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2011 Plant Management Network.
Accepted for publication 18 November 2011. Published 27 December 2011.


Survey of Fungal, Nematode and Virus Diseases of Soybean in Alabama


Edward J. Sikora, Professor, Department of Entomology and Plant Pathology, John F. Murphy, Professor, Department of Entomology and Plant Pathology, Kathy S. Lawrence, Associate Professor, Department of Entomology and Plant Pathology, and Jacqueline M. Mullen, former Extension Plant Pathology Specialist, Department of Entomology and Plant Pathology, Auburn University, AL 36849-5624


Corresponding author: Edward J. Sikora. sikorej@auburn.edu


Sikora, E. J., Murphy, J. F., Lawrence, K. S., and Mullen, J. M. 2011. Survey of fungal, nematode and viral diseases of soybean in Alabama. Online. Plant Health Progress doi:10.1094/PHP-2011-1227-01-RS.


Abstract

Observations on incidence of foliar diseases, plant viruses, and plant-parasitic nematodes were collected from soybean fields in Alabama from 2008-2010. Cercospora leaf blight (Cercospora kikuchii), downy mildew (Peronospora manshurica), and target spot (Corynespora cassiicola) were the most common foliar diseases observed in the study. Cercospora leaf blight was found in 45% (2008), 77% (2009), and 70% (2010) of the fields surveyed. Downy mildew was observed in 72% (2008), 38% (2009), and 29% (2010) and target spot was detected in 45% (2008 and 2009) and 29% (2010) of the fields in the study. Soybean rust (Phakopsora pachyrhizi) was found in 43% of the fields surveyed in 2009 but was only found in one field in 2008 and was not detected in 2010. Bean pod mottle virus was detected at relatively high levels in all three years, whereas Soybean mosaic virus occurrence was less consistent and of lower incidence. Tomato spotted wilt virus was detected for the first time on soybean in Alabama. Reniform (Rotylenchulus reniformis), soybean cyst (Heterodera glycines), root-knot (Meloidogyne spp.), and lesion nematodes (Pratylenchus spp.) were the most common plant-parasitic nematodes collected with reniform nematodes found in over 30% of the fields surveyed. Soybean cyst nematode races 2, 4, 5, 6, and 14 were identified among the field population collected. The survey has increased disease awareness among growers and has aided in directing research efforts in the state.


Introduction

Soybean acreage in Alabama has more than doubled since 2007 with the total acreage planted averaging 383,000 during the period from 2008-2010 (1). In 2010, the value of the crop was estimated at over $100 million. Grower interest in planting soybeans was spurred on by an increase in soybean prices which started in 2005 and has continued through 2011 (1).

In 2005 soybean rust (SBR), caused by the fungus Phakopsora pachyrhizi, emerged as a threat to the soybean industry in the United States (33). In response to this threat, a national SBR monitoring program was implemented that included Alabama (29). While monitoring fields for SBR it became apparent that soybeans were affected by multiple plant diseases with some such as target spot (Corynespora cassiicola), SBR, and Bean pod mottle virus (BPMV) only recently reported in Alabama (15,19,35).

Surveys for specific pest groups such as nematodes on cotton (5) and golf course putting greens (32), and plant viruses in potato, tomato, watermelon, and wheat (4,20,21,31) have been undertaken previously in Alabama. This study, however, is the first comprehensive survey of multiple plant diseases of a single crop in the state. We anticipate the results from this survey will benefit the soybean industry in Alabama by increasing grower awareness of plant diseases and guiding the development of future research efforts on disease management on soybeans.


Observational Methods and Sampling Protocols

Observations on incidence and severity of various foliar diseases and plant-parasitic nematodes were collected from over 40 commercial soybean fields in 2008 and 2009 and from 20 fields in 2010. One to four fields were surveyed in each of 14 counties in 2008, 15 counties in 2009, and 10 counties in 2010. Fields were mostly concentrated in counties where soybeans are commonly grown and individual fields were never surveyed more than once during the three-year study. Fields ranged in size from two to over 500 acres and had not been sprayed with a fungicide prior to making observations. The fields surveyed were at the R5 (beginning seed development) to R6 (full seed) growth stage and observations were made during a single visit during September. For sampling purposes, a one-acre square section of each field was used for making visual observations and for collection of leaf samples for virus tests and soil samples for the presence of nematodes. One edge of each section used for sampling was adjacent to a field-road. To maintain consistency, the first author made all visual observations, selected all leaf samples for virus testing, and collected the majority of soil samples for nematode analysis. Foliar diseases were identified in the field by visual symptoms as described in the Compendium of Soybean Diseases (8). In some cases plant samples were taken to the laboratory and pathogens were confirmed using a dissecting and/or compound microscope.

