Abstract
Bacterial leaf spot (BLS) has emerged in the last few decades as an economically important disease of both table beet (Beta vulgaris ssp. vulgaris) and Swiss chard (Beta vulgaris ssp. cicla). BLS is caused by Pseudomonas syringae pv. aptata, which is spread readily on infected seeds. Symptoms appear as circular to irregular shaped, with a tan to dark brown center and a very dark border. Disease incidence and severity is dependent on cool, humid conditions and can vary widely year to year depending on the environment. Both the vegetative and reproductive phases of these biennial crops are susceptible to the pathogen. Table beet and Swiss chard commercial cultivars (n = 21), table beet breeding lines (n = 5), and table beet plant introductions (PIs) (n = 26) were screened for response to spray inoculation with P. syringae pv. aptata in a controlled greenhouse setting. Plants were rated for severity of symptoms using percent of the area of each pair of leaves (leaf set) with symptoms and an overall plant score assigned based on the scores for each leaf pair. Accessions varied in BLS susceptibility. PI accessions were most variable, with the area under the disease progress curve (AUDPC) ranging from 1.33 to 8.75. Highly significant differences among PIs were detected for disease scores in the vegetative stage, beginning 21 days after inoculation. Screens during the reproductive growth stage showed the least variation in AUDPC among PIs. Although cultivars varied less than PIs, good BLS resistance (low disease scores) was noted for ‘Touchstone Gold’, ‘Kestrel’, ‘Bull’s Blood’, ‘Rainbow’ chard, as well as PIs 222234 and NSL 28026. Accessions W451C, Red Cloud, Detroit Dark Red, and NSL 28020 were highly susceptible. There was no consistent association between disease score in the vegetative and reproductive phases, suggesting that breeders may need to screen for BLS in both phases of the biennial life cycle. The more resistant PIs or cultivars identified in this study can be used in future efforts to breed for host resistance to BLS and to establish mapping populations to better understand the genetic control of resistance, to aid in breeding efforts.
Table beet (Beta vulgaris ssp. vulgaris) and Swiss chard (Beta vulgaris ssp. cicla) are specialty crops grown for fresh markets, processing, and baby leaf salad greens. Wisconsin and New York are the leading producers of table beet in the United States with 1650 ha and 1280 ha harvested, respectively, in 2017 [U.S. Department of Agriculture (USDA), 2019]. The table beet industry currently is experiencing growth, particularly in New York, in large part due to increased recognition and interest in the health benefits of consuming beets (Pethybridge et al., 2018).
Table beet production quality and yield can be affected by a wide variety of pathogens at several stages, both pre- and postharvest (Pethybridge et al., 2018). According to Pethybridge et al. (2018), an important factor in table beet quality and yield is foliar health. Foliar health is key for optimal photosynthesis, but also because beets grown for the foliage, such as baby leaf crops, must have disease severity below 5% to satisfy producers because of the difficulty of sorting symptomatic leaves (Pethybridge et al., 2018). Similarly stringent requirements may be found for Swiss chard production. Additionally, table beets are often harvested by top-pulling machinery (Pethybridge et al., 2017, 2020). If greens are too damaged by disease, the tops will be pulled off the roots so that the roots will not be harvested, leading to direct losses for growers (Pethybridge et al., 2017, 2020).
In recent decades, a foliar disease known as bacterial leaf spot (BLS) has increased in severity across the United States, leading to increased pressure on table beet and Swiss chard seed and vegetable producers to maintain foliar health. BLS was first found in sugar beet crops in Utah and California in the first decade of the 20th century and again in California in 1913 (Brown and Jamieson, 1913). This was followed by documentation of the disease in sugar beet crops in the Pacific Northwest (Oregon and Northern California) in 1944 (Carsner, 1944). More recently, BLS has been reported on sugar beet in Georgia in 2012 (Dutta et al., 2014) and in Oregon in 2015 (Arabiat et al., 2016). The disease was first reported in Swiss chard in California between 1999 and 2003 (Koike et al., 2003). BLS is continuing to spread to new geographic locations, with a recent report in Arizona in 2019 (Nampijja et al., 2021). The first report in table beet in Ohio was in 2017 (Rotondo et al., 2020), although BLS had been documented in table beet and Swiss chard seed crops in the Pacific Northwest for several years prior (Derie et al., 2016; Safni et al., 2016). Jacobsen (2009) noted that BLS has been observed on sugar beet and table beet in most production areas of the United States as well as in Japan, western European countries, Australia, New Zealand, and Russia; and in Swiss chard crops in the United States as well as European countries, Asia, and Australia. There are currently no reports of resistance to BLS in either table beet or Swiss chard in either the vegetative or reproductive phases of their life cycle.
Symptoms of BLS include lesions, each with a tan to brown centers surrounded by a dark border, that are circular to irregular in shape (Khan et al., 2018; Nikolić et al., 2018). Bacteria enter leaves through stomata, hydathodes, or injuries caused by insects, wind, hail, or mechanical damage, and thus, lesions can occur both along the leaf margin and across the leaf blade (Khan et al., 2018; Lamichhane et al., 2015). As the disease progresses, lesions merge to form large necrotic regions, and the leaf can become deformed (Khan et al., 2018; Nikolić et al., 2018).
BLS is caused by the pathogen Pseudomonas syringae pv. aptata (PSA). Pseudomonas syringae is a bacterial species complex that includes strains of pathogens that affect most economically important crops, including monocots and herbaceous and woody dicots (Lamichhane et al., 2015). The P. syringae species complex comprises seven phylogroups that can be differentiated by multilocus sequence analysis or whole genome sequence analysis (Gomila et al., 2017). Pathovars are determined by host range and virulence (Baltrus et al., 2017). PSA belongs to phylogroup 2 and is pathogenic on cucurbits, such as watermelon as well as members of Amaranthaceae, such as table beet and Swiss chard (Nikolić et al., 2018).
PSA can affect table beet and Swiss chard throughout the crops’ biennial lifecycle, including seedlings, mature plants during vegetative growth, and flowering plants during reproductive growth (Jacobsen, 2009). However, in the vegetative phase, symptoms are typically most severe early in growth or at up to eight sets of true leaves (Pethybridge et al., 2018). During the second year of growth, symptoms can occur throughout the season from early on, when the foliage forms a compact rosette, through the end of the season when seeds are drying in the field. It is unknown whether infection timing affects seed infection incidence, although seed infection potentially has large negative impacts on the ability to sell seed in addition to the cost of treating seed. The BLS pathogen can be seedborne, and infected seeds are one of the main ways this pathogen is spread (Ark and Leach, 1946; Gitaitis and Walcott, 2008; Lamichhane et al., 2015). Infected seeds can disseminate this pathogen across large geographic distances and are likely the main method that BLS is spread to new locations (Gitaitis and Walcott, 2008). The differences in cultivation time between vegetable and seed crops, combined with physiological differences in the plants between the first and second years of growth, have potentially large implications for breeding programs (Grahn et al., 2015).
Current BLS management strategies include preventative applications of copper treatments, removal of crop residue, drip irrigation to prevent splashing of the pathogen on leaves, and crop rotation (Lamichhane et al., 2015; Pethybridge et al., 2018). Crop rotation is a limited strategy due to the number of host plant species that PSA can both infect and survive on epiphytically (Lamichhane et al., 2015; Morris et al., 2013; Pethybridge et al., 2018; Riffaud and Morris, 2002). Postharvest seed treatment is another disease management option that can be effective for those seedborne bacterial pathogens that colonize the seedcoat rather than the endosperm, such as PSA (Singh and Mathur, 2004). However, seed treatment is expensive, and therefore, it is preferable to produce clean seed. In addition, table beet and Swiss chard seed is often decorticated mechanically before sale (Peck et al., 1967). Decortication has been shown to reduce the inoculum load of some seedborne pathogens of beet and chard without adverse effects on germination (Peck et al., 1967; Singh and Mathur, 2004).
