Evaluation of Spinach Cultivars for Resistance to Stemphylium Leaf Spot (Stemphylium vesicarium) and White Rust (Albugo occidentalis)

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Kayla A. Spawton Department of Plant Pathology, Washington State University Northwestern Washington Research and Extension Center, 16650 State Route 536, Mount Vernon, WA 98273, USA

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Larry A. Stein Department of Horticultural Sciences, Texas A&M Agrilife Research and Extension Center, 1619 Garner Field Road, Uvalde, TX 77801, USA

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Lindsey J. du Toit Department of Plant Pathology, Washington State University Northwestern Washington Research and Extension Center, 16650 State Route 536, Mount Vernon, WA 98273, USA

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Abstract

Stemphylium leaf spot, caused by Stemphylium vesicarium, and white rust, caused by Albugo occidentalis, can cause significant losses in spinach production. Management of these foliar diseases of spinach has become increasingly challenging with the development of fungicide resistance in some pathogen populations, high planting density and overhead irrigation used for baby leaf spinach production, and the fact that >60% of fresh market spinach production in the United States is certified organic. To identify spinach cultivars with resistance to Stemphylium leaf spot and white rust, a field trial was performed near Crystal City, TX, USA, in 2021 (79 cultivars), 2022 (87 cultivars), and 2023 (63 cultivars). Each year, the plants were inoculated with S. vesicarium and rated for disease severity. Plants were also rated for white rust severity that resulted from natural infection during the 2021 and the 2022 trials. During each trial, 11% to 27% of the cultivars were identified as resistant to Stemphylium leaf spot, and another 29% to 48% had moderately resistant reactions. In contrast, only 5 of 79 cultivars (6%) in the 2021 trial did not develop symptoms of white rust, and all 87 cultivars evaluated in the 2022 trial had symptoms of white rust. Although there was no significant correlation between mean Stemphylium leaf spot ratings and mean white rust ratings during these trials, the cultivars Colusa, Kodiak, PV-1569, and PV-1664 displayed resistant or moderately resistant responses to both diseases in at least two trials. Therefore, processing and fresh market spinach growers have resistant cultivars from which to select to reduce the economic impacts of Stemphylium leaf spot and white rust.

Spinach (Spinacia oleracea L.) is a cool-season, leafy green vegetable grown for both fresh and processing markets (Morelock and Correll 2008). Spinach consumption increased globally in the 1990s and 2000s with the popularity of prepacked baby leaf spinach as well as increased awareness of the nutritional value of spinach. Based on the most recent Census of Agriculture for which data are available, spinach hectares harvested in the United States increased from ∼18,800 in 2012 to 28,300 in 2017 (2600 for processing and 25,700 for fresh market) (US Department of Agriculture, National Agricultural Statistics Service 2019). California was the top-producing state in 2017, with 19,550 ha (18,900 for fresh market and 650 for processing). Arizona followed with 4900 ha, all for fresh market. The third largest spinach-producing state was Texas, with 950 ha (530 for fresh market and 420 for processing) (US Department of Agriculture, National Agricultural Statistics Service 2019).

Stemphylium leaf spot of spinach was first described in California in 2001 (Koike et al. 2001). The causal agent was identified as the fungus Stemphylium botryosum Wallr. based on morphology (Wallroth 1833). Symptoms begin as 2-mm-diameter, gray-green spots that expand and coalesce into tan, necrotic lesions that often resemble chemical burn. Stemphylium leaf spot has been reported in other regions of spinach production in the United States, including Arizona (Koike et al. 2005), Delaware, Maryland (Everts and Armentrout 2001), Florida (Raid and Kucharek 2006), New York (Spawton et al. 2020), Oregon (du Toit and Ocamb 2023b), Texas (Reed et al. 2010), and Washington (du Toit and Derie 2001), as well as internationally, including in Italy (Gilardi et al. 2018) and Japan (Misawa et al. 2017). The disease is associated with relatively warm and wet conditions (Koike et al. 2001). The pathogen can be seedborne and can infect both the pericarp and embryo of seed (Hernandez-Perez and du Toit 2006). Other sources of inoculum include infected spinach volunteers and spinach residues, especially in regions of spinach seed production where the teleomorph can overwinter on stem residues left on the soil surface after harvest of spinach seed crops (du Toit and Derie 2003). Symptomatic or asymptomatic plants may be a potential source of inoculum, as documented for Stemphylium pathogens of other crops (Foster et al. 2019; Hanse et al. 2015; McDonald et al. 2022). For example, isolates of Stemphylium spp. were found to infect both Welsh onion (Allium fistulosum) and spinach (Misawa et al. 2017).

With recent revisions to the taxonomy of the genus Stemphylium (Woudenberg et al. 2017), and with many more DNA sequences of Stemphylium isolates now available publicly, S. beticola and S. vesicarium have been determined more recently to be the two causal agents of Stemphylium leaf spot of spinach (Gilardi et al. 2018, 2022; Liu et al. 2020; Spawton et al. 2019, 2020). Isolates identified previously as S. botryosum on spinach are now recognized to be S. beticola, a species first characterized in 2016 after the fungus was found to cause yellow leaf spot on sugar beet (Beta vulgaris subsp. vulgaris) in the Netherlands (Crous et al. 2016; Hanse et al. 2015).

Stemphylium spp. can colonize both the pericarp and embryo of spinach seed (Hernandez-Perez and du Toit 2006), but the spinach pathogens are relatively thermophilic (Koike et al. 2001), which may account for why disinfectant, hot water, and steam treatments of spinach seed had limited efficacy for eradicating the pathogen from infected seed lots (du Toit and Hernandez-Perez 2005; du Toit et al. 2018b). Nonetheless, hot water seed treatment can eradicate Stemphylium spp. from seed lots with low incidences of infection or when infection is limited to the pericarp (du Toit and Hernandez-Perez 2005), and it can be a valuable organic seed treatment, particularly because >60% of baby leaf spinach production in the United States is certified organic (Colfer 2023). For seed that is infected more internally with Stemphylium spp., hot water and chlorine treatments can reduce, but not eradicate, Stemphylium spp. (du Toit and Hernandez-Perez 2005).

Fungicide seed treatments, such as Coronet (pyraclostrobin + boscalid; BASF, Ludwigshafen, Germany), can be effective for controlling seed transmission of Stemphylium spp. (du Toit et al. 2007, 2010, 2018a). However, numerous isolates of S. vesicarium obtained from symptomatic spinach crops in multiple states during the past 5 years have been demonstrated to be resistant to azoxystrobin and pyraclostrobin, which are two fungicides in Fungicide Resistance Action Committee (FRAC) group 11 (Spawton et al. 2019). Additionally, even though Cabrio (pyraclostrobin; BASF) and Quadris (azoxystrobin; Syngenta, Basel, Switzerland) initially were very effective for controlling Stemphylium leaf spot in spinach crops in Florida (Raid et al. 2017) and Washington (du Toit et al. 2004), applications of these two fungicides have failed to control this disease in baby leaf spinach crops in Florida during the past 5 years (Raid et al. 2018).

