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FORAGE & GRAZINGLANDS

Forage Bermudagrass Cultivar Responses to Inoculations with Exserohilum rostratum and Bipolaris spicifera and Relationships to Field Persistence

^a USDA-ARS, Crop Sci. Res. Lab., Waste Management and Forage Res. Unit, P.O. Box 5367, Mississippi State, MS 39762
^b USDA-ARS, U.S. Dairy Forage Res. Center, Madison, WI 53706-1108

^* Corresponding author (rpratt{at}ars.usda.gov)

	ABSTRACT

TOP NOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION REFERENCES

 
In the southeastern USA, bermudagrass [Cynodon dactylon (L.) Pers.] is a principal species to which animal wastes are applied for nutrient removal. Diseases caused by Exserohilum, Bipolaris, and Curvularia spp. may limit its effectiveness for this purpose. This study evaluated responses of seven forage bermudagrass cultivars (Alicia, Brazos, Coastal, Common, Russell, Tifton 44, and Tifton 85) to two pathogens, E. rostratum (Drechs.) Leonard & Suggs and B. spicifera (Bain) Subram., and persistence of cultivars with natural infection in the field. All cultivars were susceptible to both pathogens with foliar inoculations, but differed in degrees of susceptibility. Alicia was highly susceptible to both pathogens. Coastal was least susceptible to B. spicifera, but no cultivar was consistently least susceptible to E. rostratum. Persistence of cultivars for up to 1 yr in the field differed and appeared related to both sod density and susceptibility to pathogens. Dense sods appeared to enable cultivars to generate more top growth and compensate for disease losses. Common, Coastal, and Tifton 44 bermudagrasses were most persistent in the field; Tifton 85 and Alicia were least persistent. Results indicate that resistance to dematiaceous hyphomycetous pathogens, along with a strong sod-forming ability, is desirable in forage bermudagrass cultivars to sustain their persistence and productivity on animal waste application sites.

Abbreviations: LSD, least significant difference

	INTRODUCTION

TOP NOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION REFERENCES

 
FORAGE BERMUDAGRASS has long been grown throughout the southeastern USA as a crop for grazing and hay by beef and dairy cattle producers (Burton and Hanna, 1985; Hovermale and Cuomo, 1996). In addition to these traditional uses, forage bermudagrass in this region also has come to be used as a receiver crop for land-applied wastes from confined swine and poultry production farms that have increased greatly in number and size in recent years (Burns et al., 1990; King et al., 1990; Poore and Green, 1996; Evers, 1998). These animal wastes contain high levels of phosphorus, and when large quantities of wastes are disposed of by repeated application to the same soils adjacent to production sites, the risk is increased that phosphorus will leach or flow from those soils into surface waters to cause overenrichment and eutrophic pollution (King et al., 1990; Sharpley et al., 1993; Pierzynski et al., 2000).

Animal wastes are applied to bermudagrass or other forages with the intention that the growing grass will absorb and assimilate excess P and N that might otherwise move into surface waters or leach into ground water (Burns et al., 1990; Evers, 1998, Pierzynski et al., 2000). Harvest and removal of hay from animal waste application sites allows removal of assimilated P and N and reduces the likelihood that eutrophic water pollution or increase of N levels in groundwater will be initiated from those sites (Burns et al., 1990; Pierzynski et al., 2000; Brink et al., 2002).

Effective use of bermudagrass to capture excess nutrients from applied animal wastes requires satisfactory production of forage in response to waste applications (Evers, 1998, 2002; Brink et al., 2002; McLaughlin et al., 2004). Diseases that limit growth or persistence of the grass in these situations may not only restrict yields, but also disrupt nutrient removal and pollution control. In recent years, fungal diseases caused by species of Exserohilum, Bipolaris, and Curvularia, which are collectively referred to as "dematiaceous hyphomycetous pathogens," were considered to have this potential on animal waste application sites in Mississippi (Pratt, 2000, 2001, 2005). These pathogens cause necrotic lesions on leaves, stems, stolons, rhizomes, and roots that may spread and intensify to cause loss of stands (Couch, 1995; Smiley et al., 2005). In one study of a swine waste application site, yields of samples from moderately diseased bermudagrass sod that was infected with these pathogens were reduced by approximately 50% in comparison to yields from healthy-appearing grass (Pratt, 2000). Although most of the same fungal pathogens are present on both swine and poultry waste application sites (Pratt, 2001), symptoms are more severe on swine sites where wastes are applied in liquid form (Pratt, 2000, 2005).

