium sativum P.K. & B.) (Luttrell, 1963, 1964; Saari, 1985; Shoemaker, 1959). For common root rot, the most characteristic symptomology would be brown- to black-coloured lesions on the sub-crown internode, and typically lesion severity increases throughout the growing season. Thus, lesion incidence and severity can be monitored throughout the growing season as long as the sub-crown internodes remain intact. Hence, similar to dryland root rot and take-all, the destruction of the sub-crown internode by common root rot can result in whitehead symptoms as the plants approach maturity. In more humid climates, there may be potential for progression into a foliar blight phase (Weise, 1987), where it can cause distinct dark to black lesions on the leaves.

Dryland root rot

Dryland root rot is caused by Fusarium culmorum (W.G. Smith) Sac., F. graminearum Schwabe and other species (Booth, 1977; Francis and Burgess, 1977; Nelson et al., 1983; Zillinsky, 1983). As wheat nears maturity, one may observe the development of scattered white-headed areas consisting of a few tillers to large irregular patchy areas involving many plants. The lower internodes of plants with whitehead symptoms will be dark to light brown in colour when Fusarium spp. are involved. In most climates, the development of whiteheads will be correlated with drought stress because as the level of drought stress increases, whitehead symptoms increase proportionately in root rot-prone areas.

Browning root rot

Browning root rot is caused by Pythium spp. (Middleton, 1943; Plaats-Niterink, 1981; Waterhouse, 1967, 1968; Weise, 1987). Host range studies (McCarter and Littrell, 1970) point out that given species can have relatively broad host ranges in attacking both soybeans and wheat to some degree. Pythium damage in the field can result in stunting and yellowing of plants, which can be quite obvious, although almost indistinguishable from nitrogen deficiency problems (Weise, 1987). Upon direct examination of the roots, however, if Pythium is involved, roots will be stunted and have a water-soaked appearance with dark to reddish-brown coloration. Oospores maybe observable in such tissue by staining with lacto fuchsin (0.1 g acid fuchsin/100 ml lactic acid) (Carmichal, 1955).

Take-all

Take-all is caused by Gaeumannomyces graminis var. tritici (Sacc.) Arx & Oliv. (syn. Ophiobolus graminis Sac.) (Weise, 1987). Damage in temperate areas is primarily associated with the occurrence of irregular patchy areas of prematurely dead plants (whiteheads) similar to that caused by Fusarium, for example. Examination of the lower internodes will reveal the presence of a deep black charcoal-like discoloration of the roots and lower internodes of the wheat plants that is distinctly different from the symptomology caused by Fusarium. Microscopically, a superficial black network of mycelia will be present on infected root surfaces.

Rhizoctonia root rot and sharp eyespot

Rhizoctonia root rot and sharp eyespot are caused by Rhizoctonia solani Kühn and R. cerealis Van der Hoeven, respectively (Carling and Sumner, 1992; Weise, 1987). Rhizoctonia can cause seedling blight damage and/or mature plant damage. As a mature plant problem, sharp eyespot (causal agent R. cerealis) can cause eyespot-like lesions on lower culms, which can result in weakening of the stem and subsequent lodging. In Oklahoma, this pathogen is widely distributed and occurs in conjunction with dryland root rot. Sharp eyespot produces an elliptical eye-spot like lesion on the outer leaf sheaths that later penetrate directly through to the basal culms tissue proper.

SOIL-BORNE DISEASE CONTROL

Control of soil-borne diseases of wheat is a challenge for pathologists, breeders and other plant scientists. A listing of all the soil-borne pathogens that will be encountered was not intended to be provided here. Based on the available literature, probable soil-borne pathogen candidates have been presented. Also, precise control recommendations for all soil-borne pathogens cannot be given, but various principles or approaches for control will be presented. Some sources for control recommendations and principles for soil-borne disease control can be found in the references (Cook and Baker, 1983; Dickson, 1956; Garrett, 1965; Kommedahl and Williams, 1983; Weise, 1987. Most disease control measures encompass the following basic principles: exclusion, eradication and protection (Stakman and Harrar, 1957) and will only be mentioned here. Once a soil-borne pathogen has been found in an area, it is practically too late to take advantage of either exclusion or eradication as control measures.