Effective cultural practices to minimize conidia production and dispersal of Stemphylium spp. include limiting periods of leaf wetness by irrigating crops earlier in the day, reducing the frequency of irrigation, and avoiding the use of overhead irrigation (although this is not feasible for baby leaf production) (du Toit and Ocamb 2023b). Other cultural practices include planting rows into the primary wind direction to reduce the duration of leaf wetness after rain and irrigation events (Raid and Kucharek 2006), incorporating crop residues into the soil after the harvest of spinach crops (particularly residues of spinach seed crops) (du Toit and Derie 2003), increasing the duration of crop rotation out of spinach, and avoiding sequential plantings of spinach.

Another management option for Stemphylium leaf spot is planting resistant cultivars. However, studies published to date regarding screening for resistance to Stemphylium leaf spot of spinach have focused on S. beticola, not S. vesicarium. Spinach isolates of S. botryosum (S. beticola) caused leaf spots on 10 flat leaf, 8 semi-savoy, and 2 savoy spinach cultivars tested when the disease was first described (Koike et al. 2001). Mou et al. (2008) screened 338 accessions from the United States Department of Agriculture (USDA) National Plant Germplasm System (NPGS) collection as well as 22 commercial cultivar for resistance to S. beticola. All plant introduction (PI) lines or cultivars developed symptoms. Similarly, Shi et al. (2016) found that all 265 accessions from the USDA NPGS and 8 commercial cultivars screened developed Stemphylium leaf spot when inoculated with S. beticola. However, they identified eight single-nucleotide polymorphism (SNP) markers associated with quantitative resistance to Stemphylium leaf spot caused by S. beticola.

White rust of spinach is caused by the obligate oomycete Albugo occidentalis G. W. Wils. (Wilson 1907). The disease was first identified on spinach in Virginia in 1910, and it became important economically in 1937 after white rust was found on spinach grown in Texas and sold at New York vegetable markets (Walker 1952; Wiant 1937). In the United States, white rust is a major disease of spinach grown for processing and fresh markets in Arkansas, Oklahoma, and Texas (Morelock and Correll 2008; Walker 1952). More recently, white rust was found in a single location in California (Putnam 2020). The disease has also been documented in Greece (Vakalounakis and Doulis 2013), Italy (Gilardi et al. 2021), Mexico (Correll et al. 2017), and Turkey (Soylu et al. 2018). Chlorotic lesions first develop on the adaxial leaf surface, and then white pustules, in which sporangia are produced, form on the abaxial leaf surface (Raid and Kucharek 2006). Severe infection can lead to foliar necrosis (Raabe and Pound 1952).

White rust is exacerbated by extended periods of leaf wetness, and the pathogen grows optimally at 12 to 18 °C (Sullivan et al. 2002). A. occidentalis overwinters as thick-walled oospores that develop in the stems and leaves of spinach. Management of white rust is based on planting resistant cultivars, using a minimum 3-year rotation out of spinach, and applications of fungicides at planting and to foliage [e.g., the systemic fungicide metalaxyl (FRAC group 4)] (Correll et al. 1994; Dainello et al. 1990). Cultural practices to reduce periods of leaf wetness, such as planting spinach on raised beds and the use of furrow irrigation for processing crops, can also reduce disease pressure (Holloway et al. 2003). Previous studies that screened cultivars for resistance to white rust identified some cultivars with partial resistance, but all cultivars developed some level of symptoms (Brandenberger et al. 1994; Goreta and Leskovar 2006). A genome-wide association study by Awika et al. (2019) identified 448 minor alleles associated with severity of white rust in 267 spinach accessions, whereas Shi et al. (2022) identified nine SNPs associated with white rust resistance during the screening of 346 USDA NPGS accessions.

With the development of resistance to FRAC group 11 fungicides in populations of S. vesicarium, the predominant causal agent of Stemphylium leaf spot of spinach in the southern United States (Raid et al. 2018, 2020, 2021; Spawton et al. 2019), the dense plantings used for baby leaf spinach production with overhead irrigation and sequential plantings, and the growing popularity of certified organic spinach in the United States, it is increasingly challenging to produce high-quality spinach without losses to foliar diseases like Stemphylium leaf spot and white rust. Identifying or breeding spinach cultivars with resistance to these diseases represents one of the best options for managing these diseases more sustainably. The objective of this study was to screen commercial spinach cultivars for resistance to Stemphylium leaf spot caused by S. vesicarium in the Texas Wintergarden region of spinach production. During the field trials, spinach plants became infected naturally with A. occidentalis, providing an opportunity to screen the cultivars for resistance to white rust as well as Stemphylium leaf spot.

Materials and Methods

2021 field trial.

Spinach was planted on 17 Dec 2020 in a grower-cooperator’s field in the Wintergarden region near Crystal City, TX, USA (28°43′34″N, 99°48′26″W), that was irrigated by center pivot to screen cultivars for resistance to Stemphylium leaf spot caused by S. vesicarium. S. vesicarium was selected instead of S. beticola because the majority (>90%) of isolates from symptomatic spinach crops in Texas during the past 5 to 10 years have been S. vesicarium (Spawton et al. 2019). Seed was planted in three replicate plots (each with a length of ∼3 m) for each of 79 cultivars submitted by six vegetable seed companies (Supplemental Table 1) on raised beds at ∼6.2 million seed/ha using the grower’s Seed Spider Planter (Sutton Agricultural Enterprises, Inc., Salinas, CA, USA) with 42 lines per bed, as is typical for baby leaf spinach production in Texas. Each bed had a height of ∼13 cm and width of ∼1.6 m. The large scale of the planter necessitated planting three beds at a time, with cultivars planted in the order of seed size for the lots received (smallest to largest); therefore, the 79 cultivars were planted in the same order in each replicate block. Nontreated seed of each cultivar was requested from seed companies, but seed of a few cultivars received were treated with fungicides (Supplemental Table 1). Spinach plants were maintained by the grower-cooperator using practices typical for the Wintergarden region of Texas (Holloway et al. 2003). The field was fertilized before planting with 15N–27P–9K–3S (Helena Agri-Enterprises, LLC, Collierville, TN, USA) at 567 kg⋅ha−1. Plants were irrigated with ∼1.9 cm of water after planting using the center pivot, and ∼1.9 cm of water every week or every other week leading up to the first inoculation, depending on weather conditions. Dual Magnum (S-metolachlor; Syngenta, Basel, Switzerland) was applied immediately after planting at 0.58 L⋅ha−1 to control weeds. PermaStar (permethrin; LG Life Sciences America Inc., Englewood Cliffs, NJ, USA) was applied 3 weeks after planting at 0.22 L⋅ha−1, and Baythroid (cyfluthrin; Bayer CropScience LP, St. Louis, MO) was applied 4 weeks after planting at 0.22 L⋅ha−1 to control cucumber beetle (Diabrotica undecimpunctata). All applications were broadcast with a John Deere 4630 sprayer (Moline, IL, USA).