Depending on the environmental conditions of a particular growing season, BLS outbreaks can be severe and cause economic losses. BLS thrives in wet and cool conditions ranging from 10 to 25 °C (Jacobsen, 2009; Pethybridge et al., 2018). When conditions are conducive, disease incidence and severity can be high. For example, in New York in 2017, when conditions were especially wet, the severity of BLS in-table beet fields surveyed in which the disease was observed was 75%, whereas the average incidence of BLS in these individual infected fields was 80% (S. Pethybridge, Cornell University, personal communication). Similar patterns have been observed in Washington State, with up to 50% incidence and up to 75% severity observed in some table beet seed crops in 2020, when conditions were cool and wet. However, in 2015, one of the hottest and driest years on record for western Washington State, there was no BLS observed in any of a dozen table beet and Swiss chard seed crops surveyed (L. du Toit, Washington State University, personal communication). Similar results were noted during the hot and dry 2021 season in western Washington, when temperatures reached ∼40 °C (L. du Toit, Washington State University, personal communication). In baby leaf production, whole crops can be lost due to incidences of disease as low as 5% because of the difficulty of sorting symptomatic leaves after harvest. For fresh market root or bunching crops, some growers lose whole crops when disease intensity is high.
As weather conditions change in beet and chard growing areas, BLS impacts have the potential to increase. In the midwestern and northeastern United States, predicted increases in precipitation, particularly in winter and spring, may provide the cool, wet conditions in the beginning of the growing season under which P. syringae thrives. Such conditions may also increase the chance of splash dispersal within fields (Pryor et al., 2014; Xin et al., 2018). The opposite rainfall patterns are predicted in the Pacific Northwest and southwestern United States (Gonzalez et al., 2018; May et al., 2018). However, with drier conditions expected in these areas, there will be greater need for irrigation. Overhead irrigation increases the risk of splash dispersal of this pathogen (Jacobsen, 2009). In baby leaf production, planting densities are very high (∼8 to 9 million seed/ha), and therefore, splash dispersal can be detrimental. A study by Derie et al. (2016) demonstrated that less than 10 CFU/g seed is enough for seed transmission of BLS under overhead irrigation in baby leaf production in western Washington State. Seed transmission at that low level of seed infection was sufficient to render the leaves unmarketable when conditions were wet and cool (Derie et al., 2016).
Difficulties can arise when screening for differences among accessions in a field setting. For example, reports of BLS from field surveys suggest there are usually “hot spots” of disease resulting from natural infection, meaning not all areas are affected equally (L. du Toit, Washington State University, personal communication). A greenhouse setting allows for better control over environmental conditions, including temperature, humidity, and soil moisture (Wintermantel and Kaffka, 2006). In addition, many studies in sugar beets have demonstrated consistency between greenhouse screens and field trials for ranking of accessions between the two experimental settings for several types of fungal diseases, including black root rot and pocket rot pathogens, as well as viral diseases such as curly top (Okazaki et al., 2005; Scholten et al., 2001; Wintermantel and Kaffka, 2006).
Despite the potential impact BLS could have on table beet and Swiss chard production, at present, there are few highly effective control strategies and no known genetic resistance to this pathogen. On the basis of reports from growers, field sampling, and known variation among germplasm accessions to other beet pathogens, we hypothesized that susceptibility to BLS differs among B. vulgaris accessions. Therefore, the goal of this study was to evaluate vegetable-type B. vulgaris accessions, designated as plant introductions (PIs), from the USDA National Plant Germplasm System, publicly available inbred lines from the University of Wisconsin–Madison table beet breeding program, and commercial cultivars of both table beet and Swiss chard for their responses to PSA in a controlled greenhouse setting to measure responses to inoculation in both the vegetative and reproductive growth stages.
Methods
Vegetative evaluations.
In the spring and summer of 2021, three experiments were conducted to measure disease severity of different Beta vulgaris accessions when exposed to PSA during vegetative growth. These are hereafter called experimental repeats. A total of 13 commonly grown table beet cultivars, five widely used table beet breeding lines from the University of Wisconsin–Madison table beet breeding program, seven commonly grown Swiss chard cultivars, and 27 PIs were evaluated (Table 1).
Accessions and sources for study of reaction of Beta vulgaris materials in response to inoculation with P. syringae.
PIs were evaluated in a group that is referred to hereafter as the PI screen. Commercial cultivars and breeding lines were split into two groups that are called the commercial screens. Although all cultivars and breeding lines were originally screened together, lesions had a different physical appearance on leaves with lighter colored foliage compared with leaves with dark colored foliage. The appearance of symptoms on cultivars and breeding lines with light-colored foliage was not always consistent with the description of lesions having tan to brown centers surrounded by a dark border. In some accessions, such as ‘Silverado’, lesions started out tan to gray, and the dark border was absent until later in the progression of the disease (Supplemental Fig. 9). Therefore, accessions with lighter colored foliage were re-screened. Rescreening allowed for standardization of disease ratings across all accessions. The rescreening of the lighter colored accessions is referred to as the commercial screen “light-colored foliage accessions”; the screening of the darker colored accessions is referred to as the commercial screen “dark-colored foliage accessions.” The duration of these vegetative screens was ∼9 weeks from planting to final evaluation.
Accessions within each group were organized in a completely randomized design in a greenhouse at the Walnut Street Greenhouse complex in Madison, WI. Greenhouse tables were divided into 46 cm × 46 cm grids, with each grid containing one pot. Approximately five seeds were planted in a size 100 (11.75 cm height, 11 cm top diameter; Nursery Supplies Inc., Pairless Hills, PA) plastic pot in a one-to-one mix of field soil from Madison, WI, and ProMix (high porosity + bio fungicide and mycorrhizae, Premier Tech Horticulture, Québec, Canada). Once plants exhibited one true leaf, they were thinned to one plant per pot. Pots were placed in saucers, and plants were bottom watered via saucers to prevent splashing on the leaves. Day length was set at 16 h with lighting in the greenhouse, and temperatures ranged from 22 to 24 °C. For each accession, four plants were spray-inoculated with PSA and one plant served as a negative control treatment that was sprayed with sterilized Milli-Q water.
Plants were inoculated with PSA strain BP 1452 obtained from Dr. Carolee Bull of Pennsylvania State University that was isolated originally from Swiss chard in Washington State by Dr. Lindsey du Toit. BP1452 is pathogenic on both table beet and Swiss chard. The strain was grown on nutrient agar in petri dishes and incubated at 28 °C with no light for 48 h. The spray inoculation protocol was based on a modified protocol from Dr. Carolee Bull. Briefly, colonies of BP 1452 were suspended in sterilized MilliQ water at a concentration of 1 × 108 CFU/mL (optical density of 0.8 at 600 nm measured spectrophotometrically) directly before inoculation. Inoculations occurred at the two true-leaf growth stage and then again 2 weeks later. At each inoculation, each plant was sprayed with 4.7 mL of inoculum or MilliQ water. The spray was targeted at the underside of leaves on all sides of the plant. Plants were enclosed in clear plastic bags 24 h before inoculation and then rebagged for 48 h post-inoculation to increase humidity and favor infection.
Visual disease ratings were conducted four times per plant starting 1 week post-inoculation. Ratings included the percentage surface area of a pair of leaves with lesions (Table 2). The first pair of leaves was the oldest pair. This percentage was then translated into a leaf pair score that ranged from 0 to 7 (Fig. 1). This leaf pair score was then combined with the number of leaf sets that had symptoms for an overall plant score (Table 1). For example, multiple sets of leaves for one plant individually could have a score of 1, whereas the overall plant has a score of 2 because the symptoms were on multiple leaf pairs. Overall plant score ranged from 0 to 7. For example, a score of 3 means that lesions started to coalesce, and a score of 5 means that at least half of the first two pairs of leaves died, and a leaf pair had at least scores of 2 or higher.