Most soil-borne pathogens are: (i) endemic and environmentally adapted for survival; (ii) have broad host range capabilities; and (iii) survive as resistant propagules in soil and/or as mycelia in crop debris. Obviously, control measurers cannot have much of an influence on the endemic and adapted characteristics of a soil-borne pathogen. However, once a pathogen is known to be present, control recommendations must be developed for it. For example, there are some possibilities for control of pathogens with specific environmental requirements for survival. Take-all is favoured by alkaline soils that are deficient in nitrogen and phosphorus (Weise, 1987). As a result, it may be possible to decrease the soil fertility, thus effectively putting the pathogen at a disadvantage in relation to the host.

The broad host range capabilities of soil-borne pathogens must be dealt with in terms of host resistance. Also, the possibility for diversification in developing and using rotation systems that include non-hosts should be explored. Unfortunately, this may seem to be an unlikely possibility with the group of pathogens covered here. However, in cases where a pathogen has a narrow host range, advantage must be taken of such a weakness in a pathogen's life cycle. Most soil-borne pathogens have some well-adapted means of survival in the soil as propagules and/or in association with plant debris. Thus, most soil-borne disease control practices will utilize various cultural and chemical controls and host resistance in an integrated package with other agronomic practices. The expected result will be a programme that will allow the producer to economically produce a wheat crop.

Cultural control

Cultural control includes tillage, soil fertility, green manure crops, crop rotation and sanitation practices. With these approaches, the main objective is to reduce pathogen inoculum levels and their effects to such an extent that the producer can attain an economic return. Tillage methods would include burying infested host residues to hasten decomposition of pathogen propagules and infested plant debris, thus exposing a pathogen to direct competition with other soil saprophytes. Obviously, these practices will be more effective against the more fastidious pathogens, such as G. graminis var. tritici, and less effective against pathogens such as S. rolfsii. Where it is possible, crop rotation schemes should be employed to avoid situations where a previous crop will produce inoculum for the next.

As shown in Table 19.1, planting dates are a critical component of the expression of root rot disease damage. With early planting (late August to early September), soil temperatures at planting depth are high (32°C), and soil pathogens are more aggressive in attacking seedlings. As shown, maximum and minimum soil temperatures declined as planting dates were delayed by two-week intervals. Also, disease incidence values declined as the planting dates were delayed. Thus, there was apparently a lessened amount of infection of wheat seedlings as soil temperatures declined. By contrast, grain yields increased as planting dates were delayed. Thus, the later plantings were escaping the effects of damage by soil-borne pathogens as a result of the lower soil temperatures at planting. These results are representative of the fact that greater disease and yield loss from soil-borne pathogens occurs with early planting for forage and grain production. Therefore in root rot-prone areas, the following grower recommendations are suggested:

• In areas of chronic root rot disease pressure, cultural control by delayed planting (15 October) is suggested as an effective alternative to early planting.

• In Oklahoma environment, growers will have to be educated as to the risks associated with early planting practices.

Chemical control

With the development of chemicals with systemic capabilities in addition to protectant action, there has been an increase in the possibilities for soil-borne disease control. For example, it was found that triadimenol as a seed treatment could delay the development of take-all on spring wheat for up to 53 days (Mathre et al., 1986). Such results with this compound and others, such as ridomil for Pythium spp. and imazalil for common root rot control, indicate the need for further work of this type. These are short term solutions and are not the ultimate answer to a soil-borne disease problem. The author has found that these compounds do work well for controlling a specific pathogen. However, in the field there is usually more than one pathogen at a time, and the control of one only opens up the opportunity for another pathogen to cause damage. Thus, there is a need to develop chemicals with broader spectra of activity and/or to use them in combination.

