Seedling Disease and Damping-off. Poor stand establishment of sorghum may involve interactions of several biotic and abiotic factors, but in the United States ...
Pythium Root and Seedling Rots
Pythium Root and Seedling Rots G.N. Odvody and G. Forbes* Summary Pythium spp cause a root and mesocotyl rot of sorghum seedlings in cold, wet soils and a root rot of mature sorghum in warm, wet soils. Identity of the causal species is incomplete for several reasons, including changing and variable nomenclature, isolate variability, and differences in interpretation of fungal structures in culture. Pythium can cause death of seedlings and mature plants, and although disease incidence and severity are influenced by several environmental factors, temperature and moisture are most important. Seed treatments with most fungicides are generally ineffective in controlling seedling disease, but new, specific systemic fungicides need to be evaluated for efficacy against pythium seedling disease and pythium root rot of mature plants. There is host plant resistance against both, but better characterization of the resistance is needed. More knowledge is needed concerning the mechanism of pathogen survival, initial inoculum, initial infection, and the influence of specific host-pathogenenvironment interactions.
In the literature of the past several decades, numerous reports describe identified and unidentified Pythium spp occurring on sorghum roots, and most are discussed either in the review by Tarr (1962) or the publication by Pratt and Janke (1980). Most published information concerning Pythium as a sorghum pathogen is fraught with confusion because of errors in isolation, inoculation, species identification, and establishment of particular isolates as actual causal agents of observed disease in the field (Pratt and Janke 1980). Although Pythium arrhenomanes is a true root pathogen of sorghum, its erroneous, long-term acceptance as the causal agent of milo disease (Elliott et al. 1937) until 1948 (Leukel 1948) has cast further doubt on many earlier reports. The great majority of reports of Pythium on sorghum refer to its occurrence on young seedlings in the field, but there are some reports of its occurrence on mature plants (Frederiksen et al. 1973, Pratt and Janke 1980). The reported susceptibility of sorghum seedlings to
Pythium isolates from other hosts provided no beneficial information, because the results obtained under controlled environmental conditions were never related to disease occurrence in field-grown sorghum (Pratt and Janke 1980). Difficulties in species identification, nomenclatural changes, and disagreement about either the characteristics of species or their synonomy further confuse earlier reports.
Seedling Disease and Damping-off Poor stand establishment of sorghum may involve interactions of several biotic and abiotic factors, but in the United States environment has often been considered the most important through the direct, detrimental effects of low soil temperature, saturated soil, and soil crusting (Leukel and Martin 1943). The involvement of fungal pathogens in preand postemergent damping-off of sorghum was
*Plant Pathologist/Assistant Professor, Texas A&M University Agricultural Research and Extension Center, Rt.2, P.O. Box 589, Corpus Christi, TX 78410; and graduate student, Department of Plant Pathology and Microbiology, Texas A&M University, College Station, Texas 77843, USA. International Crops Research Institute for the Semi-Arid Tropics. 1984. Sorghum Root and Stalk Rots, a Critical Review: Proceedings of the Consultative Group Discussion on Research Needs and Strategies for Control of Sorghum Root and Stalk Rot Diseases, 27 Nov - 2 Dec 1983, Bellagio, Italy. Patancheru, A.P. 502 324, India; ICRISAT.
31
first studied extensively by Leukel and Martin (1943), who distinguished between seedborne and soilborne pathogens attacking seeds and seedlings in soil. They tried to determine the effect of pathogens on germination, emergence, and subsequent growth of the seedling. Research by Leukel and Martin (1943) and others demonstrated that fungicide seed treatments reduced preemergent damping-off associated with several seed-rotting fungi (e.g., species of Aspergillus, Rhizopus, Penicillium, and Fusarium), which rapidly colonize unprotected seed primarily in cold, wet soils. Sometimes Penicillium and Fusarium spp proceed to parasitize the host tissue and cause postemergent damping-off. However, Pythium is the fungus most frequently isolated from diseased seedlings grown in cold, wet soil, and Leukel and Martin (1943) demonstrated that Pythium spp isolated from root and mesocotyl lesions of sorghum seedlings were highly virulent to sorghum planted in soils with high moisture and low temperature (15°C). Standard fungicide treatments do not protect against infection by Pythium attack, probably because either the site of parasitic attack is distal to the seed or the fungicide (captan or thiram) has no significant effect on Pythium. Symptoms on seedlings are either brown or gray water-soaked roots or root tips, or lesions on roots (Forbes 1983) that become flaccid and necrotic (Edmunds and Zummo 1975). Lesions also occur on the plumule and mesocotyl (Leukel and Martin 1943, Forbes et al. 1983), and the mesocotyl produces somewhat more pigment in response to the pathogen than do the roots (Odvody, unpublished observation, 1983). However, the lesion pigmentation is less than that induced by other soilbome pathogens, e.g., Fusarium (Edmunds and Zummo 1975). Plants succumbing to postemergent damping-off usually wilt rapidly and die, but often many stunted plants remain alive despite the loss of most leaves and Pythium damage to the roots and mesocotyl (Odvody, unpublished observation, 1983; Edmunds et al. 1970). However, there is usually wide variation in plant height and spacing throughout affected fields, and many plants may be adversely affected throughout subsequent development (Edmunds et al. 1970).