Spinach plants in each plot were inoculated with a spore suspension of a mixture of three isolates of S. vesicarium (St0481, St0487, and St0523) obtained originally from symptomatic spinach crops in Texas in 2019 and verified as pathogenic on the spinach cultivar Mandolin (Spawton et al. 2019). Inoculum was applied on 19 Jan and 2 Feb 2021, 5 and 7 weeks after planting, respectively. For each inoculation, each isolate was grown on clarified V8 (CV8) agar medium (300 plates/isolate) for a total of 900 plates per inoculation. CV8 agar medium was prepared by mixing 4.5 g of CaCO3 with 200 mL of V8 juice (Campbell Soup Co., Camden, NJ, USA) in a flask with a magnetic stirrer for 15 min. The suspension was centrifuged at 3500 rpm for 15 min. A 200-mL sample of clarified V8 supernatant was added to 800 mL of deionized water and 15 g agar, and the suspension was autoclaved at 15 psi and 121 °C for 30 min. Cultures of each isolate were initiated on CV8 agar medium from a piece of colonized, dried filter disk (diameter, 1.5 cm; #413; VWR International, LLC, Radnor, PA, USA) kept in long-term storage at room temperature (20 ± 2 °C) for the Vegetable Seed Pathology Program at the Washington State University Mount Vernon Northwestern Washington Research and Extension Center. A 5-mm3, colonized agar plug was taken from the leading edge of a 10-day-old colony, placed on each of 300 plates of CV8 agar medium for each isolate, and incubated on a lab bench at room temperature near a south-facing window with blinds or a north-facing window with a ∼12-h/12-h day/night cycle using supplementary indoor fluorescent lighting (4100K) by day. After 2 weeks, the colonized petri plates were stored at 4 °C for up to 6 weeks, when the inoculum was shipped to the Texas A&M AgriLife Research and Extension Center in Uvalde, TX, USA.

For each inoculation, the colonized agar medium was removed from the petri plates with a spatula and mixed with water in a blender for 12 to 15 s; then, the suspension was poured through a 20-wire mesh tea strainer to remove the agar. A total of ∼45.4 L of spore suspension was prepared for each inoculation, and the surfactant DyneAmic (methyl esters of C16 to C18 fatty acids; Helena Agri-Enterprises, LLC) was added at 0.37% for the first inoculation and 0.88% for the second inoculation. Half of the inoculum (∼22.7 L) was applied over the entire trial at each inoculation using a CO2-pressurized backpack sprayer set to 40 to 42 psi. The remainder of the inoculum was used for other spinach trials in that field. The boom had a single 8008 nozzle that dispensed inoculum in a ∼0.9-m wide band at ∼748 L⋅ha−1. Plants were irrigated with ∼0.6 cm of water when first inoculated, ∼0.4 cm of water the following day, and ∼0.4 cm of water every other day until the plants were rated for disease severity, to provide a conducive environment for Stemphylium leaf spot. White rust developed during the trial as a result of natural infection.

Each plot was rated for the severity of white rust on 12 Feb 2021, 8 weeks after planting, and for severity of Stemphylium leaf spot on 20 Feb, 9 weeks after planting. Each plot was rated using a scale of 1 (no symptoms) to 10 (90%–100% of the foliage symptomatic), with ratings in ∼10% increments for each disease. Each disease was rated separately.

2022 field trial.

The spinach cultivar trial was repeated in the same center pivot-irrigated field in 2021 to 2022. On 15 Dec 2021, seed of 81 spinach cultivars submitted by nine seed companies (Supplemental Table 2) were planted in each of three replicate blocks at ∼6.2 million seed/ha, as described for the 2021 trial. An additional six spinach cultivars were planted at ∼1.2 million seed/ha to represent a planting density typical for processing spinach production because these cultivars are grown primarily for processing. Of the 81 cultivars planted at the baby leaf density, 46 had been in the 2021 field trial. The field was fertilized before planting using 16N–32P–8K (Helena Agri-Enterprises, LLC) at 545 kg⋅ha−1. PermaStar, Baythroid, and Dual Magnum were applied as described for the 2021 trial. A similar irrigation schedule was used as described for the 2021 trial.

Spinach plants were inoculated with the same three isolates of S. vesicarium used in the 2021 trial. Inoculum was applied on 18 Jan and 3 Feb 2022, 5 and 7 weeks after planting, respectively, using the protocol described for the 2021 trial. As noted for the previous trial, the spinach plants became infected with A. occidentalis from naturally occurring inoculum in the field. Each plot was rated for severity of white rust and severity of Stemphylium leaf spot on 15 Feb 2022, 9 weeks after planting, using the rating scale described for the 2021 trial.

2023 field trial.

The trial was repeated in the same center pivot-irrigated field in 2022 to 2023. On 20 Dec 2022, seed of 63 spinach cultivars submitted by eight seed companies (Supplemental Table 3) were planted in each of three replicate blocks at ∼6.2 million seed/ha, as described for the previous trials. Of the 63 cultivars, 26 were included in the 2021 trial and 27 in the 2022 trial. Overall, 15 cultivars were included in all three trials. The field was fertilized before planting using 19N–23P–7K–5S–0.28Fe (Helena Agri-Enterprises, LLC) at 696 kg⋅ha−1. Ridomil Gold (mefenoxam, Syngenta) was banded directly over the soil surface at planting at ∼0.73 L⋅ha−1 to control white rust because the severity of white rust in the 2021 and 2022 trials confounded severity ratings for Stemphylium leaf spot on those cultivars that were highly susceptible to white rust. Ridomil Gold was broadcast over the plants 4 weeks after planting at 0.29 L⋅ha−1, and again 6 weeks after planting at 0.58 L⋅ha−1, using a John Deere 4630 sprayer. The insecticides Perm-Up (permethrin; United Phosphorus Inc., King of Prussia, PA, USA) and Radiant (spinetoram, Corteva Agriscience, Indianapolis, IN, USA) were applied at 0.22 and 0.37 L⋅ha−1, respectively, at the two-leaf stage to control cucumber beetle. Fastac (alpha-cypermethrin; BASF) was applied again 3 weeks after planting at 0.29 L⋅ha−1, and Perm-Up was applied 6 weeks after planting at 0.29 L⋅ha−1 to control cucumber beetle. Trilogy (neem oil; Certis Biologicals, Columbia, MD, USA) was applied on 20 Feb, 9 weeks after planting, at 1.46 L⋅ha−1 to control false chinch bug (Nysius raphanus). A similar irrigation schedule as described for the previous trials was used.

Spinach plants were inoculated with the same three isolates of S. vesicarium used in the previous trials, on 18 Jan and 3 Feb 2023, 4 and 6 weeks after planting, respectively, using the protocol described, except 0.01% Tween 80 was added to the inoculum instead of DyneAmic. Each plot was rated for severity of Stemphylium leaf spot on 21 Feb 2023, 9 weeks after planting, using the rating scale described previously.

Weather data were retrieved from a weather station managed by DTN (Burnsville, MN, USA) near Crystal City, TX, USA, for the duration of each trial, i.e., from December to February, including daily minimum, maximum, and average temperatures (°C), minimum and maximum relative humidity (%), and total daily precipitation (mm), to examine these weather parameters in relation to development of Stemphylium leaf spot and white rust in each trial.

Data analysis.

PROC GLIMMIX (SAS Enterprise version 3.81; SAS Institute Inc., Cary, NC, USA) was used to calculate an analysis of variance (ANOVA) for each trial to assess whether there were significant differences in severity of Stemphylium leaf spot or white rust among cultivars. Cultivar was treated as a fixed effect and replication was treated as a random effect in each trial. Data were analyzed separately for each trial because of differences in the cultivars included in each trial. PROC GLIMMIX also was used to assess the significance of differences in severity ratings for Stemphylium leaf spot and white rust among cultivars included in any of the three trials, with cultivar treated as a fixed effect, trial treated as a random effect, and replication treated as a random effect nested within each trial. Similarly, an ANOVA was used to determine the significance of differences in severity of Stemphylium spot among the 15 cultivars common to all three trials. The COVTEST function was used to assess whether variances of the trials and the interaction of trial with cultivar were significant. Severity ratings were rank-transformed using Friedman’s nonparametric test for all ANOVAs because of heterogenous variances across the trials. Data combined from all trials were sorted by year before ranking, whereas data analyzed individually for each trial were sorted by replication. Spearman’s correlation coefficient (ρ) was calculated for severity of white rust and Stemphylium leaf spot within each trial and to compare mean severity ratings for each disease between trials for those cultivars planted in at least two trials.