Disease rating scale for the percentage of vegetative leaf set (pair) and the reproductive growth stage leaf with symptoms of bacterial leaf spot for Beta vulgaris subsp. cicla and Beta vulgaris subsp. vulgaris spray inoculated with Pseudomonas syringae pathovar aptata strain BP 1452. 0 = 0% diseased tissue; 1 = 1% to 10% of leaf area with disease symptoms; 2 = 10% to 25% of leaf area affected; 3 = 25% to 50% of leaf area affected; 4 = 50% to 75% of leaf area affected; 5 = 75% to 90% of leaf area affected; 6 = 90% to 99% of leaf area affected; 7 = 100% of leaf area affected/leaf is dead.
Citation: HortScience 57, 11; 10.21273/HORTSCI16777-22
Bacterial leaf spot severity rating system of Beta vulgaris subsp. cicla and Beta vulgaris subsp. vulgaris inoculated with the bacterium Pseudomonas syringae pathovar aptata.
Reproductive evaluations.
Twenty-four accessions, including seven Swiss chard commercial cultivars, 12 table beet commercial cultivars, and five table beet breeding lines, were sown by hand in the field during Summer 2020 at East Madison Agricultural Research Station in Hartland, WI. Each accession was represented by a 3.7-m-long row and was replicated four times in the field. The layout was a completely randomized design. Roots were harvested ∼12 weeks after planting. At harvest, foliage was removed from the roots, leaving ∼2 cm of meristematic tissue at the crown. Roots were then packed with woodchips inside paper bags, which were then placed inside plastic bags. The bags were then placed in a cooler at 12 °C for vernalization. After 13 weeks, roots were removed from the cooler and planted in ProMix in size 200 pots (14.8 cm height, 14 cm top diameter) (Nursery Supplies Inc., Pairless Hills, PA) at the Horticulture Research Farm greenhouses (Arlington, WI) in December. Pots were placed in saucers and plants were watered from the saucers. Day length was set at 16 h, and temperatures ranged from 22 to 24 °C. Flower stalks began to emerge in January and were in full flower by early February.
Two reproductive growth stage screens were conducted, and the duration of each screen was ∼12 weeks from planting of the root until the final evaluation. These plants were also inoculated with PSA strain BP 1452. Preparation of bacteria and greenhouse layout were as described for the vegetative experiments. Approximately 6 weeks after planting roots, and then biweekly for the next month, plants were spray-inoculated. Inoculum was prepared as described for the vegetative screens. Each plant received 10.9 mL of the BP1452 suspension or MilliQ water. Plants were enclosed in clear plastic bags 24 h before inoculation and bagged again for 48 h post-inoculation to increase humidity. Holes were cut in the tops of the bags through which the inoculum was sprayed onto all surfaces of the plant, and then these holes were later sealed.
Disease ratings were conducted starting 1 week post-inoculation and occurred for the next 5 weeks. Ratings were based on the percentage of leaf area with lesions, as described earlier, with the exception that the percentage leaf area with symptoms was determined for individual leaves rather than leaf pairs as leaf pairs were difficult to distinguish at this growth stage. Four individual leaves were chosen at random at the first rating and marked to ensure ratings of the same leaf week after week. Leaf scores for all four leaves were then averaged to give the overall plant score, which ranged from 0 to 7. A score of 0 meant that the plant was healthy (no lesions present). A score of 2 meant that the individual scores of the four leaves averaged together were a 2 or that, on average, the four leaves had 10% to 25% of their total surface area with lesions. A score of 7 translated to all four leaves being covered with lesions or dead.
After 6 weeks of ratings, plants that were producing seed continued to be watered for 8 more weeks. At this time, seeds were harvested and threshed to prepare them for seed testing. Seeds from each plant were sent to Eurofins BioDiagnostics Inc. (Longmont, CO) and tested for the presence of PSA. Seeds were sown in individual boxes. Any lesions that appeared on the seedlings were then excised, macerated, and plated onto semiselective KBBC and KBZ media. Colonies were incubated for 4 to 7 d at 27 to 30 °C. The colonies were then compared with a positive control strain of PSA based on appearance. No colonies matched the positive control. Therefore, no isolates were sequenced for confirmation.
Statistical analysis.
Data from both the vegetative and reproductive evaluations were analyzed using R version 4.1.1 (RStudio, Boston, MA). Analysis of variance (ANOVA) models for vegetative and reproductive evaluations were linear mixed models with accession and days post-inoculation as main effects, and pot number as the random effect. These linear mixed models were fit with ‘lmer’ from the “lme4” package (version 1.1–23). ANOVA was performed using the “lmerTest” package in R (version 3.1–2). When an interaction was significant between accession and days post-inoculation, results for each week were analyzed separately. In such cases, the model was a linear fixed model with the main effect of accession, and data were fit using ‘lm’ from the “stats” package (version 4.0.4).
ANOVAs were conducted with overall mean disease score from the four inoculated plants to assess differences among accessions in reaction to inoculation. ANOVAs were performed without data for the noninoculated control treatments because little disease was observed on these plants. Based on the ANOVA, all models with P values < 0.1 were analyzed with “emmeans” from the “emmeans” package (version 1.4-8) for determining differences among accessions.
Area under the disease progress curve (AUDPC) for each accession was estimated using the “agricolae” package (version 1.3-3) in R. AUDPC was used to compare accessions as a quantitative measure of disease incidence over the duration of the trial. AUDPC was analyzed as a fixed model with accession as the main effect. ANOVA of AUDPC values was performed with “aov” from the “stats” package in R (version 4.0.4). Noninoculated control treatments were excluded from the ANOVA analysis. Pairwise comparisons were made using “emmeans” at α = 0.05.
Results
The method of inoculation was verified by the presence of negative, noninoculated control plants of each accession. Although BLS was observed on some of the noninoculated plants, there were large differences in overall mean disease scores observed between inoculated and noninoculated control plants for all accessions (Supplemental Figs. 1–4), providing assurance that the inoculation technique was suitable for comparison of accessions.
Vegetative evaluations, commercial screen: dark-colored foliage accessions.
No significant interaction was found between experimental repeat and accession for disease severity ratings (P > 0.1). Therefore, data were analyzed together for both experimental repeats. Additionally, no significant interaction was found between days post-inoculation and accession for BLS severity ratings. Significant differences were not detected among accessions for overall disease ratings. Nevertheless, ‘Bull’s Blood’ consistently had one of the lowest overall disease scores over time, whereas ‘Boro’ consistently had one of the highest over time. BLS symptoms occurred on all inoculated plants in experimental repeats 1 and 2. The mean AUDPC ratings for inoculated plants ranged from 3.94 to 7.36 with an average AUDPC of 5.70 (Fig. 2). No symptoms occurred on six of 10 control plants in experimental repeat 1, and the mean AUDPC was 0.70. ANOVA revealed no effect of accession on mean AUDPC (P > 0.1), although ‘Bull’s Blood’ had the smallest AUDPC, and ‘Boro’ and ‘Detroit Dark Red’ had the largest AUDPCs (Fig. 2).
Mean area under the disease progress curve (AUDPC) of eight Beta vulgaris subsp. vulgaris commercial cultivars, one Beta vulgaris subsp. vulgaris breeding line, and one Beta vulgaris subsp. cicla commercial cultivar in response to spray inoculation with Pseudomonas syringae pathovar aptata strain BP 1452 during vegetative growth in two screening trials in a greenhouse in 2021.
Citation: HortScience 57, 11; 10.21273/HORTSCI16777-22
Commercial screen: light-colored foliage accessions.