manes was erroneously considered the cause of "milo disease" in Texas and other areas of the United States where this disease occurred (Elliot et al. 1937). Severe root rot in the North Texas High Plains in 1971-72 (Frederiksen et al. 1973) was caused by a species of Pythium identified as P. graminicola (Pratt and Janke 1980). Symptoms on the large adventitious (or buttress) roots are darkened and blackened roots (Frederiksen et al. 1973) and sunken red-brown to black root lesions, and sometimes at root death the entire lesion or root has a tan color (Pratt and Janke 1980). Fusarium spp and other fungi may rapidly follow attack by Pythium spp (Odvody, unpublished observation, 1982) and cause greater pigmentation of lesions than Pythium alone (Edmunds and Zummo 1975). Once established, these secondary fungi are more easily isolated (Frederiksen et al. 1973) than the primary pathogenic Pythium. In 1972, stalk rots (caused primarily by Fusarium spp) followed development of the pythium root rot and were important causes of subsequent stalk lodging (Frederiksen et al. 1973). Isolates of Pythium obtained from roots of mature plants were highly virulent on sorghum seedlings (Frederiksen et al. 1973, Pratt and Janke 1980), but the occurrence of similar Pythium strains in seedling infections in the field is unknown. On the North Texas High Plains, root infections of sorghum began to increase at the boot stage or later when large numbers of adventitious roots were being produced in irrigated fields (high soil temperature and high soil moisture conditions) (Odvody, unpublished observation, 1983). Pratt and Janke (1980) demonstrated that P. graminicola from roots could cause stalk rot when plants were inoculated at maturity, but it is probably not the cause of stalk rot in the field. At one South Texas location, Pratt and Janke (1980) isolated P. myriotylum and P. periplocum from insect-damaged roots and stalks of mature sorghum. Only the former was pathogenic on sorghum seedlings inoculated in the greenhouse. Because only one site was investigated, the extent of the natural occurrence of P. myriotylum on mature sorghum roots is unknown.
T a x o n o m y of Pathogens Root Rot of Mature Plants The occurrence of Pythium spp on roots of mature plants was first reported in 1937, when P. arrheno-
32
The changes in Pythium taxonomy during the past few decades present both problems and benefits in understanding the occurrence of this pathogen on sorghum. Hendrix and Campbell (1973) proposed
that P. graminicola and P. arrhenomanes form a complex in which isolates have characteristics that constitute a continuum between the two typespecies and that other similar complexes exist. This helps clarify some of the older literature and may lend more support for the pathogenic activities of Pythium reported in 1937, despite its erroneous identification with milo disease (Elliott et al. 1937). The Pythium spp attacking seedlings also remain insufficiently characterized. Forbes (1983) demonstrated that a majority of isolates from infected seedlings grown in a field soil in the greenhouse produced lobulate sporangia but only 50% of those produced oospores in culture. The characteristics of these latter isolates were most similar to P. arrhenomanes as described by Drechsler (1936).