Dematiaceous hyphomycetes typically occur on forage bermudagrass on swine waste application sites in Mississippi as fluid complexes of major and minor pathogen species that are subject to change over years, rather than as individually occurring pathogens (Pratt, 2005). Eight species of the three genera were found to occur as components of disease complexes on forage bermudagrass in Mississippi. Of these, E. rostratum is usually the most common species; B. spicifera occurs less frequently overall, but it was one of the most common species on the site where stand dieback was most severe (Pratt, 2000, 2005).

Resistant varieties usually offer the best means for controlling plant diseases. A limited number of cultivars of forage bermudagrass that differ in morphology and agronomic characteristics have been bred or selected in the past 60 yr (Taliaferro and Richardson, 1980; Burton and Hanna, 1985; Alderson and Sharp, 1995; Ball and Pinkerton, 1996; Hovermale and Cuomo, 1996; Taliaferro et al., 2002). However, most of these cultivars do not appear to have been bred or selected for fungal disease resistance, and most have never been critically evaluated for such resistance (Burton and Hanna, 1985; Alderson and Sharp, 1995). Apart from reported resistance of Coastal and ‘Oklan’ to B. cynodontis (Marig.) Shoemaker (Helminthosporium cynodontis Marig.) (Burton and Hanna, 1985), it is not known if any forage bermudagrass cultivars possess either physiological resistance to dematiaceous hyphomycetes or morphological features that might favor their persistence in the presence of these pathogens.

Quantitative resistance to E. rostratum in plants of Common bermudagrass has been demonstrated experimentally with both excised-leaf and whole-plant inoculations (Pratt, 2003). With excised-leaf inoculations, continuous variability in responses, from highly susceptible to moderately resistant, was observed among 40 genotypes randomly selected from Common. However, such relative, quantitative resistance has not yet been incorporated into cultivars or germplasms, with the possible exception of Coastal and Oklan (Taliaferro and Richardson, 1980; Burton and Hanna, 1985).

Use of forage bermudagrass with resistance to dematiaceous hyphomycetous pathogens would likely be beneficial for maintaining or improving forage yield, stand persistence, and pollution control on animal waste application sites. Therefore, this study was undertaken to evaluate the relative susceptibility or resistance of seven cultivars of forage bermudagrass to two individual dematiaceous hyphomycetous fungal pathogens, E. rostratum and B. spicifera, and to evaluate persistence of the cultivars following natural infection by these and other pathogens on a swine waste application site.

	MATERIALS AND METHODS

TOP NOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION REFERENCES

 
Growth of Plants and Inoculation with Individual Pathogens
Rooted stem cuttings of Alicia, Brazos, Coastal, Common, Russell, Tifton 44, and Tifton 85 (Burton and Hanna, 1985; Alderson and Sharp, 1995; Hovermale and Cuomo, 1996; Brink et al., 2003) were transplanted into commercial potting mixture (Miracle-Gro) (Miracle-Gro, Marysville, OH) in 10-cm-diameter clay pots (three cuttings per pot). Cuttings of Common originated from stems of approximately 100 randomly selected genotypes grown in broadcast-seeded field plots. Plants were grown with repeated clipping and applications of 15-30-15 fertilizer (Miracle-Gro) at 2–3 wk intervals until 75% of the surface area of each pot contained stems and stolons. Leaves and stems were 18–24 cm tall at times of inoculation.

Plants were inoculated by spraying spores onto leaves and foliage at known concentrations. Cultures of E. rostratum and B. spicifera were grown aseptically on autoclaved mixtures of wheat (Triticum aestivum L.) and oat (Avena sativa L.) grain, infested grain was comminuted dry in a food blender (Osterizer, Galaxie model, Sunbeam Corp., Boca Raton, FL) (10 g for 10 s on "high, grate"), and particles were evenly dusted over the surface of 2% water agar in large (15-cm-diameter) Petri dishes (1.0 g per plate). After 7–10 d, spores were collected by applying a sticker solution (2% Pel-gel, Liphatech, Milwaukee, WI), over surfaces of plates, scraping with a microspatula, and filtering the spore suspension through double-layer cheesecloth. Spores of three isolates each of E. rostratum and B. spicifera were composited, counted with a hemacytometer and adjusted to concentrations of 2.2–4.4 x 10⁴ and 1.9–2.5 x 10⁵ mL^–1 for the two pathogens, respectively. Additional details of inoculum preparation are as described previously (Pratt, 2000).

