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Soilborne Crop Pathogens Under Direct Seeding: FusariumRichard
Smiley, Professor of Plant Pathology, Oregon State University, Fusarium is a diverse genus of fungi that includes several soilborne plant pathogens. These pathogens damage small grain cereals by rotting seed, seedlings, roots, crowns, basal stems or heads of wheat, barley, oats, corn, grasses and some broadleaf crops. Damage to spring and winter cereals are often unnoticed until whiteheads appear shortly before the crops mature, or until shriveled grain is noted during harvest. Damage can be highly variable within fields. Several pathogenic species and genera cause similar damage and are typically present in different proportions in each geographic region. The disease complex is therefore dominated by different pathogens in different areas, or even by different pathogens during successive growing seasons on individual fields. Primary members of the pathogen complex in the Pacific Northwest (PNW) include Fusarium culmorum, F. pseudograminearum (previously known as F. graminearum Group 1), F. graminearum (= F. graminearum Group 2, or Gibberella zeae), F. avenaceum, Microdochium nivale (= F. nivale), and Bipolaris sorokiniana (= Cochliobolus sativus). Diseases caused by these fungi are known by a variety of names, including dryland foot rot, Fusarium foot rot, dryland root rot, Fusarium root rot, common root rot, and Fusarium crown rot. Dryland foot rot is the name commonly applied to the complex in winter wheat-summer fallow rotations in the PNW, and Fusarium crown rot is the name commonly applied to this complex in spring cereals. Common root rot is the name officially recognized by the American Phytopathological Society, but is considered unacceptable to this author because that name refers specifically to a complex heavily dominated by B. sorokiniana in the Prairie Provinces of Canada and the Northern Plains of the USA. Fusarium culmorum and F. pseudograminearum usually dominate the complex in the PNW. Therefore, Fusarium foot rot, or foot rot for short, will be the disease names used in this paper. Foot rot fungi are considered "unspecialized" pathogens because they can attack any plant tissue if conditions at the tissue surface are favorable for infection. These pathogens also have ecological differences that influence their survival and pathogenicity. For instance, F. culmorum and B. sorokiniana survive adverse conditions mostly as resiliant spores either in plant residue or soil. F. pseudograminearum and F. avenaceum survive mostly as relatively fragile mycelium inside plant residue. Resiliant spores are often able to remain viable over longer periods than mycelial fragments that depend upon protection by undecomposed plant tissue. These differences are very important to the dominance among foot rot pathogens in tillage-intensive systems but are less important in direct-drill systems where all forms of inoculum are more concentrated near the soil surface. This is so because the principal infection site for each of these pathogens depends on the vertical distribution of crop residue or spores in soil. Infections occur mostly in crowns or stem bases in direct-drill systems in which most residue is at or near the surface. Infection sites are mostly at a lower level below the surface (crown, subcrown internode, root, or seed) when most of the residue is incorporated or burned. These spacial relationships are typically modified further by subtle differences among pathogen species and by soil temperature and moisture. All of these pathogens cause chronic infections, with measurable effects on yield becoming most apparent when cereals are subjected to water stress and/or warm temperatures late in the growing season, or are kept wet by growing crops under irrigation or in regions of high rainfall. Each of the pathogens can also be seed-borne, providing immediate potential for seed rot or damping-off of seedlings emerging from untreated seed. It is readily apparent that the foot rot disease is very complex even though it is very common and symptoms are quite uniform. Management of damage by Fusarium foot rot has been heavily dependent on practices that are not necessarily aligned with preferred agronomic or economic considerations, or with uncontrollable events related to weather. For instance, these management practices include adjustments in planting dates and in the balance of nitrogen fertility with respect to anticipated availability of water to the crop late in the growing season. Disease control and farm profitability could be improved by incorporating genetic resistance into the integrated management practices already recognized. However, at least three obstacles impeded the search for genetic resistance. First, it became clear that routine disease ratings in region-wide breeding nurseries were yielding highly diverse rankings among varieties, depending on the season and geographic region. More precise screening programs would be exceedingly expensive and could not be guaranteed to identify germplasm with stable resistance across regions. Definitive knowledge of economic damage caused by foot rot was not documented, and was therefore necessary to determine if expanded expenditures could be justified for the search for genetic resistance. Moreover, it is likely