Etiology and Infection Pythium spp pathogenic to sorghum probably survive in soil as oospores (Hendrix and Campbell 1973). Saprophytic growth may be of minor importance because Pythium is a poor competitor that apparently colonizes tissue only when other organisms are either absent or relatively inactive due to environmental factors (Hendrix and Campbell 1973). Other data (Hendrix and Campbell 1973) indicate that oospores of Pythium spp pathogenic to sorghum germinate in response to host seed and root exudates in wet soil—either directly by producing germ tubes or indirectly by producing zoospores that encyst and then germinate. The pathogen then rapidly penetrates host cells and tissues that lack secondary wall thickenings (Hendrix and Campbell 1973). Although numerous environmental factors influence these germination and infection processes by the pathogen, temperature and moisture (especially in combination) are the two most important ones (Hendrix and Campbell 1973, Leukel and Martin 1943), probably because of their additional effect on the host plant and associated soil microflora. Under cold, wet soil conditions, germination of seed and growth of seedlings are slowed such that emergence is delayed, primary root growth is reduced, and in older seedlings, new roots are slow to establish from the mesocotyl and crown. The transitory root system of emerging seedlings is especially vulnerable to attack in cold, wet soils (Edmunds and Zummo 1975), and the delay in production of the permanent root system from the crown is probably one of the greatest factors involved in postemer-
gent damping-off. We have often observed the primary root system and mesocotyl of 2-week-old seedlings being killed by Pythium, but without postemergent damping-off because a healthy, permanent crown root system was established in the well-drained upper soil layer. Pythium pathogens isolated from seedlings may have an optimum growth temperature in culture much different from the environment in which they are normally pathogenic (Hendrix and Campbell 1973). Thus, the pathogen's competitive ability in the soil-plant environment may be more important than its ability to grow in a noncompetitive cultural environment. However, the Pythium root rot that occurs on mature plants in warm, wet (floodirrigated) soil of the North Texas High Plains correlates well with the high optimum temperature reported for P. graminicola (Waterhouse and Waterston 1964a) and P. arrhenomanes (Waterhouse and Waterston 1964b). Infection in these mature plants appeared to occur on roots of all sizes and ages, but initial infections may have occurred earlier in root development (Odvody, unpublished observation, 1983). For both pythium seedling disease and mature plant root rot, nothing is known about either the levels of inoculum or the increase and secondary spread of the pathogen. In maize, oospores and sporangia of Pythium are rapidly formed in infected tissues (Nyvall 1981), and oospores, sporangia, and coenocytic mycelia have been observed in roots of infected sorghum seedlings (Forbes et al. 1983). However, the role of these sporangia and zoospores in the infection of proximal, healthy roots of the same and different plants is not known. The influence of previous crops and of tillage and cultural practices on Pythium diseases in sorghum is not known, but these variables are conjectured to have some effect, especially in relation to initial inoculum and soil moisture and soil temperature (Leukel and Martin 1943, Hendrix and Campbell 1973). The incidence and severity of pythium root rot on mature sorghum may be directly affected by irrigation and irrigation frequency.
Potential Control with Fungicides Most fungicides applied to sorghum seed are not effective in controlling damping-off caused by Pythium (Leukel and Martin 1943), but some new systemic fungicides, like metalaxyl and fosetyl-A1,
33
may provide the previously lacking protection of tissues distal to the seed. The additional cost of seed treatment must be compared with the potential for pythium seedling diseases in the planting area. There is a continued need for additional fungicides like captan to control the principal seedrotting fungi, because most of the potentially effective systemic fungicides are specific for Phycomycetes.
Potential Control Through Host Plant Resistance Host plant resistance to Pythium attack in the seedling stage is not well defined, but most germplasm is thought to be susceptible in disease-conducive cold, wet soil. In general, varieties are more susceptible than hybrids, and plants from either old or low-quality seed are more susceptible than those from either young or high-quality seed. Although some cultivars were less affected by Pythium caused damping-off in the field (Forbes et al. 1983), the reason for and consistency of the reduced damage is not known. The multiplicity of factors involved with stand establishment in the field necessitates evaluations in controlled environments to determine major factors responsible for increased stand establishment. For a particular genotype, the increased stand in cool, wet soils could be due either to resistance to Pythium or to physiological and physical factors like continued germination and growth under these conditions, rapid establishment of a permanent root system, and secondary thickening of cell walls in outer root tissues. Any stress factor that delays establishment of the permanent root system from the coleoptile and upper nodes probably increases the potential for Pythium caused seedling damage or dampingoff in cool, wet soils. Varieties are likely more susceptible to Pythium damage because of their reduced vigor. They are generally slower to germinate, emerge, and establish a permanent root system. Plants from old seed of hybrids (and varieties) are more susceptible than plants from young seed because their reduced vigor is especially apparent in cool, wet soils. Plants from either nontreated or damaged seed are also more susceptible to seedling disease, not only because Pythium can attack more readily, but also because other seed-rotting fungi additionally reduce vigor and delay emergence and plant establishment (Leukel and Martin 1943).
34
The Pythium disease syndrome on mature plants is incompletely characterized, but some genotypes (e.g., Tx 2751, Tx 2737) demonstrate more lateseason plant death associated with Pythium than do others. However, other pathogens and factors may either promote Pythium attack or contribute to plant death. Root wounding by nematodes and insects may be a contributing factor (Frederiksen et al. 1973), as might primary and secondary infections by other root pathogens like Fusarium and Periconia. Additionally, genotypes may differ in their tolerance to similar amounts of root loss caused by Pythium (Odvody, unpublished observation, 1983).
Research Needs 1.
Better characterization of Pythium species or species complexes that are pathogenic to sorghum roots.
2.
Determination of geographical and local variation in Pythium spp pathogenic to sorghum.
3.
Improved understanding of initial inoculum, germination stimuli, type of germination (direct or indirect), type of infective propagules (oospores, sporangia, or zoospores), site of infections), and importance of secondary spread of the pathogen.
4.
Improved knowledge of environmental factors necessary for disease development and how they interact with the pathogen, soil microflora, and host to cause disease.
5.
Development of meaningful screening techniques to identify resistant genotypes and to determine mechanisms of field resistance or susceptibility.
6.
Determination of the effects of cropping sequence, tillage, and cultural practices (especially irrigation in relation to mature-plant root rot) on disease incidence and severity and on increase in soilborne inoculum.
7.
Investigation of other edaphic and biotic factors that influence disease incidence and severity.
8.
Evaluation of new systemic fungicides for ability to control Pythium on seedlings and mature sorghum.
References
Mycological Institute) Descriptions of plant pathogenic fungi and bacteria Kew, Surrey, U.K.: CMI. 2 pp.
DRESCHLER, C. 1936. Pythium graminicolum and P. arrhenomanes. Phytopathology 26:676-684. EDMUNDS, L.K., FUTRELL, M.C., and FREDERIKSEN, R.A. 1970. Sorghum diseases. Pages 200-234 in Sorghum production and utilization (eds. J.S. Wall and W.M. Ross). Westport, Connecticut, USA: AVI Publishing Co. EDMUNDS, L.K., and ZUMMO, N. 1975. Sorghum diseases in the United States and their control. U.S. Department of Agriculture Handbook No. 468. Washington, D.C., USA: U.S. Government Printing Office. 47 pp.
Questions Partridge: You indicated Fusarium follows Pythium infection. Is there a predominant Fusarium that is isolated from roots following Pythium?
ELLIOTT, C., MELCHERS, L.E., LEFEBVRE, C.L., and WAGNER, F.A. 1937. Pythium root rot of milo. Journal of Agricultural Research 54:797-834.
Odvody: We didn't routinely identify these Fusarium species except to determine their presence, because Pythium was so predominantly isolated.
FORBES, G.A. 1983. Development of a technique for screening seedlings of Sorghum bicolor (L.) Moench for resistance to seedling disease. M.Sc. thesis, Texas A&M University, College Station, Texas, USA.
Partridge: Do cold-tolerant sorghums tend to be resistant?
FORBES, G.A., COLLINS, S.D., ODVODY, G.N., and FREDERIKSEN, R.A. 1983. Seedling disease in South Texas in 1983. Sorghum Newsletter 26:124-125. FREDERIKSEN, R.A., ROSENOW, D.T., and TULEEN, D. 1973. Pythium root rot of sorghum on the Texas High Plains 1972. Sorghum Newsletter 16:137-138.
Odvody: Not in the limited number observed in the field, but more research is needed to clarify this important aspect of seedling disease.
HENDRIX, F.F., Jr., and CAMPBELL, W.A. 1973. Pythiums as plant pathogens. Annual Review of Phytopathology 11:77-97. LEUKEL, R.W. 1948. Periconia circinata and its relation to milo disease. Journal of Agricultural Research 77:201 222. LEUKEL, R.W., and MARTIN, J.H. 1943. Seed rot and seedling blight of sorghum. U.S. Department of Agriculture Technical Bulletin 839. 26 pp. NYVALL, R.F. 1981. Diseases of com (Zea mays L). Pages 55-86 In Field crop diseases handbook. Westport, Connecticut, USA: AVI Publishing Co. PRATT, R.G., and JANKE, G.D. 1980. Pathogenicity of three species of Pythium to seedlings and mature plants of grain sorghum. Phytopathology 70:766-771. TARR, S.A.J. 1962. Diseases of sorghum, sudan grass and broom corn. Kew, Surrey, U.K.: Commonwealth Mycological Institute. 380 pp. WATERHOUSE, G.M., and WATERSTON, J.M. 1964a. Pythium graminicola. No. 38 in CMI (Commonwealth Mycological Institute), Descriptions of plant pathogenic fungi and bacteria, Kew, Surrey, U.K.: CMI. 2 pp. WATERHOUSE, G.M., and WATERSTON, J.M. 1964b. Pythium arrhenomanes. No. 39 in CMI (Commonwealth
35