Plants were inoculated by individual complete blocks. Pots, one per cultivar, were randomized on a cart, and leaves and stems were sprayed evenly with 140 mL of spore suspension. Control plants received sticker solution alone. Pots were sealed individually in plastic bags with moisture to create a saturated atmosphere and incubated for 3 d under indoor plant growth lights at 25°C (Pratt, 2000) to initiate infection and symptom development. Bags then were removed, and the percentage of leaf and stem tissue with symptoms of necrosis and chlorosis as caused by E. rostratum or B. spicifera was estimated for each pot. Plants were grown in ambient air (18–35°C) from 28 Apr. to 20 May 1999, in all experiments, in the greenhouse for >7 d, and symptom severity was then again estimated.

Two experiments were conducted for each pathogen plus controls. Each experiment used a randomized complete block design with five replicates and the seven cultivars. Low levels of light brown discoloration of lower leaves, often similar to that caused by infection, were observed in control plants incubated for 3 d in humidity in the absence of fungal pathogens. To account for these symptoms, values for pathogens were adjusted by subtracting infection estimates for controls from those for pathogens for each cultivar at 3 and 10 d. Data were subject to analysis of variance for a randomized complete block design combined over two experiments using the PROC MIXED procedure of SAS software (SAS Institute, 1994). For each fungus, significant differences between adjusted cultivar means were identified using a least significant difference (LSD) test at P < 0.05.

Establishment and Evaluation of Field Plots
Persistence of the seven forage bermudagrass cultivars in the presence of natural disease in the field was evaluated in two experiments established in May of 1999 and 2000 on an Ora loam soil (fine-loamy, siliceous, semiactive, thermic Typic Fragiudult) on the swine effluent application site in Clay county, MS, where severe disease symptoms were observed previously in Common (Pratt, 2000). Each experiment was located in an area 12 x 18 m where foliar symptoms were observed during the year before establishment. Experimental areas initially were sprayed three times with glyphosate (N-[phosphoromethyl]glycine) (0.65 mL a.i. m²) at 7- to 10-d intervals to eliminate existing bermudagrass. Row plots 101.6 cm long then were established in randomized complete blocks by transplanting nine rooted stem cuttings into soil at 12.7-cm intervals. Plots were separated by 0.61 m of row within blocks, and 10 blocks in each experiment were separated by 1.83-m alleys. Cultivars were allowed uninhibited growth within a strip 0.7 m wide for each plot, but spread of cultivars across alleys and into adjacent plots was prevented by hoeing and spot-spraying with a contact herbicide (diquat) (6,7-dihydrodipyrido[1,2-a:2',1'-c]pyrazinedium dibromide) (2.17 mL a.i. L). The experiment was located each year under the center pivot for effluent application, and overhead applications usually were applied two or three times per week during the growing season. All cultivars developed full and complete stands in row plots after growth for 2 to 3 mo under this regime of frequent irrigation and ample nutrients for growth.

In early July, after natural disease symptoms first appeared in surrounding bermudagrass, symptomatic foliage was harvested with a lawnmower and scattered over all plots evenly to augment natural infection. Lesions typical of those caused by E. rostratum, B. spicifera, and other dematiaceous hyphomycetes were evident on foliage within plots by late July.

Near the end of the first growing seasons, on 18 Sept. 1999 and 14 Oct. 2000 when all plots had complete stands, and near the beginning of the second seasons on 12 May of both years, each plot was evaluated for persistence by estimating visually the percentages of stand with healthy-appearing sod and foliar regrowth within a band 15 cm wide down the length of each plot 9–14 d after removal of foliage by mowing. For each evaluation time, treatments were compared by analysis of variance after arcsin square root transformation of data and by use of Fisher's protected LSD test at P = 0.05. Correlations of treatment means between evaluation times and experiments also were determined with nontransformed data, and their significance was evaluated at P = 0.05. To verify disease in plots, six samples of dead or symptomatic (necrotic lesions) stolons 3 to 5 cm long were selected randomly from the sod in each plot, in three blocks of each experiment, in September or October, and assayed for pathogens by surface disinfesting, plating on water agar, and observing for sporulation by E. rostratum and B. spicifera (Pratt, 2000).