Disease severity ratings for foliar diseases were made on groups of soybean plants at 20 sites within each field section. For each fungal disease identified, a severity rating was assigned based on the average percentage of foliage expressing symptoms among the 20 sites. Severity ratings ranged from: trace = less than 1% disease; low = 1 to 5%; moderate = 6 to 15%; and high = 15 to 35%. For root or stem diseases such as charcoal rot (Macrophomina phaseolina) and stem canker (Diaporthe phaseolorum var. meridionalis), disease incidence was estimated as a percentage of individual plants expressing symptoms of a disease within the field section.

For nematode sampling, a soil sample was collected by taking 25 soil cores from multiple locations within a field following a zig-zag sampling pattern. Soil cores were 6 to 8 inches deep and taken through the soybean plant’s root zone with a 1-inch-diameter soil probe. Soil cores were combined in a plastic bag, stored in a cooler and transported to Auburn University for processing. Soil samples were thoroughly mixed and a 150-cm³ sub-sample was extracted for analysis of plant-parasitic nematodes. The nematodes were separated from the soil by gravity sieving (10). Cysts of soybean cyst nematode (SCN, Heterodera glycines) were separated by a 250-µm mesh sieve. Juveniles were accumulated on a 45-µm sieve and processed by modified sucrose centrifugation (10). The resulting juvenile and cyst samples were enumerated using an inverted Nikon TSX 100 microscope at 60× and a Nikon SMZ800 stereo zoom microscope at 20× magnification. The race of each SCN population was determined in greenhouse evaluations following the guidelines of Riggs and Schmitt (26). These guidelines were used instead of HG-typing (22) so that results would be comparable to a past report on the occurrence of SCN races in Alabama (6).

Leaf samples to be assayed for plant viruses were collected from 40 soybean fields in 2008 and 2009, and from 20 fields in 2010. Because of an unforeseen problem during storage that could affect the reliability of our results with specific leaf samples in 2008 and 2010, we decided that only 19 samples that were properly stored would be assayed for viruses in those years. A total of 50 trifoliate leaves were collected from 10 sites (five leaves/site) from each field. Leaves were placed into plastic bags, stored in a cooler, and transported to the laboratory for processing. Leaf samples were assayed for BPMV, Soybean mosaic virus (SMV), and Tomato spotted wilt virus (TSWV) in all three years of the study. Leaves were also assayed for Soybean dwarf virus (SbDV) in 2008. The central leaflet of the trifoliate leaf sample was tested for each virus using a commercial enzyme-linked immunosorbent assay (ELISA) kit specific for each virus (Agdia Inc., Elkhart, IN). A sample was considered positive for the presence of virus if the ELISA absorbance value at 405 nm was greater than the healthy control threshold. The healthy control threshold was determined from the average ELISA absorbance value plus three standard deviations of three healthy soybean leaf samples added to each microtiter plate.


Cercospora Leaf Blight, Downy Mildew, and Target Spot Most Common Foliar Diseases

Cercospora leaf blight (Cercospora kikuchii), downy mildew (Peronospora manshurica), and target spot were the most common foliar diseases observed in all three years of the study (Figs. 1, 2, and 3). Cercospora leaf blight was found in 45% (2008), 77% (2009), and 70% (2010) of the fields surveyed. Downy mildew was observed in 72% (2008), 38% (2009), and 29% (2010) of the fields surveyed and target spot was detected in 45% (2008 and 2009) and 29% (2010) of the fields included in the study.


 

Fig. 1. Purple leaf discoloration caused by Cercospora blight.

 

Fig. 2. Yellow lesions on upper leaf surface caused by downy mildew.


 

Fig. 3. Target spot lesions surrounded by a slight yellow halo on soybean.

 

Weather Conditions Promote Development of Soybean Rust and Aerial Blight

Prevailing weather conditions in Alabama increased incidence of select foliar diseases in 2009 and 2010. For example, in 2009 SBR was found in 43% of the fields surveyed with severity in the moderate-to-high range in nearly 50% of the fields where it was observed. By comparison, SBR was only found in one field in 2008 and was not detected in 2010. Above average rainfall from early August through the end of the cropping season in 2009 favored the development and spread of SBR throughout Alabama. In fact, Alabama was the first state to detect SBR in every county within its border when it was confirmed in all 67 counties in 2009 as part of the National Soybean Rust Monitoring Program (28).

Aerial blight, caused by the fungus Rhizoctonia solani, was not detected in 2008 or 2009 but was found in 53% of the fields surveyed in 2010, typically at trace-to low levels. The disease was favored by periods of prolonged humidity and warm temperatures that occurred during flowering for many commercial fields in 2010 (2). Further progress of the disease was inhibited during an abnormally dry period from mid August through September of 2010.