TABLE 19.1
Maximum and minimum soil temperatures, root rot disease incidence and grain yield for four planting dates, Oklahoma, United States, 1994

^a Mean disease incidence from four replications per ten culms was obtained by a summation of the severity ratings for 1st and 2nd internodes after their conversion as follows: ³ 2 to 1, and < 2 to 0 with the total sum being divided by two.

Source: Singleton and Krenzer, 1996.

Host resistance

Without a doubt, effective root rot disease resistance characters are going to be necessary for efficient and stable wheat production where root pathogens are a consistent problem. The question arises: Will pathologists and breeders put the effort forward to identify and utilize host resistance against these pathogens? The following points must be considered and resolved. The genetics of resistance to soil-borne pathogens is largely unknown (Bruehl, 1983), and the modes of inheritance are generally found to be complex, involving more than one or two genes (Bruehl, 1983). Thus, pathologists and breeders are going to be dealing with characters, such as yield, where many genes may be involved. Secondly, such resistance characters may be functionally inoculum-dependent (high levels of inoculum may mask the effectiveness of a resistance character). These problems and others will have to be worked out through the cooperation of pathologists and breeders if progress is going to be made in controlling soil-borne pathogens with host resistance genes. For these and other reasons, the development of soil-borne, disease-resistant cultivars is not going to be an easy task. However, it will be necessary if a stable level of wheat production is going to be attained in root rot problem areas. When programmes are initiated and areas are chosen for developing resistance cultivars, research must be conducted under environmental conditions that favour the pathogen if functional levels of host resistance are to be identified. Too often, the tendency is towards carrying out selections under conditions that favour the host, which may not reflect the actual worth of the cultivar.

ACKNOWLEDGEMENTS

The author wishes to thank Dr C.C. Russell and Dr E.G. Krenzer, Jr.

REFERENCES

Bland, W.L. 1992. Quantifying plant-root development. In L.L. Singleton, J.D. Mihail & C.M. Rush, eds. Methods for Research on Soilborne Phytopathogenic Fungi, p. 225-235. St Paul, MN, USA, American Phytopathological Society Press. 264 pp.

Bolley, H.C. 1913. Wheat troubles and soil deterioration. ND Agric. Exp. Sta. Bull., 107: 1-98.

Booth, C. 1977. Fusarium laboratory guide to identification of the major species. Kew, Surrey, UK, Commonwealth Mycological Institute.

Bruehl, G.W. 1983. Nonspecific genetic resistance to soilborne fungi. Phytopathology, 73: 948-951.

Carling, D.E. & Sumner, D.R. 1992. Rhizoctonia. In L.L. Singleton, J.D. Mihail & C.M. Rush, eds. Methods for Research on Soilborne Phytopathogenic Fungi, p. 157-165. St Paul, MN, USA, American Phytopathological Society Press. 264 pp.

Carmichal, J.W. 1955. Lacto fuchsin: a new medium for mounting fungi. Mycologia, 47: 611.

Cook, R.J. & Baker, K.F. 1983. The nature and practice of biological control of plant pathogens. St Paul, MN, USA, American Phytopathological Society Press.

Dhingra, O.D. & Sinclair, J.B. 1985. Basic plant pathology methods. Boca Raton, FL, USA, CRS Press.

Dickson, J.G. 1956. Diseases of field crops, 2nd ed. New York, NY, USA, McGraw & Hill Book Company.

Francis, R.G. & Burgess, L.W. 1977 Characteristics of two populations of Fusarium roseum graminearum in eastern Australia. Trans. Br. Mycol. Soc., 68: 421-427.

Garrett, S.D. 1965. Toward biological control of soilborne plant pathogens. In K.F. Baker & W.C. Snyder, eds. Ecology of soilborne plant pathogens, p. 4-17. Berkeley, CA, USA, University of California Press Berkley.