BLS symptoms occurred on all inoculated plants in experimental repeats 1 and 2. For experimental repeat 1, the mean AUDPC rating for inoculated plants ranged from 1.62 to 8.5 with an average AUDPC of 4.92 (Figs. 3 and 4). For experimental repeat two, the mean AUDPC for inoculated plants ranged from 4.5 to 11.67 with an average AUDPC of 8.77 (Figs. 3 and 4). No symptoms occurred on 11 of 16 control plants in experimental repeat 1. The mean AUDPC was 0.66. In repeat 2, eight of 16 control plants did not have symptoms, and the mean AUDPC was 1.03.
Area under the disease progress curve (AUDPC) of six Beta vulgaris subsp. vulgaris commercial cultivars, four Beta vulgaris subsp. vulgaris breeding lines, and six Beta vulgaris subsp. cicla commercial cultivars in response to spray inoculation with Pseudomonas syringae pathovar aptata strain BP 1452 during vegetative growth in two greenhouse screening trials in 2021.
Citation: HortScience 57, 11; 10.21273/HORTSCI16777-22
Mean area under the disease progress curve (AUDPC) of six Beta vulgaris subsp. vulgaris commercial cultivars, four Beta vulgaris subsp. vulgaris breeding lines, and six Beta vulgaris subsp. cicla commercial cultivars in response to spray inoculation with Pseudomonas syringae pathovar aptata strain BP 1452 during vegetative growth in a greenhouse screen carried out twice in 2021. Bars not sharing a common letter are significantly different at P ≤ 0.05.
Citation: HortScience 57, 11; 10.21273/HORTSCI16777-22
ANOVA of disease severity ratings for the combined experimental repeat revealed a significant interaction for experimental run and accession (P < 0.01). Therefore, experimental repeats were kept separate for analysis. ANOVA for experimental repeat 1 showed a significant interaction between accession and days post-inoculation on overall mean disease score (P = 0.05), indicating that accessions did not maintain the same ranking at each rating time (Table 3). At 7 and 14 d post-inoculation, accession had no significant effect on overall mean disease score (P > 0.05) because there was inadequate disease intensity to differentiate among accessions (Table 3; Fig. 3). ANOVA of overall mean disease scores 21 d post-inoculation indicated significant differences among accessions (P < 0.05) (Table 2). ‘Blushing Not Bashful’ and ‘Touchstone Gold’ had significantly lower mean disease scores than ‘Golden Detroit’, ‘Silverado’, ‘Chioggia Guardsmark’, ‘Detroit Dark Red’, ‘Barese’, ‘Bright Lights’, ‘Rhubarb’, and W451C. The main effect of accession also was significant for overall mean disease score (P < 0.05) 28 d post-inoculation (Table 3). W452C and ‘Blushing Not Bashful’ had significantly lower mean disease scores than ‘Silverado’ and ‘Chioggia Guardsmark’. ‘Touchstone Gold’ had a significantly lower mean disease score than ‘Silverado’, ‘Chioggia Guardsmark’, ‘Golden Detroit’, W411A, ‘Bright Lights’, ‘Detroit Dark Red’, ‘Rhubarb’, W451C, ‘Barese’, and ‘Evansville Orbit’.
Analysis of variance for experimental runs 1 and 2 for average disease scores of six Beta vulgaris subsp. cicla commercial cultivars, six Beta vulgaris subsp. vulgaris commercial cultivars, and four Beta vulgaris subsp. vulgaris breeding lines in response to inoculation with Pseudomonas syrinage pathovar aptata strain BP 1452 in a greenhouse screen evaluated in 2021.
ANOVA for experimental repeat 2 also showed a significant interaction between accession and days post-inoculation on overall mean disease score (P < 0.01). Therefore, the effect of accession was analyzed for each week individually. At 7 d post-inoculation, accession had a significant effect on mean overall mean disease score (P < 0.05) because BLS developed much quicker in repeat 2 than in repeat 1 (Table 3; Fig. 3). Accessions ‘Rainbow’, ‘Touchstone Gold’, ‘Fordhook Giant’, ‘Chioggia Guardsmark’, and ‘Golden Detroit’ all had significantly lower mean overall disease ratings compared with ‘Silverado’ and W451C at this 7-day rating (Table 3). Accession also had a significant effect on the overall mean disease score 14 d post-inoculation (P < 0.05) (Table 3), when ‘Chioggia Guardsmark’ and ‘Golden Detroit’ had significantly lower mean overall disease scores than the other accessions. ANOVA of overall mean disease scores 21 or 28 d post-inoculation indicated no significant difference among accessions (Table 3; Supplemental Figs. 5–8).
ANOVA for experimental repeat one showed a significant effect of accession on mean AUDPC (P < 0.05). ‘Touchstone Gold’ had a significantly smaller AUDPC compared with ‘Silverado’, ‘Rhubarb’, ‘Chioggia Guardsmark’, ‘Bright Lights’, W451C, ‘Detroit Dark Red’, and ‘Golden Detroit’ (Fig. 4). AUDPC for experimental repeat 2 showed a significant effect of accession on mean AUDPC (P < 0.1). The mean AUDPC value for ‘Golden Detroit’ and ‘Chioggia Guardsmark’ was significantly less than the mean AUDPC for ‘Evansville Orbit’, W453B, W411A, W451C, ‘Rhubarb’, or ‘Silverado’, in contrast to results for repeat 1 of this experiment (Fig. 4, Supplemental Figs. 5–8). In both repeat 1 and repeat 2, ‘Touchstone Gold’ consistently had one of the smallest AUDPCs. W451C consistently had one of the largest AUDPCs in both repeats. ‘Rainbow’ was consistently the Swiss chard cultivar with the smallest AUDPC rating. No Swiss chard cultivar reliably had the largest AUDPC rating of the accessions evaluated in these trials.
PI screen.
BLS symptoms occurred on all inoculated plants in experimental repeats 1 and 2. For experimental repeat 1, the mean AUDPC rating for inoculated plants ranged from 1.33 to 8.75 with an average AUDPC rating of 5.35 (Figs. 5 and 6). For experimental repeat 2, the mean AUDPC for inoculated plants ranged from 1.5 to 8.75 with an average AUDPC rating of 4.37 (Figs. 5 and 6). No symptoms occurred on eight of 25 control plants in experimental repeat 1, and the mean AUDPC rating was 2.26. In repeat 2, 15 of 20 control plants did not have symptoms, and the average AUDPC rating was 0.78.
Area under the disease progress curve (AUDPC) of 26 Beta vulgaris subsp. vulgaris plant introductions (PIs) in response to spray inoculation with Pseudomonas syringae pathovar aptata strain BP 1452 during vegetative growth in two greenhouse screening carried out twice in 2021.
Citation: HortScience 57, 11; 10.21273/HORTSCI16777-22
Mean AUDPC of 26 Beta vulgaris subsp. vulgaris plant introductions (PIs) in response to spray inoculation with Pseudomonas syringae pathovar aptata strain BP 1452 during vegetative growth in a greenhouse trial carried out twice in 2021. Bars not sharing a common letter are significantly different at P ≤ 0.05.
Citation: HortScience 57, 11; 10.21273/HORTSCI16777-22
Significant interactions were found for experimental repeat and accession on BLS disease severity ratings (P < 0.001). In experimental repeat 1, plants exhibited higher overall mean disease scores than plants in experimental repeat 2. Therefore, experimental repeats were kept separate for analysis. There was no significant interaction between accession and days post-inoculation for either experimental repeat (Table 4).
Analysis of variance for experimental runs 1 and 2 for average disease scores of 26 Beta vulgaris subsp. vulgaris plant introduction in response to inoculation with Pseudomonas syringae pathovar aptata strain BP 1452 during vegetative growth in a greenhouse in 2021.