that genetic resistance will differ for the various pathogens involved in this disease complex. The search for resistance would therefore have to be initially focussed upon only one species and expanded later to include other species. As such, selection of the first "target" pathogen required a better understanding of which one was the most important across the region, and how each of the species are influenced by geographic and seasonal diversity. Objectives of this study were to determine the 1) economic damage caused by foot rot, 2) geographic distribution of foot rot pathogens in the PNW, and 3) resistance or tolerance among wheat varieties and breeding lines. ECONOMIC DAMAGE Commercial fields of mature winter wheat were selected for sampling during 1994. Seven fields were in Oregon (Gilliam and Sherman counties) and six were in Washington (Benton and Walla Walla counties). Varieties in each field were determined after sampling was complete. All plants in 10-foot row sections were dug from two randomly selected areas in each of the 13 fields. Numbers of plants with and without symptoms of foot rot were recorded. Tillers were then separated and leaf sheaths removed to expose culms. Tillers in each sample were separated into root rot classes representing the extent of culm browning. Foot rot severity classes were D0 (none), D1 (browning up to the first node), D2 (second node), D3 (third node), and D4 (4th node or above). Measurements of plant characteristics within each foot rot classification included numbers of tillers, tillers without heads, percentage of headed tillers, straw weight, tiller height, grain weight, grain protein (calculated by multiplying percent N in grain by 5.7), and kernel weight. Estimates of crop damage were based on regression analyses of disease severity characteristics on individual tillers. Characteristics for calculating yield loss included five disease severity classes (described above), number of headed tillers (T) in each severity class, and grain weight/tiller for tillers in each severity class (GDx), where the "x" in "Dx" represents disease severity class numbers 0, 1, 2, 3, or 4. The measured yield (MY) for each bundle was calculated by adding grain weights obtained from heads in each severity class. Potential yield (PY) was calculated by adding numbers of headed tillers in each severity class and multiplying the sum by the grain weight/tiller, as obtained from healthy tillers in class D0. The percentage yield loss (%YL) was then calculated by subtracting MY from PY, multiplying by 100, and dividing by PY. For example, if MY was 42 bu/acre and PY was estimated at 45 bu/acre, the percent yield loss from foot rot would be 6.7 percent. Equations for these calculations were as follows: MY
= GD0+GD1+GD2+GD3+GD4 PY = (TD0+TD1+TD2+TD3+TD4) GD0 The 13-field sample from four counties during 1994 included six winter wheat varieties; Gene (1 field), Lewjain (1), Madsen (3), Malcolm (1), Stephens (5), and Weston (2). Percentages of plants with foot rot ranged from 24 to 98 percent, with a mean of 76 percent. Percentages of tillers affected ranged from 6 to 90 percent. The sample size was too small to reach conclusions on relative susceptibility among varieties. Overall, foot rot reduced all plant and yield characteristics examined (Table 1). Increasing disease severity ratings were associated with decreasing numbers of kernels/head, kernel weight, grain weight/head, percentage tillers with heads, straw weight/tiller, and head height. There was a tendency for protein to increase with severity of disease but the relationship was not statistically significant, and appeared to be masked by excess protein in most samples. Five fields with lowest protein were therefore evaluated as a sub-group (Table 1). Compared to the 13-field analysis, the lower-protein sub-group exhibited more pronounced effects of foot rot on kernel weight, grain weight/head, tiller height, yield loss, and protein content. When all tillers were evaluated, foot rot in the 13 fields reduced yields by 0 to 35 percent (average of 9 percent). Grain yield was correlated with the percentage of tillers in disease severity class D4. Yield declined by 1 percent for each 1 percent of tillers in D4 (Table 2). Similar relationships were found for calculations based on the five fields planted to Stephens, and the five lower-protein fields. Yield loss relationships were also evaluated by comparing two groups of four fields selected for either high or low foot rot severity, from among the 13 fields sampled. Yield losses for plants in four "lightly" and four "heavily" affected fields averaged 3 percent and 18 percent, respectively (Table 3). Numbers of plants with foot rot and numbers of headed tillers/foot of row were similar in the light and heavily affected fields. Compared to heavily affected fields, lightly affected fields had a higher proportion of tillers in disease severity classes D0 and D1, and a lower proportion of tillers in classes D3 and D4. Protein did not differ significantly among groups of fields when evaluated on the basis of entire bundles (Table 3) or sub-samples for disease severity classes D0 (healthy) through D3 (moderately severe). Grain from D4 tillers had higher protein in the heavily affected than lightly affected fields; 15.7 and 12.5 percent protein, respectively; lsd=2.0.