Spinach cultivars were categorized into five disease severity classes (resistant, moderately resistant, moderate, moderately susceptible, and susceptible) based on the z-scores of the mean severity rating of each cultivar over the three replications (Pataky et al. 2011) calculated separately for each disease and trial. The z-score was calculated with PROC STANDARD in SAS, with a mean of 0 and SD of 1. For Stemphylium leaf spot ratings in each trial, the z-scores of cultivars were considered as follows: <−0.900, resistant; −0.900 to −0.301, moderately resistant; −0.300 to 0.300, moderate; 0.301 to 0.900, moderately susceptible; and >0.900, susceptible. For white rust ratings in the 2021 trial, the z-scores of cultivars were considered as follows: <−1.200, resistant; −1.200 to −0.401, moderately resistant; −0.400 to 0.400, moderate; 0.401 to 1.200, moderately susceptible; and >1.200, susceptible. For white rust ratings in the 2022 trial, the five categories were based on z-scores of <−1.800, −1.800 to −0.601, −0.600 to 0.600, 0.601 to 1.800, and >1.800, respectively.

Results

Inoculation with S. vesicarium resulted in the development of Stemphylium leaf spot in all three field trials. Based on the ANOVA for Stemphylium leaf spot severity ratings across the three trials, there was a significant cultivar main effect (P < 0.001), a significant trial main effect (P = 0.002), and a significant trial × cultivar interaction (P < 0.001), but the effect of replications nested in the trial was not significant (P = 0.105). For white rust severity ratings in the two trials in which this disease was not controlled with fungicides, there was a significant cultivar main effect (P < 0.001), trial main effect (P = 0.046), and trial × cultivar interaction (P < 0.001), but replications nested in the trial were not significant (P = 0.258). Therefore, results were analyzed separately by trial for each disease.

2021 trial.

In the 2021 trial, the severity of Stemphylium leaf spot and white rust differed significantly among the 79 cultivars (P < 0.001) (Supplemental Table 1). Stemphylium leaf spot severity had a rating range of 1.0 to 8.0 (out of a maximum of 10.0) for individual plots and an average of 2.9 ± 0.1 (mean ± SE) (Fig. 1A). The mean severity for individual cultivars ranged from 1.0 to 7.0, with a median of 1.7 and mean of 2.9 ± 0.2 for all 79 cultivars. Based on the z-score categories of cultivar responses to inoculation with S. vesicarium, 21 cultivars were categorized as having a resistant response (mean severity of 1.0, i.e., no symptoms of Stemphylium leaf spot), 23 had moderately resistant ratings (1.3–2.0), 9 had moderate ratings (2.3–3.3), 2 had moderately susceptible ratings (4.0–4.7), and 24 had susceptible ratings (5.0–7.0).

Fig. 1.
Fig. 1.

Mean severity of Stemphylium leaf spot caused by Stemphylium vesicarium for each of 79 spinach cultivars evaluated during a field trial in 2021 (A), 87 cultivars evaluated during a field trial in 2022 (B), and 63 cultivars evaluated during a field trial in 2023 (C) near Crystal City, TX, USA. Disease severity was rated using a scale of 1 to 10 (1 = no symptoms and 10 = 90%–100% of the canopy with symptoms). Each cultivar was planted in three replicate plots at ∼6.2 million seed/ha, except for six processing cultivars (denoted with an asterisk) planted in the 2022 trial at ∼1.2 million seed/ha: 308, Baboon, Molokai, Solomon, SV3580VC, and Vancouver. Each plot had a length of 3.0 m and width of 1.6 m. Plants were inoculated with three isolates of S. vesicarium obtained originally from symptomatic spinach crops in Texas. Ratings are color-coded based on the disease severity category of each cultivar (resistant, moderately resistant, moderate, moderately susceptible, and susceptible) determined using the z-scores for mean disease severity in each trial.

Citation: HortScience 59, 1; 10.21273/HORTSCI17373-23

The severity of white rust resulting from natural infection had a range of 1.0 to 10.0 in individual plots and an average of 4.0 ± 0.1 (Fig. 2A, Supplemental Table 1). The mean severity for individual cultivars ranged from 1.0 to 8.7, with a median of 3.7 and mean of 4.0 ± 0.2 for all 79 cultivars. Based on the z-scores, 10 cultivars had resistant responses to white rust (mean severity of 1.0–1.3), 19 had moderately resistant ratings (1.7–3.0), 23 had moderate ratings (3.3–4.7), 17 had moderately susceptible ratings (5.0–6.3), and 10 had susceptible ratings (6.7–8.7).

Fig. 2.
Fig. 2.

Mean severity of white rust caused by Albugo occidentalis for each of 79 spinach cultivars planted during a field trial in 2021 (A) and 87 spinach cultivars planted during a field trial in 2022 (B) near Crystal City, TX, USA. Disease severity was rated using a scale of 1 to 10 (1 = no symptoms and 10 = 90%–100% of the canopy with symptoms). Each cultivar was planted in three replicate plots at ∼6.2 million seed/ha, except for six processing cultivars (denoted with an asterisk) planted in 2022 at ∼1.2 million seed/ha: 308, Baboon, Molokai, Solomon, SV3580VC, and Vancouver. Each plot had a length of 3.0 m and width of 1.6 m. White rust developed as a result of natural infection. White rust mean severity ratings are color-coded based on the disease category (resistant, moderately resistant, moderate, moderately susceptible, and susceptible) determined using the z-scores calculated for each cultivar in each trial.

Citation: HortScience 59, 1; 10.21273/HORTSCI17373-23

The correlation between mean Stemphylium leaf spot ratings and mean white rust ratings for the 79 cultivars was not significant (ρ = 0.170; P = 0.134) (Table 1). Salamander was the only cultivar categorized as resistant to both diseases, with a mean Stemphylium leaf spot rating of 1.0 ± 0 (no symptoms in all replicate plots) and a mean white rust rating of 1.3 ± 0.3. Besides Salamander, the following 16 other cultivars were categorized as resistant or moderately resistant to both diseases: 51-se721, Baboon, Colusa, Corvus, Fantail, Houston, Kodiak, Laredo, PV-1526, PV-1569, PV-1599, PV-1664, Renegade, Scorpius, Spiros, and Sunangel. The following four cultivars had susceptible responses to both diseases: Magnetic, Kona, RSO6661470, and Rapanui.

Table 1.

Correlations of mean severity ratings of Stemphylium leaf spot caused by Stemphylium vesicarium in spinach field trials in Texas in 2021, 2022, and 2023, and severity of white rust caused by Albugo occidentalis in the 2021 and 2022 trials.

Table 1.

2022 trial.