ANOVA for 7 d post-inoculation indicated that accession had no significant effect on overall mean disease score (P > 0.1) (Table 4; Supplemental Fig. 7). ANOVA at 14 d post-inoculation showed a moderately significant difference between in overall mean disease scores among the accessions (P < 0.1) (Table 4). PI 222234 and PI 174059 had a significantly smaller overall mean disease score compared with PI 164805, PI 612338, NSL 28020, PI 285591, PI 169015, PI 124528, and PI 379097. ANOVA at 21 d (P < 0.05) and 28 d (P < 0.1) post-inoculation were also significant for the effect of accession on mean disease ratings. At 21 d post-inoculation, PI 222234 and PI 174059 had significantly smaller overall mean disease scores than Ames 22163, PI 323938, NSL 28024, PI 169028, PI 612330, PI 164805, PI 285591, PI 141919, PI 169015, NSL 28020, PI 612338, PI 379097, and PI 124528. Finally, at 28 d post-inoculation, PI 222234, PI 174059, and PI 271439 had significantly smaller overall mean disease scores than PI 169015, PI 141919, NSL 28020, PI 379097, PI 612338, and PI 124528.
ANOVA for experimental repeat 2 at 7 and 14 d post-inoculation did not show a significant difference in mean disease scores due to accessions (Table 4). At 21 d post-inoculation, accessions had a significant effect on overall mean disease (P < 0.05) (Table 4). PI 193458, PI 222234, PI 109039, PI 169015, PI 269309, PI 592989, PI 612334, and PI 323938 all had significantly smaller overall mean disease scores than PI 169028, PI 271439, and PI 28020. At 21 d post-inoculation, accession again was significant for overall mean disease (P < 0.05) (Table 4). PI 109039, PI 269309, PI 592989, PI 323938, PI 612334, PI 193458, PI 222234, PI 169015, PI 141919, and PI 612340 all had significantly smaller overall mean disease scores than PI 28020, PI 169028, and PI 271439.
ANOVA for experimental repeat 1 showed a significant effect of accession on mean AUDPC ratings (P = 0.05). PI 222234 and PI 174059 had significantly smaller AUDPC ratings than PI 612330, PI 164805, NSL 28024, PI 141919, PI 285591, PI 612338, NSL 28020, PI 169015, PI 124528, and PI 379097 (Fig. 6). AUDPC rating for experimental repeat 2 showed a moderately significant effect of accession on mean AUDPC (P < 0.01). PI 193458 had a significantly smaller AUDPC rating than PI 164805, PI 271439, or NSL 28020 (Fig. 6). PI 22234 and NSL 28026 performed consistently with some of the smallest AUDPCs in both experimental repeats. NSL 28020 had one the largest AUDPC ratings in both repeats. PI 612330 and PI 612338 were consistently midrange for AUDPC ratings.
Reproductive evaluations.
Although reproductive evaluations were conducted with 24 accessions, only 10 accessions were included in the analysis because of differences between accessions with light- and dark-colored foliage. Reproductive evaluations had been completed before this recognition, thus necessitating dropping the light-colored foliage accessions from the analysis.
ANOVA of experimental repeats 1 and 2 combined did not reveal a significant interaction between experimental repeat and accession. Experimental repeat was moderately significant, however (P < 0.1), with repeat 2 generally having a higher overall mean disease score than repeat 1. As a result, repeat trial data were analyzed separately.
ANOVA for experimental repeat 1 did not reveal a significant interaction between accession and days post-inoculation (Table 5). No rating days had significant differences in overall mean disease scores as a result of accessions (Table 5). ANOVA for experimental repeat 2 indicated a significant interaction between accession and days post-inoculation (P < 0.05) (Table 5). Accessions changed rank as days post-inoculation increased. ANOVA indicated no significant differences in overall mean disease as a result of accessions, regardless of rating period (Table 5; Supplemental Fig. 8).
Analysis of variance for experimental run 1 and 2 for average disease scores of one Beta vulgaris subsp. cicla commercial cultivar, seven Beta vulgaris subsp. vulgaris commercial cultivars, and one Beta vulgaris subsp. vulgaris breeding lines in response to inoculation with Pseudomonas syringae pathovar aptata strain BP 1452 during reproductive growth in a greenhouse in 2021.
BLS symptoms occurred on all inoculated plants in experimental repeats 1 and 2. For experimental repeat 1, the mean AUDPC rating for inoculated plants ranged from 3.38 to 4.84 with an average AUDPC rating of 4.23 (Fig. 7). For experimental repeat 2, the mean AUDPC for inoculated plants ranged from 3.19 to 6.44 with an average AUDPC rating of 4.84 (Fig. 7). Overall, both repeats 1 and 2 of the reproductive evaluations had a smaller range for AUDPC ratings than the vegetative evaluations. In experimental repeat 1, all noninoculated control plants showed symptoms of disease. The mean AUDPC rating was 1.58. In repeat 2, one of nine control plants did not have symptoms, and the average AUDPC rating was 2.1.
Area under the disease progress curve (AUDPC) of eight Beta vulgaris subsp. vulgaris commercial cultivars, one Beta vulgaris subsp. vulgaris breeding line, and one Beta vulgaris subsp. cicla commercial cultivar in response to spray inoculation with Pseudomonas syringae pathovar aptata strain BP 1452 during reproductive growth in a greenhouse trial completed twice in 2021.
Citation: HortScience 57, 11; 10.21273/HORTSCI16777-22
No significant effect of accession on mean AUDPC rating was noted for experimental repeat 1 or 2 (P > 0.1). Although there were no significant differences among accessions, some patterns emerged. ‘Kestrel’ had the smallest AUDPC rating in both repeats. ‘Boro’ and W357B consistently were midrange for AUDPC. Similar to the vegetative screen, ‘Red Cloud’ consistently had one of the largest AUDPC ratings.
Seed testing for the presence of PSA did not result in positive identification of any inoculated plants despite these plants showing leaf symptoms. Overall, seed set was low compared with a typical seed production field because plants were in individual pots and widely spaced in the greenhouse. In addition, moisture and humidity may not have been optimal for the pathogen to colonize developing fruits and seeds.
Discussion
The method of inoculation and testing used in this study revealed significant differences in leaf ratings between inoculated and noninoculated control plants, suggesting this approach was valuable for evaluation of BLS in Beta vulgaris. The noninoculated control plants served as a check to indicate that symptoms were the result of inoculation with PSA (Supplemental Figs. 1–4). However, it was unknown if seed used for the vegetative and reproductive screens were clean of PSA. The negative control plants of certain accessions developed BLS lesions while others did not display symptoms. This suggests that seeds for these particular accessions may have been infected with PSA or that there may have been a low level of cross-contamination between plants over the duration of each experiment. Future experiments could either use verified clean seed or treat the seed before use in disease screens to reduce this potential effect. These disease evaluations also demonstrated that Beta vulgaris subsp. vulgaris commercial cultivars, breeding lines, and PIs as well as Beta vulgaris subsp. cicla commercial cultivars have a range of reactions to spray inoculation with PSA.
Disease screens during the vegetative growth stage of beet or chard accessions with light-colored foliage revealed significant differences among accessions in response to inoculation with PSA. The main effect of accession in experimental repeat 2 was marginally significant with a P value of 0.065; however, some individual comparisons were significant at P < 0.01. For table beets, ‘Touchstone Gold’ showed the greatest resistance based on a consistently low AUDPC in both repeats, whereas inbred line W451C consistently had one of the highest AUDPCs. In experimental repeat 1, ‘Touchstone Gold’ had a 78% smaller mean AUDPC rating than ‘Detroit Dark Red’ and a 76% smaller mean AUDPC rating than W451C. In experimental repeat 2, the differences were greatly reduced. ‘Touchstone Gold’ had a 12% smaller mean AUDPC rating than ‘Detroit Dark Red’ and a 29% smaller mean AUDPC rating than W451C.
For Swiss chard, ‘Rainbow’ consistently had the lowest mean AUDPC rating. ‘Silverado’, ‘Bright Lights’, and ‘Rhubarb’ were variable between experimental repeats but exhibited some of the highest mean AUDPC ratings. Koike et al. (2003) first reported BLS infection on commercially grown Swiss chard in California from 1999 to 2003. However, they did not indicate the cultivar(s) affected, and little work has been done since to determine which cultivars are more susceptible or if susceptibility varies among cultivars. This study demonstrates that there is variability in responses among Swiss chard cultivars.