Gilchrist, L.I. 1985. CIMMYT methods for screening wheat for Helminthosporium sativum resistance. In Wheats for more tropical environments, p. 149-151. Mexico, DF, CIMMYT.

Huber, D.M. & Graham, R.D. 1992. Techniques for studying nutrient-disease interactions. In L.L. Singleton, J.D. Mihail & C.M. Rush, eds. Methods for Research on Soilborne Phytopathogenic Fungi, p. 204-214. St Paul, MN, USA, American Phytopathological Society Press. 264 pp.

Johnson, L.F. & Curl, E.A. 1972. Methods for research on the ecology of soilborne plant pathogen. Minneapolis, MN, USA, Burgess Publ.

Kommedahl, T. & Williams, P.H., eds. 1983. Challenging problems in plant health. St Paul, MN, USA, The American Phytopathological Society.

Luttrell, E.S. 1963. Taxonomic criteria in Helminthosporium. Mycologia, 55: 643-674.

Luttrell, E.S. 1964. Systematics of Helminthosporium and related genera. Mycologia, 56: 119-132.

Mathre, D.E., Johnston, R.H. & Engel, R. 1986. Effect of seed treatment with tradimenol on severity of take-all of spring wheat caused by Gaeumannomyces graminis var. tritici. Plant Dis., 70: 749-751.

McCarter, S.M. & Littrell, R.H. 1970. Comparative pathogenicity of Pythium aphanidermatum and Pythium myriotylum to 12 plant species and intraspecific variation in virulence. Phytopathology, 60: 264-268.

Middleton, J.T. 1943. The taxonomy, host range and geographic distribution of the genus Pythium. Memoirs of the Torrey Botanical Club, 20: 1-170.

Nelson, P.E., Toussoun, T.A. & Marasas, W.F.O. 1983. Fusarium species. University Park, PA, USA, The Pennsylvania State University Press.

Papavizas, G.C. 1967. Evaluation of various media and antimicrobial agents for isolation of Fusarium from soil. Phytopathology, 57: 848-852.

Plaats-Niterink, A.J., van der. 1981. Monograph of the genus Pythium. Centralbureau voor schimmelcultures, Baarn. Studies in Mycol. No. 21.

Saari, E.E. 1985. Distribution and importance of root rot diseases of wheat, barley and triticale in south and southeast Asia. Wheats for more tropical environments, p. 189-195. Mexico, DF, CIMMYT.

Shoemaker, R.A. 1959. Nomenclature of Drechslera and Bipolaris grass parasites segregated for Helminthosporium. Can. J. Bot., 37: 879-887.

Singleton, L.L. & Krenzer, G. 1996. Seed treatment, variety and planting date effects on sharp eyespot and Fusarium root rot at Perkins. Biol. Cul. Tests, 11: 91.

Singleton, L.L., Mihail, J.D. & Rush, C.M., eds. 1992. Methods for research on soil-borne phytopathogenic fungi. St Paul, MN, USA, American Phytopathological Society Press. 264 pp.

Stack, R.W. 1977. A simple selective medium for isolation of Cochilobolus sativus from diseased cereal crowns and roots. PDR, 61: 521-522.

Stakman, E.C. & Harrar, J.G. 1957. Principles of plant pathology. New York, NY, USA, The Ronald Press Company.

Waterhouse, G.M. 1967. Key to Pythium pringsheim. Commonwealth Mycological Institute. Mycological Papers, 109: 1-15.

Waterhouse, G.M. 1968. The genus Pythium pringsheim. Commonwealth Mycological Institute. Mycological Papers, 110: 1-71; 50 illustration.

Weise, M.V., ed. 1987. Compendium of wheat diseases, 2nd ed. St Paul, MN, USA, APS Press, American Phytopathological Society. 112 pp.

Wilhelm, S. 1966. Chemical treatments and inoculum potential of soil. Ann. Rev. Phytopath., 4: 53-78.

Zillinsky, F.J. 1983. Common diseases of small grain cereals: a guide to identification. Mexico, DF, CIMMYT.