During the 2022 trial, similar to the 2021 trial, severity of Stemphylium leaf spot and white rust differed significantly among the 87 cultivars (P < 0.001) (Supplemental Table 2). Stemphylium leaf spot severity ranged from 1.0 to 7.0 for individual plots, with an average of 2.1 ± 0.1 (Fig. 1B). The mean severity for individual cultivars ranged from 1.0 to 5.0, with a median of 1.7 and mean of 2.1 ± 0.1 for all 87 cultivars. Stemphylium leaf spot was less severe overall in the 2022 trial compared with the 2021 trial (Fig. 1B). Based on the z-scores, 10 cultivars had resistant ratings (mean of 1.0), 38 had moderately resistant ratings (1.3–1.7), 18 had moderate ratings (2.0–2.3), 2 had moderately susceptible ratings (2.7–3.0), and 19 had susceptible ratings (3.3–5.0).

White rust severity ranged from 1.0 to 9.0 in individual plots, with an average of 5.2 ± 0.1 (Fig. 2B, Supplemental Table 2). The mean severity for individual cultivars ranged from 2.0 to 8.3, with a median of 5.3 and mean of 5.2 ± 0.2 for all 87 cultivars. In contrast to Stemphylium leaf spot, white rust was more severe in the 2022 trial than the 2021 trial. Based on the z-scores, 3 cultivars had resistant responses (mean severity of 2.0–2.3), 22 had moderately resistant ratings (2.7–4.0), 39 had moderate ratings (4.3–6.0), 20 had moderately susceptible ratings (6.3–7.7), and 3 had susceptible ratings (8.0–8.3). All cultivars evaluated developed symptoms of white rust, even those categorized as resistant.

Similar to the 2021 trial, the correlation of mean Stemphylium leaf spot ratings with mean white rust ratings for the 87 cultivars in the 2022 trial was not significant (ρ = 0.062; P = 0.567) (Table 1). No cultivar had completely resistant reactions to both diseases. San Juan was highly resistant to Stemphylium leaf spot (mean of 1.0 ± 0) and moderately resistant to white rust (3.0 ± 0.6). PV-1569 was categorized as resistant to white rust (2.0 ± 0) and moderately resistant to Stemphylium leaf spot (1.3 ± 0.3). The following 11 cultivars had moderately resistant responses to both diseases: Aries, Bonnethead, Cabezon, Colusa, Fanfish, Kodiak, Lacerta, Nembus, Nun 05049, PV-1664, and Tabit. Kona was the only cultivar categorized as susceptible to both diseases, reflecting the same reactions of this cultivar to both diseases in the 2021 trial.

Of the six cultivars planted at the density typical for processing spinach crops, two were also planted at the baby leaf density: Molokai and SV3580VC. Molokai had a susceptible response to Stemphylium leaf spot (mean severity of 3.7 ± 0.3), a moderate response to white rust (5.3 ± 0.9) in plots planted at the baby leaf population, and it had a similar susceptible response to Stemphylium leaf spot (4.0 ± 0.6) and a moderate response to white rust (5.0 ± 0.6) in plots planted at the processing population. SV3580VC had a moderately resistant response to Stemphylium leaf spot (1.7 ± 0.3) and a moderately susceptible response to white rust (6.7 ± 0.3) in plots planted at the baby leaf population compared with a resistant response to Stemphylium leaf spot (1.0 ± 0) and a moderate response to white rust (4.7 ± 0.3) in plots planted at the processing population; in other words, this cultivar had slightly less severe responses to the two pathogens when planted at the lower processing density.

2023 trial.

In the 2023 trial, the severity of Stemphylium leaf spot differed significantly among the 63 cultivars (P < 0.001) (Fig. 1C, Supplemental Table 3). Stemphylium leaf spot severity ranged from 1.0 to 7.0 for individual plots and had an average of 2.5 ± 0.1. The mean severity for individual cultivars ranged from 1.0 to 5.7, with a median of 2.0 and mean of 2.5 ± 0.2 for all 63 cultivars. Overall, Stemphylium leaf spot was more severe in this trial than in the 2022 trial, but it was less severe than in the 2021 trial (Fig. 1). Based on the z-scores, 7 cultivars had a resistant rating (mean severity of 1.0 ± 0), 30 had a moderately resistant rating (1.3–2.0), 5 had a moderate rating (2.3–2.7), 6 had a moderately susceptible rating (3.0–3.7), and 15 had a susceptible rating (4.0–5.7). The seven cultivars categorized as resistant were Aardvark, Bandera, Callisto, Cocopah, Formax, PV-1569, and Skarne. The 15 cultivars with susceptible ratings were 51-or200, 51-se730, Crater, E6T, Frontier, Harmonica, Kona, Motutapu, Mykonos, Odin, Opal, Patton, Rangitoto, Volans, and Zisa.

Consistency of spinach cultivar reactions among trials.

The correlation of mean Stemphylium leaf spot ratings for the 46 cultivars planted in both the 2021 and 2022 trials was significant (ρ = 0.469; P = 0.001) (Table 1, Fig. 3A). Of these 46 cultivars, 15 (33%) were in the same severity category in both trials (6 as moderately resistant and 9 as susceptible) and 26 cultivars (57%) differed by only one severity category between trials. Five cultivars (11%) had disparate ratings of two or more categories between the trials: Cocopah (resistant in 2021, with a mean severity of 1.0 ± 0, and susceptible in 2022, with a mean of 4.3 ± 0.9), Fantail (moderately resistant in 2021, with a mean of 1.3 ± 0.3, and moderately susceptible in 2022, with a mean of 2.7 ± 0.3), Laredo (resistant in 2021, with a mean of 1.0 ± 0, and moderate in 2022, with a mean of 2.0 ± 0), Patton (susceptible in 2021, with a mean of 6.7 ± 0.3, and moderate in 2022, with a mean of 2.3 ± 0.3), and Silverwhale (moderate in 2021, with a mean of 3.3 ± 0.3, and resistant in 2022, with a mean of 1.0 ± 0). Of the 14 cultivars categorized as resistant in the 2021 trial (no Stemphylium leaf spot symptoms), 12 were moderately resistant in the 2022 trial. The exceptions were Cocopah, which was susceptible in the 2022 trial (Fig. 3A), and Laredo, which had a moderate rating. When Cocopah was excluded from the analysis, the correlation for mean Stemphylium leaf spot ratings for the remaining 45 cultivars in both trials increased (ρ = 0.538; P < 0.001) (Table 1). Cocopah, not Laredo, was excluded from the analysis because the discrepancy between ratings of Cocopah was exacerbated by the moderately susceptible white rust response of this cultivar (6.7 ± 0.9). Of the four cultivars resistant to Stemphylium leaf spot in the 2022 trial, the following three were moderately resistant in the 2021 trial: Parakeet, Spiros, and Vicuna. The remaining cultivar, Silverwhale, had a moderate severity rating for Stemphylium leaf spot (3.3 ± 0.3) in the 2021 trial. The seed lot of Silverwhale received was treated with ProSeed (fludioxonil), Thiram (thiram), and Apron XL (mefenoxam) in the 2022 trial, but not in the 2021 trial. The fungicide seed treatment in the 2022 trial may have impacted severity of symptoms compared with nontreated seed planted in the 2021 trial because fludioxonil and thiram have some efficacy against seedborne infection (du Toit et al. 2010, 2018a).

Fig. 3.
Fig. 3.