Generally, plants in experimental repeat 2 had more severe BLS ratings compared with plants in repeat 1 for accessions with light-colored foliage. Experimental repeat 1 occurred from the end of June to the beginning of August, whereas repeat 2 occurred from the end of July to the beginning of September. Although both occurred during the summer months, it is possible that differences in environmental conditions between these time periods accounted for some of the differences. In addition, the experimental repeats took place in different greenhouses, which could have had differences in temperature and/or humidity. Finally, experimental repeat 1 of the light-colored foliage accessions was the first round of screening in which we were aware of the difference in BLS symptoms on chard vs. beet cultivars and could therefore adjust the foliar ratings for this observation.
‘Silverado’ has been known to display BLS symptoms and has been used as a susceptible cultivar in other BLS screens (L. du Toit, Washington State University, personal communication). In experimental repeat one and two, ‘Silverado’ consistently exhibited symptoms validating the methods used in these screens. ‘Detroit Dark Red’ was included as a check in the commercial screens of accessions with both dark- and light-colored foliage. In all repeats, ‘Detroit Dark Red’ had relatively consistent performance, with AUDPC scores ranking this cultivar with the most susceptible accessions.
No significant differences were observed among accessions with dark-colored foliage during either the vegetative or reproductive screens. Experimental repeat 1 of the reproductive screens had a mean AUDPC rating range of 3.38 to 4.84, and repeat 2 had a mean rating range of 3.19 to 6.44. The range of mean AUDPC ratings for the vegetative evaluation was 3.94 to 7.36. Although there were no statistical differences among accessions, some patterns emerged that could be examined in future studies. The accession with one of the largest AUDPC rating was ‘Red Cloud’. However, an unpublished study from Sarah Pethybridge (Cornell University, personal communication) showed that ‘Red Cloud’ had “moderate” BLS symptoms compared with the cultivar Pablo, which showed severe disease. One of the more resistant accessions in the reproductive evaluations was ‘Kestrel’, although statistical analysis did not separate out this cultivar from the others screened. In experimental repeat 1, ‘Kestrel’ exhibited a 27% smaller AUDPC than ‘Red Cloud’. In experimental repeat 2, ‘Kestrel’ exhibited a 50% smaller mean AUDPC rating than ‘Red Cloud’. One of the most resistant accessions in the vegetative evaluations was ‘Bull’s Blood’, which exhibited a 47% smaller mean AUDPC rating than ‘Detroit Dark Red’ and a 45% smaller mean AUDPC rating than ‘Red Cloud’.
The lack of significance among darker color accessions inoculated with PSA may have resulted from several factors. As a result of the small sample size, standard errors were relatively large. Increasing the sample size for each accession would increase the power to identify differences among accessions. Additionally, disease screens require not only a suitable host and a virulent pathogen but suitable environmental conditions. In these screens, plants were enclosed in plastic bag for 24 h pre-inoculation and 48 h post-inoculation. However, development of the pathogen would have benefitted from increased humidity for longer periods to initiate and sustain infection and disease development. Subsequent experiments could benefit from increasing humidity through the duration of disease rating. A third possibility for the lack of significant differences among accessions with dark colored foliage is the relatively limited genetic variability of table beet cultivars with red pigmented roots. Some of the F1 hybrid table beet cultivars available on the market make use of male sterile lines developed at the University of Wisconsin–Madison from the 1960s to the present. Because table beet is a relatively minor specialty crop in the United States that does not receive large amounts of breeding activity, the amount of genetic diversity among red-rooted cultivars may be limited.
The open-pollenated cultivar Ruby Queen performed consistently between reproductive experimental repeats and was in the middle of the range of mean AUDPC ratings for both reproductive and vegetative evaluations. This is in contrast to an unpublished field study from Cornell University that found that ‘Ruby Queen’ showed “low” BLS symptoms (S. Pethybridge, personal communication). Our greenhouse study also included ‘Red Cloud’, which was considered to have “moderate” disease levels in the Cornell study. The reproductive and vegetative experimental repeats were consistent, with ‘Ruby Queen’ showing fewer disease symptoms than ‘Red Cloud’. In a study by Pethybridge et al. (2017), ‘Ruby Queen’ was the least susceptible fresh market cultivar to Cercospora leaf spot (CLS), one of the most widespread and damaging foliar diseases for table beet and Swiss chard. ‘Ruby Queen performance in both CLS and BLS disease evaluations makes it a candidate for further study and breeding efforts.
In this greenhouse study, PIs showed significant differences in responses to spray inoculation with PSA, which might be expected from this more diverse collection of germplasm compared with the commercial cultivars screened. Generally, the AUDPC for PIs spiked shortly following inoculation and then leveled off or showed a gradual increase through the remaining disease evaluation periods. Although there was variability in mean AUDPC ratings between repeats 1 and 2 of the screening, PI 222234 and NSL 28026 consistently ranked among the lowest mean AUDPC ratings for the PI accessions. PI 612338 and NSL 28020 consistently ranked among the highest mean AUDPC ratings. PI 22234 had only 18% of the mean AUDPC value of NSL 28020 in experimental repeat 1 and 34% of the mean AUDPC value of NSL 28020 in experimental repeat 2. NSL 28026 had 47% of the mean AUDPC value of NSL 28020 in experimental repeat 1 and 17% of the mean AUDPC value of NSL 28020 in experimental repeat 2. PI 109039, Ames 22163, PI 269309, and PI 592989 also had relatively stable performance between both repeats with mean AUDPC ratings on the smaller end of the range.
Testing of the seed harvested from the plants in the reproductive trials in this study, using seedling grow outs by a commercial seed testing laboratory, did not identify any seed-borne PSA despite seed coming from plants with BLS lesions. During seed production in a field environment, the microclimate can be conducive to BLS due to dense canopies that increase the humidity in the canopy, and splash dispersal from rain or irrigation can easily spread the pathogen between neighboring plants. Therefore, experiments to look at seed infection should occur in a field setting more representative of production conditions. Additionally, future seed testing could entail a seed wash technique that might be more effective at detecting seedborne PSA than grow-out assays.
There was no clear correlation for BLS severity between vegetative and reproductive evaluations of beet and chard accessions in this study. Depending on which experimental repeats were compared, Pearson’s correlation coefficients ranged from almost 0 to 0.36 for all accessions and from 0.06 to 0.78 for table beet cultivars. This suggests that the correlation between vegetative and reproductive responses to spray inoculation was inconsistent. The relationship between disease reaction in vegetative and reproductive phases should be addressed in future studies with a larger sample size for each accession. The significance of this correlation is in the degree to which plant breeders might need to screen at both the vegetative and reproductive phases of growth when breeding for resistance to BLS. If subsequent experiments demonstrate a significant correlation between these two stages of the plant life cycle, it may be possible to select only in the vegetative phase, thereby saving nearly 1 year per cycle during the breeding process. If the disease responses of accessions during two stages of the life cycle are not correlated, breeders may need to screen in both stages.
PI accessions were expected to have greater variability in response to spray inoculation with PSA than commercial cultivars as PIs commonly have a broad range of variability for agronomic traits (Wigg and Goldman, 2020). The PI accessions did have the largest range of mean AUDPC ratings in both repeats; however, the range in mean AUDPC ratings for the commercial screen of light-colored foliage accessions was similar. This contrasts with findings by Wigg and Goldman (2020) for Rhizoctonia root rot of table beet, in which PIs had less variation compared with commercial cultivars when inoculated with Rhizoctonia solani. However, when looking at the accessions with light-colored foliage, inbreds had less variation than commercial cultivars. The commercial screen of accessions with light-colored foliage also showed that table beets had a greater range of mean AUDPC ratings than Swiss chard.