These data indicate that yield losses from foot rot are important in semiarid regions of eastern Oregon and Washington, where 185 million bushels of winter wheat were produced on 3.2 million acres in 1992, for a farm gate value exceeding $700 million. Average yield in these counties during 1992 was 42 bushel/acre, and the average market price for grain was $3.85/bushel. A 9 percent yield loss for the 13-field sample represents a direct economic loss of $15.40/acre. The 18 percent loss in four heavily affected fields represented a negative impact of $30.80/acre. The 13 fields were selected at random, before symptoms of foot rot were evident. If the varieties and climates of these fields and counties represent 20 percent of the non-irrigated winter wheat acreage in eastern Oregon and Washington, estimates of direct economic damage from foot rot in the region would be 3.6 million bushels, or $14 million. Further economic loss would occur if test weight decreased, or protein increased, to the extent of reducing the market grade. Comparable data are not available for spring cereals. FOOT ROT PATHOGENS Winter wheat plants and soil were collected during 1993 from 146 fields in 10 Oregon counties (Baker, Gilliam, Jefferson, Malheur, Morrow, Sherman, Umatilla, Union, Wallowa, Wasco) and seven Washington counties (Adams, Asotin, Benton, Columbia, Lincoln, Walla Walla, Whitman). In 1994 there were 142 samples collected from the in-crop field nearest that sampled during 1993, and the survey was expanded to include Franklin and Klickitat counties in Washington. Numbers of fields sampled were proportional to acres of winter wheat harvested in each county during 1992, with a minimum of two samples/county. Fields were selected randomly. Samples consisted of collecting soil between drill rows, and plants in the row, while moving in a circle 100- to 200-feet inside each field. After sampling, extension agents assisted in compiling field histories and identification of varieties. Crown tissue was dissected from 15 plants/field. Each half of each crown segment was cultured in the laboratory on a different medium that favored isolation of either Fusarium or Bipolaris. Soil samples were evaluated for pathogens that survive as spores in soil. Fungi isolated from crowns or soils were transferred to two additional media for identification. The 1991-1992 growing season had normal precipitation except for abnormally wet periods during April and July. Excellent soil moisture in the summer fallow prompted many growers to plant winter wheat earlier than normal in the autumn of 1992, leading to numerous instances of severe crown rot as early as November in some fields. Winter and spring for the 1992-1993 season were very wet, leading to 20 percent higher than normal precipitation for the crop year. The summer, autumn, and winter of the 1993-1994 season were very dry. Plantings were often delayed until rains began during November. Plants showed signs of drought stress as early as April 1994. Samples were collected from 178 wheat fields in 10 Oregon counties and 110 fields in nine Washington counties (Figure 1). Crowns excised from plants and plated onto culture media in the laboratory included 3,445 from Oregon and 1,945 from Washington. Percentages of fields yielding isolates of the foot rot fungi in each state are presented in Table 4. F. pseudograminearum was isolated more frequently than F. culmorum during each year in each state. The third-most prevalent pathogen was F. avenaceum during 1993 (wet year), and M. nivale during 1994 (dry year). The least prevalent pathogen was B. sorokiniana during 1993 (wet year), and F. avenaceum during 1994 (dry year). Results illustrated that yearly fluctuations in prevalence occurred among these pathogens.