Sod Density Estimates
Sod densities of the bermudagrass cultivars in the absence of fungal diseases were estimated in June 2001, in four replicate plots (2 x 6 m) of each cultivar that were established independently in a randomized complete-block design in 1996 on a Brooksville silty clay loam soil (fine, smectitic, thermic Aquic Chromudert) (Brink et al., 2003). These plots were located at a different swine waste application site in north central Mississippi approximately 80 km distant from the experimental site. Observations of sod density of cultivars were made at this alternate location because no symptoms of diseases caused by dematiaceous hyphomycetous fungi were ever observed in the plots even by 4 yr after establishment. These observations were made on the premise that differences in sod density there represented features of plant morphology and growth habit that were characteristic of the cultivars. Percentages of the soil surface covered by stolons at ground level, irrespective of the amount of foliage present, were estimated visually in two randomly selected sampling areas (each 0.14 m²) within each plot, and plot means were used as replicate values in analysis. Cultivar means were compared by analysis of variance after arcsin square root transformation of data and by use of Fisher's protected LSD test at P = 0.05. Correlations of treatment means for sod density values with results of field persistence experiments in the presence of diseases were determined with nontransformed data, and their significance was evaluated at P = 0.05.

	RESULTS AND DISCUSSION

TOP NOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION REFERENCES

 
Representative symptoms of disease (Couch, 1995; Smiley et al., 2005) developed in leaves and stems of all bermudagrass cultivars following inoculations with E. rostratum and B. spicifera, indicating that all cultivars are qualitatively susceptible to both pathogens. However, significant differences in severity of symptoms occurred between cultivars at both assay times in combined experiments (Table 1). Although differences between the 3- and 10-d assay times were not compared directly, these appeared to vary and represent the balance for each cultivar between increasing symptom development in inoculated, infected tissues, and the emergence of new, asymptomatic tissues subsequent to inoculation as previously noted (Pratt, 2003). E. rostratum incited more severe symptoms than B. spicifera as previously reported (Pratt, 2000) and also elicited more differences in cultivar responses. Alicia was relatively highly susceptible to both pathogens, and Tifton 44 and Tifton 85 were relatively highly susceptible to E. rostratum. Coastal was numerically least susceptible to B. spicifera. No cultivar was clearly least susceptible to E. rostratum at both evaluation times (Table 1). To our awareness, these results represent the first evaluations of responses of forage bermudagrass cultivars to these specific fungal pathogens.

View this table: [in this window] [in a new window]   Table 1. Severity of disease induced by Exserohilum rostratum and Bipolaris spicifera in seven forage bermudagrass cultivars in combined inoculation experiments.

View this table: [in this window] [in a new window]   Table 2. Correlation coefficients and their significance for responses of seven forage bermudagrass cultivars to Exserohilum rostratum and Bipolaris spicifera in individual inoculation experiments.

If responses of bermudagrass genotypes to different species of dematiaceous hyphomycetes are correlated or related, as suggested from these results, such relationships would be important for bermudagrass improvement, as breeding for resistance then would not necessarily consist of repeated selections for resistance to multiple, independent fungal pathogens. Cross-effectiveness of genetic resistance to different species of pathogens would be especially helpful for the dematiaceous hyphomycetes because these pathogens typically occur on forage bermudagrass in complexes rather than as individual pathogens (Pratt, 2005). Although quantitative resistance to E. rostratum has been demonstrated in Common bermudagrass (Pratt, 2003), it is not yet known whether this resistance is effective against other species and genera of dematiaceous hyphomycetes.

In field experiments, dieback and death of leaves, stems, and stolons were observed in plots of all cultivars at both observation times. Necrotic lesions and chlorosis were present in leaves and stems as in inoculation experiments, but most stand dieback and lack of persistence resulted from lesions that girdled and killed stolons. Exserohilum rostratum and B. spicifera were observed at high frequencies (93–98%) in total samples of necrotic stolons collected at the end of the first growing season and in 80–100% of stolons collected from each entry. Most stolons were naturally infected with both pathogens simultaneously and often with other members of the complex of dematiaceous hyphomycetes that occurs at that site (Pratt, 2000, 2005). Death of portions of stands usually was estimated to be numerically greater after 4 mo than after 1 yr; if stand dieback was in fact less after 1 yr, this may have represented compensation for previous losses by the generation of new stems and stolons from surviving stolons and rhizomes the following spring. Significant differences in persistence of cultivars were observed at all assay times (Table 3) and cultivar means for percentages of stand loss were significantly correlated in five of six possible paired comparisons (Table 4). Tifton 85 and Alicia were always least persistent; Common, Coastal, and Tifton 44 were most persistent; and Brazos and Russell were usually intermediate.

View this table: [in this window] [in a new window]   Table 3. Percentages of stand loss caused by a complex of fungal pathogens in seven forage bermudagrass cultivars at two observation times in two field experiments.

View this table: [in this window] [in a new window]   Table 4. Correlation coefficients and their significance for percentages of stand loss caused by a complex of fungal pathogens in seven forage bermudagrass cultivars at two observation times in two field experiments.