It should be noted that the screen of light-colored foliage accessions of commercial germplasm only included inbreds and open-pollinated cultivars. The screen for dark-colored foliage accessions of commercial germplasm included both open-pollinated and hybrid cultivars as well as one inbred. Hybrids had a slightly smaller AUDPC range, 5.00 to 7.43 compared with open-pollinated cultivars, which had a range of 3.94 to 7.93. The screening with the smallest range for AUDPC ratings in both experimental repeats were the reproductive evaluations. The reproductive evaluations included both open-pollinated and hybrid cultivars as well one as one inbred. There was no clear distinction between hybrid or open-pollinated cultivars regarding range of AUDPC ratings.
Public knowledge about the relative susceptibility of B. vulgaris cultivars or accessions to BLS has only started to emerge in recent years. This study serves to build our knowledge of how PSA effects B. vulgaris, including B. vulgaris subsp. vulgaris commercial cultivars, breeding lines, and PIs and B. vulgaris subsp. cicla commercial cultivars. Overall, this study identified a range of B. vulgaris accessions and cultivar responses to inoculation with PSA, suggesting varying susceptibility to BLS. On the basis of overall mean disease scores and AUDPC ratings, table beet and Swiss chard cultivars recommended for future studies and breeding are ‘Touchstone Gold’, ‘Bull’s Blood’, ‘Ruby Queen’, ‘Kestrel’, and ‘Rainbow ‘because of their lower BLS ratings. Several PIs, including PI 222234 and NSL 28026, appear to have the potential to offer valuable resistance to BLS to be used in future breeding efforts. Furthermore, these, along with more susceptible lines, can be used to generate mapping populations to identify important regions controlling resistance to PSA. Development of BLS resistant table beets and Swiss chard will aid producers in controlling this growing threat.
References
Arabiat, S., Chanda, A.K., Chittem, K. & Khan, M.F.R. 2016 First report of Pseudomonas syringae pv. aptata causing bacterial blight of sugar beet (Beta vulgaris) in Oregon Plant Dis. 100 11 2334 https://doi.org/10.1094/pdis-05-16-0746-pdn
Ark, P.A. & Leach, L.D. 1946 Seed transmission of bacterial blight of sugar beet Phytopathology 36 549 553
Baltrus, D.A., McCann, H.C. & Guttman, D.S. 2017 Evolution, genomics, and epidemiology of Pseudomonas syringae Mol. Plant Pathol. 18 1 152 168 https://doi.org/10.1111/mpp.12506
Brown, N.A. & Jamieson, C.O. 1913 A bacterium causing a disease of sugar beet and nasturtium leaves J. Agric. Res. 1 189 210
Carsner, E. 1944 Black streak, a bacterial disease of sugar beet in the Pacific Northwest Phytopathology 34 933 934
Derie, M.L., Holmes, B.J., Safni, I., Bull, C.T. & du Toit, L.J. 2016 Seedborne inoculum thresholds of Pseudomonas syringae pv. aptata, causal agent of bacterial leaf spot, in ‘Baby Leaf’ Swiss chard crops Phytopathology 106 Suppl 4 142
Dutta, B., Ingram, T., Gitaitis, R.D., Langston, D.B., Brenneman, T., Webster, T.M. & Davis, R.F. 2014 First report of bacterial blight of sugar beet caused by Pseudomonas syringae pv. aptata in Georgia, USA Plant Dis. 98 10 1423 https://doi.org/10.1094/PDIS-03-14-0235-PDN
Gitaitis, R. & Walcott, R. 2008 The epidemiology and management of seedborne bacterial diseases Annu. Rev. Phytopathol. 45 371 397 https://doi.org/10.1146/annurev.phyto.45.06280 6.094321
Gomila, M., Busquets, A., Mulet, A., García-Valdés, E. & Lalucat, J. 2017 Clarification of taxonomic status within the Pseudomonas syringae species group based on a phylogenomic analysis Front. Microbiol. 8 2422 https://doi.org/10.3389/fmicb.2017.02422
Gonzalez, P., Garfin, G.M., Breshears, D.D., Brooks, K.M., Brown, H.E., Elias, E.H., Gunasekara, A., Huntly, N., Maldonado, J.K., Mantua, N.J., Margolis, H.G., McAfee, S., Middleton, B.R. & Udall, B.H. 2018 Southwest 1101 1184 Reidmiller, D.R., Avery, C.W., Easterling, D.R., Kunkel, K.E., Lewis, K.L.M., Maycock, T.K. & Stewart, B.C. Impacts, risks, and adaptation in the United States: Fourth national climate assessment Volume II U.S. Global Change Research Program Washington, DC https://doi.org/10.7930/NCA4.2018.CH25
Grahn, C.M., Benedict, C., Thornton, T. & Miles, C. 2015 Production of baby-leaf salad greens in the spring and fall seasons of northwest Washington HortScience 50 10 1467 1471 https://doi.org/10.21273/hortsci.50.10.1467
Jacobsen, B.J. 2009 Bacterial leaf spot 59 60 Harveson, R.M., Hanson, L.E. & Hein, G.L. Compendium of beet diseases and pests. 2nd ed. American Phytopathological Society St. Paul
Khan, M.F.R., Windels, C.E. & Bradley, C.A. 2018 Comparison of Cercospora and bacterial leaf spots on sugar beet North Dakota State University Extension Service. https://www.ag.ndsu.edu/publications/crops/comparison-of-cercospora- and-bacterial-leafspots-on-sugar-beet. [accessed 1 Sep 2021]
Koike, S.T., Henderson, D.M., Bull, C.T., Goldman, P.H. & Lewellen, R.T. 2003 First report of bacterial leaf spot of Swiss Chard caused by Pseudomonas syringae pv. aptata in California Plant Dis. 87 11 1397 https://doi.org/10.1094/pdis.2003.87.11.1397b
Lamichhane, J.R., Messéan, A. & Morris, C.E. 2015 Insights into epidemiology and control of diseases of annual plants caused by the Pseudomonas syringae species complex J. Gen. Plant Pathol. 81 5 331 350 https://doi.org/10.1007/s10327-015-0605-z
May, C., Luce, C., Casola, J., Chang, M., Cuhaciyan, J., Dalton, M., Lowe, S., Morishima, G., Mote, P., Petersen, A., Roesch-McNally, G. & York, E. 2018 Northwest 1036 1100 Reidmiller, D.R., Avery, C.W., Easterling, D.R., Kunkel, K.E., Lewis, K.L.M., Maycock, T.K. & Stewart, B.C. Impacts, risks, and adaptation in the United States: Fourth national climate assessment Volume II U.S. Global Change Research Program Washington, DC https://doi.org/10.7930/NCA4.2018.CH24
Morris, C.E., Monteil, C.L. & Berge, O. 2013 The life history of Pseudomonas syringae: Linking agriculture to earth system processes Annu. Rev. Phytopathol. 51 85 104 https://doi.org/10.1146/annurev-phyto-082712-102402
Nampijja, M., Derie, M. & du Toit, L.J. 2021 First report of bacterial leaf spot caused by Pseudomonas syringae pv. aptata on Swiss chard, Beta vulgaris subsp. vulgaris, in Arizona Plant Dis. 105 11 3738 https://doi.org/10.1094/pdis-12-20-2554-pdn
Nikolić, I., Stanković, S., Dimkić, I., Berić, T., Stojšin, V., Janse, J. & Popović, T. 2018 Genetic diversity and pathogenicity of Pseudomonas syringae pv. aptata isolated from sugar beet Plant Pathol. 67 5 1194 1207 https://doi.org/10.1111/ppa.12831
Okazaki, K., Ogata, N. & Tanaka, M. 2005 Development of zoospore inoculation method for assay of black root rot resistance in sugar beet Jpn. J. Crop. Sci. 74 1 47 51 https://doi.org/10.1626/jcs.74.47
Peck, N.H., Clark, B.E. & Natti, J.J. 1967 Effect of decortication and fungicide on performance of table beet seed Agron. J. 59 1 78 80 https://doi.org/10.2134/agronj1967.00021962005900010 024x
Pethybridge, S.J., Kikkert, J.R., Hanson, L.E. & Nelson, S.C. 2018 Challenges and prospects for building resilient disease management strategies and tactics for the New York table beet industry Agronomy (Basel) 8 7 1 17 https://doi.org/10.3390/agronomy8070112
Pethybridge, S.J., Sharma, S., Hansen, Z., Kikkert, J.R., Olmstead, D.L. & Hanson, L.E. 2020 Optimizing Cercospora leaf spot control in table beet using action thresholds and disease forecasting Plant Dis. 104 6 1831 1840 https://doi.org/10.1094/PDIS-02-20-0246-RE
Pethybridge, S.J., Vaghefi, N. & Kikkert, J.R. 2017 Horticultural characteristics and susceptibility of table beet cultivars to Cercospora leaf spot in New York HortTechnology 27 4 530 538 https://doi.org/10.21273/HORTTECH03743-17
Pryor, S.C., Scavia, D., Downer, C., Gaden, M., Iverson, L., Nordstrom, R., Patz, J. & Robertson, G.P. 2014 Midwest 418 440 Melillo, J.M., Richmond, T.C. & Yohe, G.W. Climate change impacts in the United States: The third national climate assessment. U.S. Global Change Research Program https://doi.org/10.7930/J0J1012N
Riffaud, C.M.H. & Morris, C.E. 2002 Detection of Pseudomonas syringae pv. aptata in irrigation water retention basins by immunofluorescence colony-staining Eur. J. Plant Pathol. 108 539 545 https://doi.org/10.1023/A:1019919627886
Rotondo, F., Vrisman, C.M., Rani, R., Testen, A.L., Deblais, L. & Miller, S.A. 2020 First report of Pseudomonas syringae pv. aptata causing bacterial leaf spot on common beet (Beta vulgaris) in Ohio Plant Dis. 104 2 561 https://doi.org/10.1094/pdis-08-19-1720-pdn
Safni, I., Sepulveda, L.R., Goldman, P.H., Derie, M.L., du Toit, L.J., Koike, S.T., Stockwell, V.O. & Bull, C.T. 2016 Genetic diversity of Pseudomonas syringae causing bacterial leaf spot on table beet (Beta vulgaris) and Swiss chard (Beta vulgaris subsp. cicla) Phytopathology 106 Suppl 4 143
Scholten, O.E., Panella, L.W., de Bock, T.S.M. & Lange, W. 2001 A greenhouse test for screening sugar beet (Beta vulgaris) for resistance to Rhizoctonia solani Eur. J. Plant Pathol. 107 2 161 166 https://doi.org/10.1023/A:1011208903344
Singh, D. & Mathur, S.B. 2004 Histopathology and seed-borne infection CRC Press Boca Raton, FL
U.S. Department of Agriculture 2019 Census of agriculture, 2017 https://www.nass.usda.gov/Publications/AgCensus/2017/index.php#full_report. [accessed 12 Aug 2022]
Wigg, K.S. & Goldman, I.L. 2020 Variability in reaction to root and crown rot caused by Rhizoctonia solani among table beet cultivars, breeding lines, and plant introductions in controlled environment conditions HortScience 55 9 1482 1494 https://doi.org/10.21273/HORTSCI15011-20
Wintermantel, W.M. & Kaffka, S.R. 2006 Sugar beet performance with curly top is related to virus accumulation and age at infection Plant Dis. 90 5 657 662 https://doi.org/10.1094/PD-90-0657
Xin, X.F., Kvitko, B. & He, S.Y. 2018 Pseudomonas syringae: What it takes to be a pathogen Nat. Rev. Microbiol. 16 5 316 328 https://doi.org/10.1038/nrmicro.2018.17
Mean area under the disease progress curve (AUDPC) of eight Beta vulgaris subsp. vulgaris commercial cultivars, one Beta vulgaris subsp. vulgaris breeding line, and one Beta vulgaris subsp. cicla commercial cultivar during vegetative growth in a greenhouse screen evaluated in 2021. Inoculated plants were spray inoculated with PSA strain BP 1452, and control plants were sprayed with sterilized with Milli-Q water.
Citation: HortScience 57, 11; 10.21273/HORTSCI16777-22
Mean area under the disease progress curve (AUDPC) of six Beta vulgaris subsp. vulgaris commercial cultivars, four Beta vulgaris subsp. vulgaris breeding lines, and six Beta vulgaris subsp. cicla commercial cultivars during vegetative growth in a greenhouse screen evaluated in 2021. Inoculated plants were spray inoculated with PSA strain BP 1452, and control plants were sprayed with sterilized with Milli-Q water.
Citation: HortScience 57, 11; 10.21273/HORTSCI16777-22
Mean area under the disease progress curve (AUDPC) of 26 Beta vulgaris subsp. vulgaris plant introductions (PIs) during vegetative growth in a greenhouse screen evaluated in 2021. Inoculated plants were spray inoculated with PSA strain BP 1452, and control plants were sprayed with sterilized with Milli-Q water.
Citation: HortScience 57, 11; 10.21273/HORTSCI16777-22
Mean area under the disease progress curve (AUDPC) of eight Beta vulgaris subsp. vulgaris commercial cultivars, one Beta vulgaris subsp. vulgaris breeding line, and one Beta vulgaris subsp. cicla commercial cultivar during reproductive growth in a greenhouse screen evaluated in 2021. Inoculated plants were spray inoculated with PSA strain BP 1452, and control plants were sprayed with sterilized with Milli-Q water.
Citation: HortScience 57, 11; 10.21273/HORTSCI16777-22
Mean disease score over days post inoculation of eight Beta vulgaris subsp. vulgaris commercial cultivars, one Beta vulgaris subsp. vulgaris breeding line, and one Beta vulgaris subsp. cicla commercial cultivar in response to spray inoculation with PSA strain BP 1452 during vegetative growth in a greenhouse screen evaluated in 2021. The experimental unit for each accession was four inoculated plants and each accession was screened twice.
Citation: HortScience 57, 11; 10.21273/HORTSCI16777-22
Mean disease score over days post inoculation of six Beta vulgaris subsp. vulgaris commercial cultivars, four Beta vulgaris subsp. vulgaris breeding lines, and six Beta vulgaris subsp. cicla commercial cultivars in response to spray inoculation with PSA strain BP 1452 during vegetative growth in a greenhouse screen evaluated in 2021. The experimental unit for each accession is four plants. ** refers to significant differences among accessions at a particular rating time at P <0.05.
Citation: HortScience 57, 11; 10.21273/HORTSCI16777-22
Mean disease score over days post inoculation of 26 Beta vulgaris subsp. vulgaris plant introductions (PIs) in response to spray inoculation with PSA strain BP 1452 during vegetative growth in a greenhouse screen evaluated in 2021. The experimental unit for each accession is four plants. * refers to significant differences among accessions at a particular rating time at P < 0.1. ** refers to significant differences among accessions at a particular rating time at P < 0.05.
Citation: HortScience 57, 11; 10.21273/HORTSCI16777-22
Mean disease score over days post inoculation of eight Beta vulgaris subsp. vulgaris commercial cultivars, one Beta vulgaris subsp. vulgaris breeding line, and one Beta vulgaris subsp. cicla commercial cultivar in response to spray inoculation with PSA strain BP 1452 during reproductive growth in a greenhouse screen evaluated in 2021. The experimental unit for each accession is four plants.
Citation: HortScience 57, 11; 10.21273/HORTSCI16777-22
Difference in appearance of lesions on dark-colored leaves (A) and light-colored leaves (B).
Citation: HortScience 57, 11; 10.21273/HORTSCI16777-22