Mean severity of Stemphylium leaf spot for 46 spinach cultivars planted during both the 2021 and 2022 field trials (A), 26 cultivars planted during both the 2021 and 2023 field trials (B), and 27 cultivars planted during both the 2022 and 2023 field trials (C) near Crystal City, TX, USA. Disease severity was rated using a scale of 1 to 10 (1 = no symptoms and 10 = 90%–100% of the canopy with symptoms). Each cultivar was planted in three replicate plots at ∼6.2 million seed/ha. Plots were inoculated with three isolates of Stemphylium vesicarium obtained originally from spinach crops in Texas. Ratings for cultivars are color-coded based on the disease severity category (resistant, moderately resistant, moderate, moderately susceptible, and susceptible) determined using the z-scores calculated for each cultivar in each trial.

Citation: HortScience 59, 1; 10.21273/HORTSCI17373-23

There was a significant correlation of mean white rust ratings of the 46 cultivars shared between the 2021 and 2022 trials (ρ = 0.545; P < 0.001) (Table 1). Of the 46 cultivars, 18 (39%) were in the same white rust severity category between the two trials (1 resistant, 5 moderately resistant, 6 moderate, 5 moderately susceptible, and 1 susceptible). However, most cultivars (22 = 48%) only differed between the two trials by one severity category, except for the following six cultivars (13%): Eland (resistant in 2021, with a mean of 1.3 ± 0.3, and moderate in 2022, with a mean of 4.7 ± 0.3), Lizard (resistant to white rust in 2021, with a mean of 1.0 ± 0, and moderate in 2022, with a mean of 6.0 ± 0.6), Melville (resistant in 2021, with a mean of 1.0 ± 0, and moderately susceptible in 2022, with a mean of 7.3 ± 0.7), Salamander (resistant in 2021, with a mean of 1.3 ± 0.3, and moderate in 2022, with a mean of 4.3 ± 1.2), Scorpius (moderately resistant in 2021, with a mean of 3.0 ± 0.6, and moderately susceptible in 2022, with a mean of 7.3 ± 0.3), and SV2146VB (susceptible in 2021, with a mean of 7.0 ± 0.6, and moderate in 2022, with a mean of 6.0 ± 0.6). Of seven cultivars planted in both trials that were resistant to white rust in the 2021 trial, Hammerhead was the only cultivar categorized as resistant in both trials, with mean severity values of 1.3 ± 0.3 in 2021 and 2.3 ± 0.7 in 2022.

Twenty-six cultivars were planted in both the 2021 and 2023 trials (Fig. 3B), with a significant correlation in mean Stemphylium leaf spot ratings between trials (ρ = 0.389; P = 0.049) (Table 1). Of the 26 cultivars, nine (35%) were in the same severity category between trials (two resistant, four moderately resistant, and three susceptible). However, as noted for the other pairs of trials, most cultivars (13 = 50%) differed by only a single severity category between trials, except for the following four cultivars (15%): Bandera (moderate in 2021, with a mean of 2.3 ± 0.3, and resistant in 2023, with a mean of 1.0 ± 0), Dallas (resistant in 2021, with a mean of 1.0 ± 0, and moderate in 2023, with a mean of 2.7 ± 0.3), Laredo (resistant in 2021, with a mean of 1.0 ± 0, and moderately susceptible in 2023, with a mean of 3.0 ± 0.6), and Minkar (resistant in 2021, with a mean of 1.0 ± 0, and moderate in 2023, with a mean of 2.3 ± 0.3). Of 14 cultivars categorized as resistant to Stemphylium leaf spot (1.0 ± 0) in 2021, the following two were also resistant in 2023: Cocopah and PV-1569. Of the remaining 12 cultivars, nine were moderately resistant (Alcor, Canopus, Colusa, Nembus, PV-1526, PV-1611, PV-1664, Regor, and Tabit), two were moderate (Dallas and Minkar), and one was moderately susceptible (Laredo) in the 2023 trial. Bandera was the only cultivar resistant (1.0 ± 0) in 2023, but not in 2021, when this cultivar was categorized as moderate (2.3 ± 0.3).

Twenty-seven cultivars were included in both the 2022 and 2023 field trials (Fig. 3C), with a significant correlation in mean Stemphylium leaf spot ratings between the two trials (ρ = 0.473; P = 0.013) (Table 1). Of the 27 cultivars, 17 (63%) were in the same category between trials (2 resistant, 11 moderately resistant, and 4 susceptible). Of the remaining 10, seven (26%) differed by one severity category, with the exceptions being Aries (moderately resistant in 2022, with a mean of 1.3 ± 0.3, and moderately susceptible in 2023, with a mean of 3.0 ± 0), Cocopah (susceptible in 2022, with a mean of 4.3 ± 0.9, and resistant in 2023, with a mean of 1.0 ± 0), and Patton (moderate in 2022, with a mean of 2.3 ± 0.3, and susceptible in 2023, with a mean of 5.0 ± 0.6). Of four cultivars categorized as resistant to Stemphylium leaf spot in the 2022 trial, two were also resistant in the 2023 trial (Callisto and Formax), and the following two were moderately resistant: Boxfish (1.7 ± 0.3) and Traverse (1.7 ± 0.3). The following two cultivars were categorized as resistant in 2023 (1.0 ± 0), but not in 2022: Cocopah and PV-1569. PV-1569 was moderately resistant, whereas Cocopah was susceptible. When Cocopah was omitted from the correlation analysis, similar to the 2021 and 2022 trials, the correlation was stronger among the remaining 26 cultivars (ρ = 0.592; P = 0.001) (Table 1).

Based on the ANOVA for Stemphylium leaf spot severity ratings of the 15 cultivars common to all three trials (Fig. 4), there was a significant cultivar main effect (P < 0.001) and a significant trial × cultivar interaction (P < 0.001), but the trial main effect (P = 1.000) and effect of replications nested in trial were not significant (P = 0.196). When Cocopah was omitted from the analysis, the trial × cultivar interaction was no longer significant (P = 0.253), but there was still a significant cultivar main effect (P < 0.001). The trial main effect (P = 1.000) and replications nested in trial remained not significant (P = 0.299).

Fig. 4.
Fig. 4.

Mean severity of Stemphylium leaf spot for 15 spinach cultivars planted during each of the 2021 (A), 2022 (B), and 2023 field trials (C) near Crystal City, TX, USA. Disease severity was rated using a scale of 1 to 10 (1 = no symptoms and 10 = 90%–100% of the canopy with symptoms). Each cultivar was planted in three replicate plots at ∼6.2 million seed/ha. Plots were inoculated with three isolates of Stemphylium vesicarium obtained originally from spinach crops in Texas. Ratings for cultivars are color-coded based on the disease severity category (resistant, moderately resistant, moderate, moderately susceptible, and susceptible) determined using the z-scores calculated for each cultivar in each trial.

Citation: HortScience 59, 1; 10.21273/HORTSCI17373-23

Weather.