Previous authors have indicated that cultivars of forage bermudagrass differ in sod density; Common and Tifton 44 were considered to form tight, dense sods, while others such as Tifton 85 formed more open, loose, or less dense sods (Ball and Pinkerton, 1996). However, we are not aware of quantitative information published to date to document these observations. In this study, significant differences in sod density, as evaluated by percentages of ground area covered by stolons, were observed among the seven cultivars grown for 4 yr on a different site where disease symptoms fortuitously were not present (Table 5). This site differed from the experimental site, where persistence was evaluated in soil type, irrigation frequency, harvest frequency, and numerous other environmental and management factors. It is not known whether any of these factors may have influenced sod density. However, in the absence of information on variability, the features of sod density observed in the cultivars at the alternate site were presumed to represent characteristic and consistent features of plant morphology or growth habit that would be manifested by the cultivars at other locations also in the absence of disease. On the basis of this presumption, observations of sod density at the alternate site were used to help explain differences in persistence of cultivars at the experimental site.

View this table: [in this window] [in a new window]   Table 5. Percentages of ground area covered by stolons in stands of seven forage bermudagrass cultivars in the absence of fungal diseases.

The influence of sod density appears to have accounted most specifically for the contrasting field performances of Tifton 44 and Tifton 85. Both cultivars responded similarly to E. rostratum and B. spicifera with foliar inoculations (Table 1), but field persistence of Tifton 44 was always far superior to that of Tifton 85 (Table 3). This difference appears to be accountable to formation by Tifton 44 of a much more dense sod that could better sustain stolon losses than that of Tifton 85.

Despite the absence of significant overall correlations between results of foliar inoculation and field experiments, some cultivars showed consistent responses between the two situations. Alicia was relatively highly susceptible to both E. rostratum and B. spicifera with controlled inoculations, and it also was one of the least persistent cultivars in the field despite formation of a moderately dense sod from rooted stolons (Table 5). This suggests that high physiological susceptibility to pathogens was the principal factor that caused lack of persistence of Alicia in the field. In contrast, Coastal appeared to be slightly less susceptible to B. spicifera than most other cultivars including Alicia (Table 1), and this may have accounted for its more favorable field persistence despite a sod density similar to that of Alicia (Table 5).

One exception to the hypothesis that field persistence of forage bermudagrass is favored by both relatively less susceptibility to the two fungal pathogens and relatively dense sods is represented by cultivar Russell. This cultivar manifested poor field persistence (Table 3) despite intermediate susceptibility to the two fungal pathogens (Table 1) and relatively high sod density in the nondiseased stand (Table 5). Reasons for the reduced field persistence of Russell, therefore, are not apparent from results of this study.

In general, short-term persistence of forage bermudagrass in the presence of E. rostratum, B. spicifera, and related pathogens appears to require both physiological resistance and a strong sod-forming ability to reduce the impact of diseases. For more long-term persistence over a year, however, it appears that higher levels of resistance will be required than were observed in any of the seven cultivars used in these experiments. Although Common bermudagrass manifested the highest field persistence in the 1-yr experiments, over longer time periods, portions of stands of Common have been completely killed out by diseases on the same site.

These studies suggest that breeding for fungal disease resistance should be incorporated into forage bermudagrass improvement programs. This may be most necessary for bermudagrass grown on swine waste application sites, where disposal of effluent by overhead irrigation creates conditions especially favorable for infection and disease development. Possibly, if high levels of resistance to E. rostratum, B. spicifera, or other major pathogens can be obtained, then formation of a dense sod from stolons and rhizomes may be of less importance for field persistence than it appears to be in the predominantly susceptible entries evaluated in this study.

	ACKNOWLEDGMENTS

 
The authors thank Mrs. Debbie Boykin, Area Statistician, USDA, ARS, MSA, for assistance in statistical analysis of data from inoculations with individual pathogens, and J. Vetzel, C. Meriwether, M. Martin, G. Kimmel, and M. Begonia for assistance in establishing and maintaining field plots.

	NOTES

TOP NOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION REFERENCES

 
Contribution of the USDA-ARS in cooperation with the Mississippi Agric. and For. Exp. Stn., Mississippi State, MS.

Received for publication December 29, 2005.

	REFERENCES

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This Article Abstract Full Text (PDF) Free Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Pratt, R. G. Articles by Brink, G. E. Search for Related Content PubMed Articles by Pratt, R. G. Articles by Brink, G. E. Agricola Articles by Pratt, R. G. Articles by Brink, G. E. Related Collections Other Forage Crops Plant Disease