Frog-eye leaf spot (Cercospora sojina), brown spot (Septoria glycines), powdery mildew (Microsphaera diffusa), and bacterial pustule (Xanthomonas axonopodis pv. glycines) were observed during the study but were never detected in more than 3% of the fields in a given year. Stem canker was observed in 23% of the fields surveyed in 2009 with incidence in individual fields typically between 5 to 10%; incidence of 35% was recorded in two fields in Escambia Co. in southwest Alabama. Stem canker was not observed in 2008 or 2010. Charcoal rot was observed in each year of the study but incidence did not exceed 5%. Pod and stem diseases such as anthracnose (Colletotrichum truncatum) and pod and stem blight (Diaporther phaseolorum var. sojae) are relatively common in Alabama but symptoms usually become more apparent in late reproductive stages of plant growth beyond the period when observations were taken in this study (16,17).


Reniform Nematodes Most Common

Nematodes such as SCN, root-knot (Meloidogyne spp.), and reniform (Rotylenchulus reniformis) have been identified previously in soybean fields in Alabama, but a survey of their prevalence on this crop had not been undertaken. The nematode portion of the survey was conducted in 2008 and 2009 as extremely dry soil conditions in September and October of 2010 prevented collection of adequate soil samples for nematode assays that year.

Reniform nematodes were found in 30% or more of the fields surveyed in both 2008 and 2009, making it the most common plant-parasitic nematode detected (Fig. 4). SCN, root-knot nematode (RKN) and lesion nematode (Pratylenchus spp.) were detected in 11 to 13% of the fields in 2008 and in 8 to 20% of the fields in 2009. There was no discernible pattern to where the various genera were detected in the state. The majority of the fields used for the survey had a relatively long history of row crop production that may have included cotton, soybeans and corn. Populations of juveniles extracted in 150 cc of soil from infested fields ranged from 77 to 16,223 for reniform; 172 to 1155 for RKN; 77 to 462 for SCN; and 77 to 693 for lesion. We did not determine the species of RKN or lesion nematodes collected, but populations of SCN were classified to race based on greenhouse evaluations.


 

Fig. 4. Percentage of soybean fields with reniform (RR), soybean cyst (SCN), root-knot (RKN), or lesion nematodes (LES) in 2008 and 2009.

 

Five SCN Races Edentified in Alabama

Field populations of SCN are characterized as races 1 through 16 (26). SCN races 2, 4, 5, 6, and 14 were identified among the 11 field populations collected during the survey. Race 2 was found in one field in Cherokee and Etowah counties in the northeast region in the state. Race 4 was identified in three counties including Baldwin Co. in the southwest region, Jackson Co. in the northeast corner, and Talladega Co. which is centrally located in the state. Race 5 was found in four fields in counties located in the southwest (Baldwin) or southeast (Geneva and Coffee) regions of the state. Race 6 was found in one field in Jackson Co. in the northeast corner of the state and race 14 was detected in Washington Co. in the southwest region of Alabama.


BPMV Common in Soybeans in Alabama

BPMV was detected in 11 of 19 fields (58%), and in six of nine counties surveyed in 2008 with incidence ranging from 2 to 52%. In 2009, BPMV was detected in 26 of 40 fields (65%), and in 16 of the 21 counties surveyed with incidence ranging from 2 to 54%. In 2010, the virus was detected in 5 of 19 fields (26%), and in three of the 10 counties surveyed with incidence ranging from 3 to 100%. BPMV appeared to be widespread in the state in 2009, although incidence of the virus was higher in sections of west-central and north-central Alabama, areas that have had a continuous history of soybean production over the last 20 years.

SMV was not detected in 2008 and was found in only two fields in 2010 with incidence ranging from 11 to 19%. In 2009, the virus was detected in 19 of 40 fields (48%), and in 13 of the 21 counties surveyed with incidence ranging from 2 to 88%. SMV incidence greater than 80% was observed in individual fields in Baldwin and Marengo counties, located in the southwestern and west-central regions of the state, respectively.

TSWV was detected in 26% of the 19 fields and three of the nine counties surveyed in 2008 with incidence ranging from 4 to 12%. This is the first report of TSWV on soybeans in Alabama and only the third state to report the disease on soybeans in the United States (11,23). TSWV was detected in 13% of the 40 fields surveyed in 2009, but in only four of the 21 counties with incidence ranging from 6 to 11%. The virus was not detected in the 19 fields (10 counties) surveyed in 2010. In all, TSWV was detected in only seven counties during this three-year study and these included Baldwin and Washington counties in the southwestern portion of the state; Dallas, Elmore, and Marengo counties in the central/west-central sections of Alabama; and Limestone Co. located on the Tennessee border, indicating that the virus was not localized in any particular region. In 2008, leaves were assayed for SbDV but the virus was not detected. Soybean plants were not tested for SbDV infection in 2009 and 2010.


Growers Can’t Target One Disease

Results from the three-year survey show that soybeans grown in Alabama can be exposed to multiple pathogens in any given year. The extent of losses depends on the pathogen and weather conditions, the developmental stage and health of the plants when infection occurs, the severity of the disease on individual plants, and the number of plants affected (36). Soybean yield losses in Alabama due to disease were estimated at 9.8% in 2008, 10% in 2009, and 8.5% in 2010 (12,13,14).

The potential damage from SBR and aerial blight when weather conditions favor their development suggest that a well-timed fungicide application could be economical for foliar disease management in some years in Alabama. Other late season diseases such as pod and stem blight and frog-eye leaf spot can also be controlled through an effective fungicide program (27). Factors such as recent weather conditions, cost of available fungicides, an estimate of a crop’s yield potential, the current price of soybeans, and, in some years, the proximity of a field to sources of SBR inoculum should be considered when choosing a fungicide program (30).

Plant-parasitic nematodes can have a significant impact on soybean yields depending on the nematode species and their numbers in the soil relative to the age and condition of the plants and the environmental stresses involved (24). All these factors are important and should be considered in determining whether nematodes are causing economic injury to a crop. Growers should sample fields for nematodes periodically to determine if species of nematodes are present that pose a risk to the crop.


Economics Shift Cotton Acreage to Soybean

As recently as 2003, it was estimated that more than 90% of cotton grown in the state was monocultured which favored the build-up of nematodes (5). The relatively high incidence of reniform nematode was likely due to growers planting soybean in land previously planted to cotton. This may have been due to an increase in the price of soybeans, and a decrease in the price of cotton in the years prior to and during this study (1). A survey of plant-parasitic nematodes associated with cotton conducted in Alabama from 1998-2000 revealed that reniform nematodes were found in 46% of the fields sampled (5). Soybean acreage planted in Alabama nearly doubled from 2008 through 2010 while cotton acreage dropped to an average of 294,000 acres during the same period; down from an average 570,000 acres from 2000-2006 (1).


Soybean Cyst Nematode Management

SCN causes greater yield losses than any other pathogen of soybean in the United States (25). The identification of races 2, 4, 5, 6, and 14 in this study marked the first time these races have been reported in Alabama. A previous report from 1980 suggested race 3 and possibly race 4 were of the most concern to Alabama growers (6). SCN can be managed by following a crop rotation system. In fields with moderate to high populations, following a 3- or 4-year rotation using SCN-resistant varieties and non-host crops such as corn and cotton is often recommended (34). At the end of this period, a nematode analysis of the field population should be conducted and if the SCN population is relatively low, then a SCN-susceptible variety can be planted (34). Growers need to take into account the presence of other plant-parasitic nematodes when developing a crop rotation scheme for SCN.


BPMV is Relatively Common in Alabama

BPMV was first reported in Alabama in 2004, although it likely occurred previously in the state (35). The relatively high incidence of BPMV throughout the study and the presence of various leaf-feeding beetles that are known to vector the virus, such as bean leaf beetles (Cerotoma trifurcata), suggest that Bean pod mottle will be a recurring problem for soybean producers in Alabama. We are currently evaluating the effects of time of infection by BPMV on crop development.

The high levels of SMV in 2009 suggest Soybean mosaic may be more of a sporadic problem. Since soybean aphids (Aphis glycines) have only recently been detected in the state and at relatively low levels (Charles Ray, personal communication), it is likely that SMV was introduced via infected seed. Infected seed is considered to be the primary source of inoculum for SMV with secondary and long-distance spread occurring by viruliferous aphids (9).

Alabama is the third state to report detection of TSWV in soybean in the United States, joining Georgia and Tennessee (11,23). TSWV is a common problem on other crops in the state such as peanuts and tomato (7,31). Tobacco thrips (Frankliniella fusca), an efficient vector of TSWV (18), was reported to be the most abundant thrips species in Alabama (3). Soybean thrips (Sericopthrips variablis), western flower thrips (Frankliniella occidententalis), and flower thrips (Frankliniella tritici) have also been reported in Alabama (3).

This survey of plant diseases of soybean in Alabama was successful in identification of numerous fungal, nematode and virus diseases that pose a threat to the soybean industry. Results were shared with soybean growers making them aware of diseases such as target spot, Bean pod mottle virus, and reniform nematodes; diseases that they may have overlooked previously. The survey has also stimulated research efforts on the effects of these diseases on soybean production in Alabama.


Acknowledgments

The authors dedicate this paper to the memory of Dr. Jacqueline M. Mullen, a good friend and colleague who will be missed.


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