Weather conditions generally were cooler and wetter over the duration of the spinach trial in 2021, from planting to the last disease rating, compared with the 2022 and 2023 trials (Table 2). For the 2021 trial, the average daily temperature ranged from 4.4 ± 0.7 (mean ± SE) to 18.7 ± 0.9 °C over the duration of the trial, with an average daily temperature of 11.6 ± 0.8 °C. In contrast, the average daily temperature for the 2022 trial ranged from 5.6 ± 0.8 to 21.0 ± 0.8 °C, with an average of 13.3 ± 0.7 °C. Temperatures overall in the 2023 trial were similar to those of the 2022 trial, with the average daily temperature ranging from 5.8 ± 0.7 to 21.1 ± 0.8 °C, and an average of 13.4 ± 0.7 °C. Temperatures dropped below freezing for 13 d during both the 2021 and 2022 trials; however, there were only 7 d below freezing during the 2023 trial. Average daily humidity ranged from 40.9% ± 2.7% to 86.4% ± 1.5% during the 2021 trial, 32.9% ± 2.2% to 81.1% ± 2.0% during the 2022 field trial, and 34.1% ± 2.3% to 83.2% ± 1.8% during the 2023 trial. Total precipitation (not including irrigation) for the duration of the 2021 trial was 21.1 mm, with rainfall over 8 d compared to a total of 7.1 mm over 7 d for the 2022 trial, and 7.1 mm over 4 d for the 2023 trial.

Table 2.

Weather conditions during three spinach cultivar trials in Texas (2021, 2022, and 2023) in which plants were inoculated with Stemphylium vesicarium, the causal agent of Stemphylium leaf spot.

Table 2.

Weather conditions during the establishment of infection by S. vesicarium in the trials, from the first inoculation with S. vesicarium (19 Jan in 2021 and 18 Jan in both 2022 and 2023) to 1 week after the second inoculation (9 Feb in 2021 and 10 Feb in both 2022 and 2023), were warmest in the 2021 trial and coolest in the 2022 trial. The daily temperature ranged from 8.8 ± 0.8 °C to 22.8 ± 0.9 °C, with an average of 15.8 ± 0.7 °C in the 2021 trial. In contrast, during this period in the 2022 trial, the daily temperature ranged from 3.3 ± 1.0 °C to 17.9 ± 1.2 °C, with an average of 10.6 ± 0.9 °C. Temperatures ranged from 5.8 ± 0.9 °C to 18.8 ± 1.2 °C, with an average of 12.3 ± 1.0 °C over this period during the 2023 trial. During this period, temperatures dropped below freezing only during the 2022 trial over a cumulative 7 d. Average daily humidity during this infection period ranged from 40.1% ± 4.8% to 85.7% ± 2.7% during the 2021 trial, 32.6% ± 3.0% to 79.9% ± 3.2% during the 2022 trial, and 40.9% ± 4.6% to 86.2% ± 2.9% during the 2023 trial. Total precipitation during this period in the 2021 trial was 2.5 mm, which occurred over 3 d, 4.6 mm over 4 d during the 2022 trial, and 7.1 mm over 4 d during the 2023 trial. Overall, the most severe Stemphylium leaf spot symptoms occurred during the 2021 trial, which had the warmest weather during the infection period of the three trials. In contrast, more severe white rust symptoms occurred overall during the 2022 trial compared with the 2021 trial.

Discussion

The primary objective of this study was to identify spinach cultivars with resistance to Stemphylium leaf spot caused by S. vesicarium, the most prevalent species causing this disease in the primary states for baby leaf spinach production in the southern United States (Liu et al. 2020; Spawton et al. 2019). Within each of the three trials, 11% to 27% of the cultivars planted had resistant reactions, and 29% to 48% were moderately resistant. Therefore, commercial spinach cultivars resistant or moderately resistant to S. vesicarium represent a valuable resource for fresh market and processing spinach growers for management of Stemphylium leaf spot. Cultivars susceptible to Stemphylium leaf spot should be avoided in regions with a high risk of Stemphylium leaf spot caused by S. vesicarium, unless there are effective options for fungicide programs and no evidence of fungicide resistance in the local populations of S. vesicarium.

In contrast to this study, Mou et al. (2008) found that none of the 338 USDA NPGS accessions and 22 commercial cultivars tested for resistance to S. botryosum (S. beticola) was completely resistant. Similarly, Shi et al. (2016) found that none of the 265 accessions and 8 cultivars tested was completely resistant to S. beticola, although they identified eight SNPs associated with partial resistance to this species. Only one commercial cultivar, Space, was evaluated by Mou et al. (2008), Shi et al. (2016), and during this study. The cultivar Space was resistant to S. vesicarium, with a resistant rating in the 2021 trial (1.0 ± 0) and moderately resistant rating in the 2022 trial (1.3 ± 0.3) in the Texas trial. Mou et al. (2008) found that the cultivar Space had incidence rates of 70.0% and 48.8% and 3.4% and 2.8% severity of Stemphylium leaf spot caused by S. beticola in each of two trials, respectively. Shi et al. (2016) reported that the cultivar Space had relatively severe Stemphylium leaf spot (8.5%) compared with other spinach entries in that study. Although only one cultivar was common to the three studies, and each of those entailed different environments, spinach entries, and protocols for resistance screening, the contrasting responses of the cultivar Space to inoculation with S. beticola compared to S. vesicarium suggest there may be different genetic factors influencing responses of spinach to these two pathogens that cause Stemphylium leaf spot.

Resistance to pathogenic Stemphylium spp. has been evaluated in other crops. Two major resistance genes (one dominant and one recessive) to leaf spot of lettuce (Lactuca sativa) caused by S. botryosum were identified (Netzer et al. 1985). A single incompletely dominant gene, Sm, was associated with resistance to gray leaf spot of tomato (Lycopersicon esculentum) caused by S. vesicarium (Behare et al. 1991). Both major and minor genes are thought to contribute to quantitative resistance of lentil (Lens culinaris) to Stemphylium blight caused by S. botryosum (Kant et al. 2017; Saha et al. 2010). A major quantitative trait locus for susceptibility to brown spot caused by S. vesicarium was identified in pear (Pyrus spp.) (Cappai et al. 2018). Because spinach cultivars highly resistant to S. vesicarium were identified in this study, with a wide range in disease severity among all cultivars evaluated within each trial, both major and minor genes may be associated with resistance to S. vesicarium in spinach. Shi et al. (2016) and Mou et al. (2008) did not identify any spinach accessions completely resistant to S. beticola, suggesting that resistance to S. beticola may be more quantitative compared with resistance to S. vesicarium in spinach.

Severity of Stemphylium leaf spot caused by S. vesicarium in this Texas study varied across the three trials, with mean ratings of 2.9 ± 0.1 in 2021, 2.1 ± 0.1 in 2022, and 2.5 ± 0.1 in 2023. Weather conditions likely contributed to more severe Stemphylium leaf spot in the 2021 trial than that during the other two trials (du Toit and Ocamb 2023b). Although conditions were the coldest overall in the 2021 trial, this was largely caused by a severe winter storm that occurred in early Feb 2021, just before the plants were rated, outside of which conditions overall were warmer in this trial than those during the other two trials from the first inoculation to 2 weeks after the second inoculation. Daily average temperatures were similar over the entire growing season in each of the 2022 and 2023 trials, but they were lower in the 2022 trial than in the two other trials following inoculations with S. vesicarium. Likewise, the lowest daily average maximum and minimum humidity values were recorded following infection in the 2022 trial compared with the 2021 and 2023 trials. These conditions might account, in part, for less severe Stemphylium leaf spot during the 2022 trial.

Warmer temperatures and higher relative humidity are conducive for Stemphylium leaf spot. Koike et al. (2001) found that S. botryosum (S. beticola) grew at a faster rate on V8 agar medium at 24 °C than at 18 °C. The thermophilic nature of Stemphylium spp. colonizing spinach is, perhaps, exemplified in the difficulty eradicating the fungi from spinach seed with hot water (du Toit and Hernandez-Perez 2005) or steam treatments (du Toit et al. 2018b). Seedborne inoculum of S. beticola remained viable even after treating seed in water heated to 60 °C for 40 min, which killed most of the seed (du Toit and Hernandez-Perez 2005). In spinach seed crops in the mild maritime Pacific Northwest, Stemphylium leaf spot is more prevalent during warmer wet seasons, whereas Cladosporium leaf spot (caused by Cladosporium variabile) is prevalent in cooler wet seasons (du Toit and Ocamb 2023a, 2023b). Losses to S. vesicarium also have been associated with relatively warm temperatures in other crops. For example, S. vesicarium optimally infects pear leaves and fruits at 21 to 23 °C (Montesinos et al. 1995). Conidial concentrations of S. vesicarium in onion fields were positively correlated with the number of days with temperatures >15 °C (Gossen et al. 2021). Conidia production by S. vesicarium increased sooner on onion leaves, with a greater incidence of spore germination, at 25 °C than at lower temperatures (Suheri and Price 2000).

The importance of duration of leaf wetness and relative humidity for conidial germination and disease development has been demonstrated for multiple foliar diseases caused by Stemphylium spp., including S. vesicarium. Isolates of S. vesicarium pathogenic on pear require a film of water on leaves or high relative humidity during periods when leaves are dry for brown spot to occur (Llorente and Montesinos 2002; Montesinos et al. 1995). Infection of onion leaves caused by S. vesicarium increased with a longer period of leaf wetness (up to 24 h) at all temperatures tested (4 to 25 °C) (Suheri and Price 2000) or following rainfall events (Gossen et al. 2021). Similarly, severity of purple blotch of asparagus (Asparagus officinalis) caused by S. vesicarium was positively correlated with rainfall (Falloon et al. 1987). Longer periods of leaf wetness, rainfall, and relative humidity increased the number of lesions caused by S. vesicarium on garlic (Allium sativum) (Basallote-Ureba et al. 1999; Pragdos-Ligero et al. 2003). Mou et al. (2008) speculated that variations in the incidence and severity of Stemphylium leaf spot of spinach caused by S. botryosum (S. beticola) during two trials used to screen cultivars and PIs for resistance were associated with variability in humidity in dew chambers used in that study. Similarly, differences in relative humidity may have impacted the severity of Stemphylium leaf spot across the three spinach trials in this study in Texas, with the most severe disease pressure overall in the 2021 trial, when conditions were humid and warmer after the first inoculation to 1 week after the second inoculation compared with conditions in the other two trials.

Disease pressure in field trials also can be influenced by the specific cultivars or entries evaluated. All cultivars used in the three field trials were chosen by representatives of seed companies, who submitted the seed; therefore, differences among trials in the cultivars evaluated could have contributed overall to differences in Stemphylium leaf spot severity. Fifteen cultivars were common to all three trials, and some cultivars differed significantly in disease severity among trials, as evidenced by the significant cultivar × trial interaction. This could have been caused, in part, by differences in the conditions of plants at the time of rating. For example, the rating of the 2021 trial occurred after a large winter storm that caused some frost damage to plants; therefore, cultivars with moderate resistance could have been difficult to detect with the frost damage. When Cocopah, the cultivar with the most variation among the 3 years, was removed, the cultivar × trial interaction was no longer significant. The severe Stemphylium leaf spot rating of Cocopah in 2022 was attributed to susceptibility to white rust, which likely confounded ratings for the two diseases.

The spinach cultivars evaluated in the 2021 and 2022 trials were also screened for resistance to white rust that resulted from natural infection by A. occidentalis. In the 2021 trial, only 5 of 79 cultivars (6%) did not develop symptoms of white rust, whereas all 87 cultivars in the 2022 trial developed white rust. This corroborates the long-standing hypothesis that multiple genes are responsible for relatively quantitative resistance to white rust in spinach (Bowers 1974; Correll et al. 2011). Previous studies screening cultivars for resistance to white rust found that no cultivar was completely resistant, but some cultivars displayed partial resistance (Brandenberger et al. 1994; Goreta and Leskovar 2006). The quantitative nature of white rust resistance was demonstrated further by the genome-wide association study by Awika et al. (2019), who identified 448 minor alleles associated with the severity of white rust in 267 spinach accessions, and by Shi et al. (2022), who identified nine SNPs associated with white rust resistance during a screening of 346 USDA NPGS accessions.

Although the three field trials in Texas were inoculated with S. vesicarium in this study, the severity of white rust resulting from natural infection was greater than Stemphylium leaf spot in the first two trials: 4.0 ± 0.2 vs. 2.9 ± 0.1 in 2021 and 5.2. ± 0.1 vs. 2.1 ± 0.1 in 2022, respectively. White rust was favored by weather conditions in the Wintergarden area of Texas during these trials, a region used regularly to screen spinach germplasm for white rust resistance. The use of overhead irrigation also provided a conducive environment for both Stemphylium leaf spot and white rust. White rust requires relatively short durations of leaf wetness (as little as 3 h at 12 to 22 °C or 6 to 12 h at higher or lower temperatures) (Sullivan et al. 2002). Although the duration of leaf wetness required to establish Stemphylium leaf spot of spinach has not been studied, S. vesicarium was found to cause lesions on onion leaves after 18 to 24 h of leaf wetness (Shishkoff and Lorbeer 1989), on garlic leaves after 12 to 24 h (Basallote-Ureba et al. 1999), and on pear fruit after more than 6 h (Montesinos et al. 1995). The field in which the Texas spinach trials were performed has been used for spinach field research consecutively since 2017, and has been planted with spinach cultivars highly susceptible to white rust for various studies on the disease; in other words, the inoculum load of A. occidentalis oospores in the field was likely high. The severe white rust observed on some spinach cultivars in the trials confounded the evaluation of those cultivars for their reactions to S. vesicarium. Therefore, applications of metalaxyl were used effectively in the 2023 trial to limit white rust development and facilitate screening spinach cultivars for resistance to S. vesicarium, particularly cultivars highly susceptible to white rust, such as Cocopah.

Overall, white rust was more severe in the 2022 trial than the 2021 trial, in contrast to Stemphylium leaf spot. Unlike S. vesicarium, natural infection of plants by A. occidentalis could have occurred throughout the duration of each trial. Air temperatures generally were higher in the 2022 trial than the 2021 trial. The optimum temperature for white rust development (Sullivan et al. 2002) and zoospore germination by A. occidentalis was demonstrated to be 12 to 18 °C, but zoospores germinated at similar rates at warmer temperatures (16 to 25 °C) when first chilled for 1.5 h at 12 °C (Raabe and Pound 1952). Oospores developed in greater abundance at 28 °C than at 16 °C, and white rust was more severe at 28 °C (Raabe and Pound 1952), suggesting that disease severity can be influenced by whether infections are caused by oospores or zoospores, primarily. White rust development on spinach is often associated with relatively warm days and cool nights that foster dew formation (Raabe and Pound 1952). The slightly warmer conditions in the 2022 trial compared to those in the 2021 trial may have been more conducive for infection by both oospores and zoospores of A. occidentalis. Raabe and Pound (1952) observed that disease spread was slower immediately after periods of rain and high relative humidity. In contrast, