Occurrence of Foliar Fungal and Bacterial Diseases of Dry Bean in North Dakota

2006 Plant Management Network. Accepted for publication 7 June 2006. Published. Occurrence of Foliar Fungal and Bacterial Diseases of Dry Bean in North Dakota R. Harikrishnan, L. E. del Río, R. S. Lamppa, R. Padilla, F. Zabala, M. Gregoire, and C. A. Bradley, Department of Plant Pathology, North Dakota State University, Fargo 58105 Corresponding author: L. E. del Río. Luis.delrio-Mendoza@ndsu.edu Harikrishnan, R., del Río, L. E., Lamppa, R. S., Padilla, R., Zabala, F., Gregoire, M., and Bradley, C. A. 2006. Occurrence of foliar fungal and bacterial diseases of dry bean in North Dakota. Online. Plant Health Progress doi:10.1094/php-2006-0915-01-rs. Abstract An extensive field survey was undertaken during the 2003 to 2005 growing seasons to assess the prevalence and incidence of foliar fungal and bacterial diseases affecting dry bean in North Dakota. A total of 250 fields were inspected during the three years of survey. The most prevalent diseases were common bacterial blight, white mold, and bacterial brown spot. Common bacterial blight was prevalent in nearly 100% of the fields inspected in all three years, with a mean incidence of 54%. White mold was observed in 75% of the fields scouted, with a mean incidence of 16%. Bacterial brown spot and halo blight affected 31% and 1% of the fields surveyed, respectively. Rust and anthracnose were observed only in 2003 and 2005, affecting 15% and 5% of the fields inspected across both years, respectively. This survey information on the occurrence and severity of diseases affecting dry bean should help prioritize future research needs and breeding programs. Introduction North Dakota currently ranks first both in terms of area and production of dry edible bean (Phaseolus vulgaris L.) in the United States. Over the three years of this survey, approximately 220,000 ha/year were planted to dry bean, with an average estimated production value of US $120 million/year (15). Dry bean is a composite of several market classes including pinto, navy, black, small red, kidney, cranberry, and other beans. However, pinto bean is the predominant market class in North Dakota and constitutes over 50% of the dry bean hectarage. Numerous diseases that could potentially cause yield and economic losses affect dry bean. Grower surveys have been conducted for the past several years to identify important production constraints and to help develop research priorities (12,13). However, a rigorous survey of the relative occurrence of different foliar fungal and bacterial diseases would provide more accurate information that could be used to track changes in disease epidemics, as well as understand the long-term impact of weather on diseases. As a first step towards a more regular monitoring of the various foliar fungal and bacterial diseases that affect dry bean production in North Dakota, field surveys were conducted in the 2003, 2004, and 2005 growing seasons. Survey Area and Disease Assessment In all three years, surveys were conducted in fields located in Grand Forks, Pembina, Steele, Traill, and Walsh counties, accounting for nearly 60% of the hectarage planted to dry bean in the state (15). A total of 250 rain-fed dry bean fields were arbitrarily selected for inspection during 2003 to 2005. Selected fields were separated by at least 2 to 3 km. Surveys were conducted between late August and early September for all three years when the crop was in R4-R6 stages (mid- to late-pod filling). In each field, ten sites were selected along a zigzag pattern with at least 10 m between sites. At each site, 20 plants were assessed for various foliar fungal and bacterial diseases resulting in a total of 200 plants examined per field. In this

survey, "prevalence" was defined as presence or absence of a particular disease in a field and expressed as percentage of the fields surveyed. "Incidence" was the percentage of plants per field affected by a particular disease. Initial identification of the various foliar fungal and bacterial diseases observed was made based on symptoms as described in the Compendium of Bean Diseases (19). Data collected were analyzed using PROC GLM of SAS (SAS version 8.0, SAS Institute Inc., Cary, NC) and mean separation of various diseases across years were carried out using Fisher s Least Significant Difference Test at P = 0.05. Representative samples of all diseases observed were brought back to the laboratory to confirm field identifications. Fungal pathogens were isolated following standard procedures and identified by their macro and/or micro morphological characteristics, while bacterial pathogens were isolated and identified using specialized media as described by Jackson and Moser (11). Pure cultures of bacterial pathogens were inoculated onto seedlings of Maverick, a pinto bean, at the two-leaf-stage. Leaves were pin pricked and spray inoculated until run-off using 10 5 colony forming units (cfu)/ml water. Inoculated plants were incubated at > 90% relative humidity at 22 ± 2 C for two days and then left on greenhouse benches for an additional 10 days before observing for symptoms. No efforts were made to identify other biotic or abiotic stress factors affecting dry bean during the surveys. Koch s postulates were fulfilled for the pathogens from the representative disease samples by both morphological characteristics and biological indexing. The most prevalent fungal disease in all three years of survey was white mold (WM), caused by Sclerotinia sclerotiorum (Lib.) de Bary. Both prevalence and incidence of WM were significantly different across the three years of survey. White mold was prevalent in 72%, 100%, and 54% of the fields surveyed in 2003, 2004, and 2005, respectively, with a mean incidence of 14%, 28%, and 6%, respectively (Fig. 1a). The second most prevalent fungal disease was rust, incited by Uromyces appendiculatus (Pers.: Pers) Unger. Rust was found only in 2003 and 2005, affecting an average 15% of the fields with 7% mean incidence across both years (Fig. 1b). Anthracnose caused by Colletotrichum lindemuthianum (Sacc & Magnus) Lams. Scrib., was the least common fungal disease observed and was found only in 2003 and 2005 with an average 5% prevalence and 1% incidence across both years (Fig. 1c).

Fig. 1. Distribution of fungal diseases in field surveys conducted in 2003, 2004, and 2005. Prevalence and incidence of white mold (A), rust (B), and anthracnose (C). Bars followed by the same letter across years are not significantly different according to Fisher s Least Significant Difference Test at P = 0.05. The most common bacterial disease as well as the most prevalent disease in these surveys was common bacterial blight (CBB), caused by Xanthomonas axonopodis pv. phaseoli (Smith) Vauterin et al. CBB was observed in nearly 100% of the fields in all three years, with a mean incidence of 73%, 53%, and 35% in 2003, 2004, and 2005, respectively (Fig. 2a). Bacterial brown spot (BBS), caused by Pseudomonas syringae pv. syringae Van Hall and halo blight (HB), caused by Pseudomonas syringae pv. phaseolicola Burkholder were also observed. Average BBS prevalence was significantly greater in 2005 (48%) than in 2003 (28%) and 2004 (17%). However, average incidence was significantly greater in 2003 (11%) compared to 2004 (5%) and 2005 (3%) (Fig. 2b). Both prevalence and incidence of HB averaged 1% in both 2003 and 2004. HB was not observed in 2005 (Fig. 2c).

Fig. 2. Distribution of bacterial diseases in field surveys conducted during 2003, 2004, and 2005. Prevalence and incidence of common bacterial blight (A), bacterial leaf spot (B), and halo blight (C). Bars followed by the same letter across years are not significantly different according to Fisher s Least Significant Difference Test at P = 0.05. No letters indicate a nonsignificant F- test. Weather Prevailing weather conditions were monitored during the surveys. Daily mean maximum air temperature and mean rainfall were recorded during the growing season (May through August) from ten North Dakota Agriculture Weather Network (NDAWN, North Dakota State University, Fargo) stations situated across the counties surveyed. In addition, the previous eight years of daily mean maximum air temperature and mean rainfall was obtained from the same stations as reference for comparing weather patterns during the three years of survey. Weather data collected were analyzed using similar procedures as disease data. Both daily mean maximum air temperature and mean rainfall during the growing season were variable during the three-year survey. Daily mean maximum air temperature was significantly lower in 2004 compared to 2003, 2005 and to the 8-year average across all four months, with August of 2004 being one of the coldest on record (Fig. 3a). Daily mean maximum air temperature ranged from 15.8 C in May of 2004 to 28.5 C in August of 2003, while the 8-year daily mean maximum air temperature ranged from 18.8 C in May to 27 C in August. Compared to 2003, 2005, and to the 8-year average, the daily mean maximum air temperature from May through August of 2004 was

cooler by an average of 2 to 3 C. The daily mean rainfall for the month of May was greater than the 8-year average in all three years of this study. June of 2005 (5.8 mm/day) was the wettest month compared to 2003, 2004, and 8-year average. However, the daily mean rainfall for July was lower than the 8-year average for all three years, while in August the daily mean rainfall was normal (8-year) in 2004 and 2005, but was significantly lower in 2003 (Fig. 3b). Fig. 3. Daily mean maximum temperature (A) and daily mean rainfall (B) for the months of May to August for 8-year, 2003, 2004, and 2005. Average of weather data recorded from 10 representative weather stations of North Dakota Agriculture Weather Network. Bars followed by the same letter letters for a year within a month are not significantly different according to Fisher s Least Significant Difference Test at P = 0.05. Summary and Conclusions To our knowledge, this is the first attempt to survey fields to enumerate the prevalence and incidence of different foliar fungal and bacterial diseases that affect dry bean production in North Dakota. The most common diseases ranked in decreasing order of prevalence were common bacterial blight (CBB), white mold (WM), rust, bacterial brown spot (BBS), halo blight (HB), and anthracnose. Prevalence and incidence of WM greatly varied with year and was regulated by prevailing weather conditions (3). The three years in which surveys were carried out were vastly different in terms of temperature and rainfall, the two most influential environmental variables for WM development (1). Year 2004 was significantly cooler and had significantly higher WM compared to 2003 and 2005. Further, the cooler temperatures in July and August (flowering period) of 2004 delayed normal crop growth and potentially extended the infection period and disease development phase of WM. Rainfall was generally greater throughout the growing region in 2004 compared to 2003 but was similar to

2005, which additionally favored greater WM development in 2004. Ascospores of S. sclerotiorum need cool and wet conditions for germination and infection of petals or flowers (1). Other possible reasons for the difference in WM prevalence and incidence among the three years are the availability of inoculum and use of fungicides by growers in the different fields inspected. However, grower surveys indicate that in general less than 30% of them use fungicide for WM control (12,13). Earlier research has shown that yield losses ranging from 12 to 23 kg/ha can occur for every percent increase in white mold incidence depending on the market class (6). Nonetheless, it is clear from our study that the high incidence of white mold observed in the 2004 season resulted in severe economic losses. Rust, which has the potential to cause 100% crop damage, was a major concern for North Dakota growers in the past. Bean rust reached epidemic proportions during early to mid 1990s (9). Rust was found affecting dry bean only in 2003 and 2005 and with the exception of one field in Pembina County in the 2003 season, the severity of its attack was never found at high enough levels to reduce yields significantly. Rust was not detected in the 2004 season; it is possible that the very cold winter during 2003, one of the coldest in history, may have reduced the survival of inoculum in the fields (8). Additionally, the release of numerous cultivars resistant to rust, including Maverick in 1997 (2,7), has significantly reduced rust s importance as a yield-limiting factor (12,13). In 2002, Maverick was planted in approximately 30% of the dry bean hectarage in North Dakota (2). Such wide spread use of a single resistant cultivar could potentially increase selection pressure for a race shift in the rust population (17). Therefore, rust is still one of the top five disease concerns among growers (2,12,13). However, additional research is needed to monitor for changes in the race structure of the rust pathogen. Our preliminary inoculation trials with spores from recent surveys using Maverick showed that resistance was still holding (unpublished data). Bean anthracnose has a worldwide distribution and yield losses could reach 100% under ideal weather conditions (18). Anthracnose was first reported from North Dakota in 2002 (4). Anthracnose affected approximately 5% of the fields inspected and was observed only in 2003 and 2005. The low incidence observed, less than 1% of the plants showing symptoms in affected fields, was not enough as to cause significant yield reductions. More extensive damage due to anthracnose was observed in a couple of dry bean fields in neighboring Minnesota during 2003 (personal observation). C. lindemuthianum is a highly variable pathogen and races have been described (5). Recent reports of the presence of races 73 and 1161 of C. lindemuthianum in North Dakota (3,4) warrant close monitoring of race shifts. Current commercial cultivars, especially those of pinto bean do not provide adequate resistance or tolerance to these races (3,5). Contaminated seed is one of the many ways of dissemination of this fungal pathogen (18); therefore, growers have been advised through educational programs to take extreme care when procuring certified seed material and to avoid planting recycled seed. Over the past few years, bacterial diseases have become a major concern among growers (2,13). The high prevalence and incidence of bacterial diseases, especially CBB is of great concern. In warm and humid conditions, bacterial diseases can cause devastating yield losses (10), such conditions are present in some years for a few days during the month of July in North Dakota; if such conditions would prevail for 10 days or more, the impact of CBB could be catastrophic. Nevertheless, the impact of CBB on dry bean yield needs more scrutiny under North Dakota growing conditions. Common management practices for bacterial diseases are use of pathogen-free seed, crop rotation, planting of resistant/ tolerant cultivars wherever possible, and application of copper-based fungicides. Crop rotation could be a viable option to manage bacterial diseases; in North Dakota, 76% of the growers use three-year rotations or more between dry bean crops (2). However, successful control would only be possible if crop rotation is practiced with certified pathogen-free seed. X. axonopodis pv. phaseoli, P. syringae pv. syringae, and P. syringae pv. phaseoli, the causal agents of CBB, BBS, and HB, respectively, are all known to be seedborne and seed could potentially provide the initial source of inoculum. Once

initial infection takes place within a field, these bacterial pathogens can be disseminated by rain splashing to the rest of the crop in the field. Recently, the population structure of the HB pathogen in ND was reported (14). Similar efforts are required to understand the population structure of CBB, especially now that a set of differential accessions has been proposed (16). A few cultivars are considered resistant or tolerant to HB; however, most of the available cultivars are susceptible to CBB and BBS. Additional investigations are needed to understand the increase in bacterial diseases in our region. Control of bacterial diseases with copper-based fungicides is currently under evaluation, but only for seed production purposes. From the results of these surveys, it is evident that white mold and common bacterial blight are two of the most important foliar diseases affecting dry bean production in North Dakota. The relative importance of these and other diseases detected in these surveys need to be addressed for economic impact. Economic action thresholds that could be used by growers are not available. Also, constant monitoring of changes in the dynamics of bean diseases and their causal agents are needed to help evaluate, develop, and prioritize continuing research needs. Additionally, prolonged increase of a particular disease would suggest shifts in the biology or fitness of a pathogen or the development of aggressiveness or a new race of a pathogen. Further understanding of the relationship between weather and diseases can help in devising disease forecasting systems and management practices. Acknowledgments This work was supported partially through funding by the USDA-ARS National Sclerotinia Initiative and Northarvest Bean Growers Association. Literature Cited 1. Abawi, G. S., and Grogan, R. G. 1979. Epidemiology of diseases caused by Sclerotinia sclerotiorum. Phytopathology 69:899-904. 2. Berglund, D. R. 2004. North Dakota Dry Bean Performance Testing 2003. N. Dak. State Univ. Ext. Rep. No. 654. 3. del Río, L. E., and Lamppa, R. S. 2004. Identification of a possible new anthracnose race of dry beans. (Abstr.) Phytopathology 94:S25. 4. del Río, L. E., Lamppa, R. S., and Gross, P. L. 2002. First report of dry bean anthracnose (Colletotrichum lindemuthianum) race 73 in North Dakota. Plant Dis. 86:562. 5. del Río, L. E., Lamppa, R. S., and Gross, P. L. 2003. Characterization of the reaction of North Dakota dry bean cultivars to three races of Colletotrichum lindemuthianum. Plant Dis. 87:263-265. 6. del Río, L. E, Venette, J. R., and Lamey, H. A. 2004. Impact of white mold incidence on dry bean yield under non-irrigated conditions. Plant Dis. 88:1352-1356. 7. Grafton, K. F., Venette, J. R., and Chang, K. C. 1997. Registration of "Maverick" pinto bean. Crop Sci. 37:1672. 8. Gross, P. L., and Venette, J. R. 2001. Over winter survival of bean rust urediospores in North Dakota. Plant Dis. 85:226-227. 9. Gross, P. L., and Venette, J. R. 2002. Bean rust races in North Dakota. Ann. Rept. Bean Improv. Coop. 45:106-107. 10. Ishimaru, C., Mohan, S. K., and Franc, G. D. 2005. Diseases caused by bacteria. Pages 25-27 in: Compendium of Bean Diseases, 2nd Ed. H. F. Schwartz, J. R. Steadman, R. Hall, and R. L. Foster, eds. The American Phytopathological Society, St. Paul, MN. 11. Jackson, L. E., and Moser, P. E. 1994. Development of a medium for isolation and differentiation of three bacterial plant pathogens. Ann. Rept. Bean Improv. Coop. 37:23-24. 12. Lamey, H. A., Zollinger. R, K., McMullen, M. P., Luecke, J. L., Venette, J. R., Berglund, D. D., Grafton, K. F., and Glogoza, P. A. 2000. 1999 dry bean grower survey of pest problems and pesticide use in Minnesota and North Dakota. N. Dak. State Univ. Ext. Rep. No. 64. 13. Lamey, H. A., Zollinger, R. K., Luecke, J. L., Venette, J. R., Berglund, D. R., Glogoza, A., and Grafton, K. F. 2001. 2000 dry bean grower survey of pest problems and pesticide use in Minnesota and North Dakota. N. Dak. State Univ. Ext. Rep. No. 72.

14. Lamppa, R. S., Gross, P. L., and del Río, L. E. 2002. Races of Pseudomonas syringae pv. phaseolicola in North Dakota. Ann. Rept. Bean Improv. Coop. 45:72-73. 15. North Dakota Agricultural Statistical Service. 2004. North Dakota Agricultural Statistics 2004. Report No. 73:107-112. 16. Opio, A. F., Allen, D. J., and Teri, J. M. 1996. Pathogenic variation in Xanthomonas axonopodis pv. phaseoli, the causal agent of common bacterial blight in Phaseolus beans. Plant Pathol. 45:1126-113. 17. Pastor-Corrales, M. A. 2001. The reaction of 19 bean rust differential cultivars to 94 races of Uromyces appendiculatus and the implication for the development of rust resistance cultivars. Ann. Rept. Bean Improv. Coop. 44:103-106. 18. Pastor-Corrales, M. A. 2005. Anthracnose. Pages 16-17 in: Compendium of Bean Diseases, 2nd Ed. H. F. Schwartz, J. R. Steadman, R. Hall, and R. L. Foster, ed. The American Phytopathological Society, St. Paul, MN. 19. Schwartz, H. F., Steadman, J. R., Hall, R., and Foster, R., eds. 2005. Compendium of Bean Diseases, 2nd Ed. The American Phytopathological Society, St. Paul, MN.