The pathogen complex within individual counties was also diverse and variable (Table 5). The dominant pathogens region-wide were F. pseudograminearum and F. culmorum. Lack of isolation of these pathogens in Columbia County WA was an artifact; foot rot clearly also occurs in that county. M. nivale was prominent in two Oregon counties. B. sorokiniana was present in six Oregon counties but did not appear to be a dominant member of the root rot complex. B. sorokiniana and M. nivale each appeared dominant in three Washington counties during 1994. Frequent identification of each pathogen in eastern Oregon and Washington, and seasonal variability for their dominance in the complex, indicates that all may be important in some areas during some years. This complexity indicates that chemical, cultural, and genetic disease management strategies must be developed to improve overall plant health rather than specifically targeting only one or two pathogen species. This will be challenging and will surely involve combinations of fungicides, varieties, rotations, and management practices such as timing, placement and rate of nitrogen application, and management of surface residue. These diseases and their management are likely to increase in importance in high-residue cropping systems and short rotations. Foot rot and yield were assessed on 69 wheat and one triticale entry during two growing seasons (2000 and 2001) at the Columbia Basin Agricultural Research Center, near Pendleton. Soil was a Walla Walla silt loam. Trials each year were planted into different fields, both of which were maintained as cultivated summer fallow for 14 months following harvest of lentil (1999-2000 experiment) or winter wheat (2000-2001 experiment). Wheat was planted during late September into 5 x 20 foot plots with a John Deere HZ deep-furrow drill equipped with a cone-seeder and four openers spaced at 14 inches. Each wheat entry was planted in paired plots, one with and one without supplemental inoculum consisting of five isolates of F. pseudograminearum collected from infected wheat crowns in Oregon and Washington during 1993 and 1994. Inoculum was prepared by infesting autoclaved millet seed with an isolate of the pathogen, drying the inoculum, and mixing the five isolates in equal proportions. Inoculum was banded one inch directly above the wheat seed to force the wheat coleoptile to emerge through the zone of infestation. Inoculum was metered from a Gandy spreader mounted on the seed drill, and dispensed at about 140 millet seeds (0.7 g) per foot of row. Wheat seed was treated with Benlate (0.7 oz/cwt seed) to reduce pre-emergence damping-off by the pathogen. Wheat was planted at 23 seeds/square foot and 3-inch depth into moist soil covered with 1.5-inch dust mulch during 1999, and at 25 seeds/square foot and 1.5-inch depth into moist soil during 2000. Data included assessments of emergence, stand density, plant growth, disease incidence and severity, whiteheads, grain yield, test weight, and kernel weight. Selected data are reported for 16 named varieties. The 1999-2000 experiment was planted into soil with sub-optimal moisture for seed germination. Emergence was slow and seedlings were stressed until autumn rains began on October 28, 1999. Supplemental inoculum of the pathogen was in the air-dry dust mulch for five weeks from planting until soil was moistened. In contrast, rain began on September 3, 2000 and soil was continuously wet into the winter. Inoculum was therefore placed into moist soil at the time of seeding during the 2000-2001 experiment. The 20-year mean crop-year precipitation (September-August) at the experimental site is 17.9 inch; deviations for experiments in 1999-2000 and 2000-2001 were +7% and -9%, respectively. Placement of millet seed inoculum colonized by F. pseudograminearum above the seed did not significantly affect seedling emergence, plant stand or tillering, but increased (p<0.05) foot rot indices and reduced yield and test weight (Table 6). Inoculation of the 70 wheat and triticale entries reduced grain yields by an average of 11-12%, with ranges of 2-28% in 1999-2000 and 0-22% in 2000-2001 (Table 7). Varieties exhibiting the least damage by F. pseudograminearum were Alzo triticale and Brundage, Gene and Eltan winter wheat. Promising breeding lines were also identified for future emphasis. Varieties with high impacts from the pathogen included Bruehl, Coda, Connie, Dusty, Lambert, Lewjain and Rohde. Whiteheads were more prevalent during 2000-2001 than 1999-2000. Regression analysis revealed highly significant correlations between grain yield and percentages of whiteheads during both years. Yield in the inoculated-plot series was associated with yield reductions of 6.5 and 0.9 bu/ac for each percentage of whiteheads during 1999-2000 and 2000-2001, respectively. The first year, with the higher impact of the whitehead disease symptom, was a comparatively wet year that began with an exceedingly dry autumn. The second year, in which the disease apparently had a smaller impact, was a comparatively dry year that began with a very wet autumn and planting season. While whiteheads are an indicator of Fusarium foot rot as well as other diseases, it was clear that the relationship between whiteheads and economic damage is not consistent (in a quantifiable sense) from year to year.
Modern diagnostic systems are being developed to detect and quantify to amount of inoculum for soilborne plant pathogens in soil and plant tissue. These systems are based on the extraction of pathogen DNA directly from soil or plants. Scientists at the South Australian Research and Development Institute (SARDI), Adelaide, Australia developed tests for root pathogens of small grain cereals into a commercially available testing system. These tests are proprietary with SARDI and have now been licensed to C-Qentec Diagnostics, a subsidary of Aventis CropScience. Farmers in Australia are currently able to obtain a report on the amount of inoculum of soilborne pathogens for about $A4 per acre. The results for the fungal pathogens are expressed as picograms (pg) of DNA of the pathogen per gram of soil. For parasitic nematodes, the results are expressed as numbers of nematodes (or eggs) per gram of soil. Tests currently available include Fusarium pseudograminearum and F. culmorum (Fusarium crown rot), Gaeumannomyces graminis var. tritici (take-all), Rhizoctonia solani AG-8 (Rhizoctonia root rot), Heterodera avenae (cereal cyst nematode), and Pratylenchus species (lesion nematodes). A similar set of diagnostic systems has been under development at Pendleton since 1998. We have evaluated tests for Pythium (9 species), Fusarium (5 species), three Gaeumannomyces graminis (3 varieties), and Rhizoctonia (2 species). The systems have been particularly valuable for rapidly and precisely identifying the pathogens, identifying components of disease complexes that are very difficult to evaluate using traditional methods, and providing improved insight into processes of disease development and pathogen spread in plants and soil. For instance, the DNA tests at Pendleton have shown that a pathogen such as R. solani AG-8 is endemic throughout the Inland PNW, that there is no correlation between the presence of the pathogen and expression of the acute phase (bare patch) of the disease, and that the pathogen spreads through soil well in advance of the appearance of stunted plants the following season. Drs. Jim Cook and Tim Paulitz (WSU and USDA-ARS, Pullman, WA; personal communication) recently arranged with SARDI to conduct DNA tests on 124 soil samples representing GPS-referenced sites over 30 acres on the WSU Cunningham Agronomy Farm near Pullman. F. pseudograminearum was detected in 66% of the soil samples, with 30% recorded at 50-100 pg of DNA per gram of soil (low infestation), 30% at 100-500 pg/g of soil (medium infestation), and 7% at greater than 500 pg DNA of this pathogen per gram of soil. One sample had more than 1500 pg DNA of this pathogen per gram of soil. F. culmorum was present in all 124 soil samples at 30 to 300 pg DNA per gram of soil (low to intermediate). Both pathogens have been isolated from plants with crown rot in this field in earlier years, but this is the first indication of the widespread presence of the two pathogens as a mixture in this field. While it was not uncommon to detect multiple pathogens within individual fields and sometimes individual plants during the survey of pathogens reported earlier in this paper, the DNA report from SARDI suggests that the mixtures may be much more common than has been detected by traditional means. This would support the observation that the species dominance in the foot rot complex differs from year to year even within a single field, presumably due to poorly understood influences of weather and farming systems on the biology of these pathogens. As with the other root diseases of wheat, and even moreso with Fusarium crown rot, having inoculum of the pathogens in the soil is only half the requirement for development of disease. The other requirement is having the right environment for infection and disease development. In spite of the presence of both pathogens in the 30-acre Cunningham Farm field, spring wheat yielded 64 bushels per acre during 2001. While drought conditions such as occurred in the 2001 crop year would normally have favored this disease, and did result in severe outbreaks of Fusarium crown rot in drier areas of the Inland PNW, obviously the soil conditions on the Cunningham Farm were not conducive to this disease in 2001. Nevertheless, the pathogen is obviously maintaining its population under the conditions on this farm and could, in any year, produce havoc in a wheat or barley crop. CONCLUSIONS Fusarium foot rot causes important economic damage to winter and spring cereals in the Pacific Northwest. Yield suppressions for winter wheat in this study varied from zero to 35 percent, with a mean of 9 percent. The disease is caused by a complex of pathogens that differ in importance among fields, and also from season to season within fields. While the dominant pathogens in the Pacific Northwest are F. pseudograminearum and F. culmorum, it is often difficult or impossible to predict which of these pathogens, or another of the foot rot pathogens, will have the dominant influence on yield. Due to its overall dominance, F. pseudograminearum was selected as the pathogen for the first phase of enhanced screening for resistance to foot rot in wheat. In collaboration with Dr. Jim Peterson (OSU), high variability in genetic susceptibility to F. pseudograminearum was demonstrated among winter wheat varieties and breeding lines. Resistance screening with this pathogen was recently expanded to include spring wheat and club wheat, in collaboration with Drs. Kim Kidwell (WSU) and Kim Campbell (USDA-ARS), respectively. Additional collaboration is now also underway with scientists in South Dakota, South Australia, Queensland, and international centers in Syria (ICARDA), and Mexico and Turkey (CIMMYT). Further development of molecular-based diagnostic systems will also assist in gaining an improved understanding of the complexity of the foot rot disease and interactions with other diseases and the environment. ACKNOWLEDGEMENTS Funding was provided by the Oregon Wheat Commission, USDA-CSRS-Pacific Northwest STEEP Research Program, Cooperative Research Agreement with the USDA-ARS (Pullman), and Oregon Agricultural Experiment Station. Appreciation is expressed for assistance by OSU and USDA-ARS technical research staff at Pendleton, Dr. Jim Peterson (OSU Wheat Breeder), OSU and WSU Extension Service faculty, and growers who provided access to their fields. FURTHER READING Cook R.J. 1980. Fusarium
foot rot of wheat and its control in the Pacific Northwest. Plant Dis.
64:1061-1066. Cook, R.J., and R.J.Veseth.
1991. Wheat Health Management. Amer. Phytopathol. Soc., St. Paul, MN.
152 p. Melanson, D.L., and
S.A. Easley. 2001. Molecular detection of cereal root pathogens in eastern
Oregon. pp. 25-26 in I.J. Porter (ed.). Proc. Second Australasian Soilborne
Diseases Symposium. Lorne, Victoria. Nelson, P.E., T.A.
Toussoun, and R.J. Cook (eds.). 1981. Fusarium: Diseases, Biology, and
Taxonomy. Pennsylvania State Univ. Press, University Park, PA. 457 p. Ophel-Keller, K.,
and A. McKay. 2001. Root Disease Testing Service: Delivery and commercialisation.
pp. 17-18 in I.J. Porter (ed.). Proc. Second Australasian Soilborne Diseases
Symposium. Lorne, Victoria. Smiley, R.W., and
L.-M. Patterson. 1996. Pathogenic fungi associated with Fusarium foot
rot of winter wheat in the semiarid Pacific Northwest USA. Plant Dis.
80:944-949. Sturz, A.V., and
C.C. Bernier. 1989. Influence of crop rotations on winter wheat growth
and yield in relation to the dynamics of pathogenic crown and root rot
fungal complexes. Canad. J. Plant Pathol. 11:114-121. Windels, C.E., and Holen, C. 1989. Association of Bipolaris sorokiniana, Fusarium graminearum Group 2, and F. culmorum on spring wheat differing in severity of common root rot. Plant Dis. 73:953-956. |
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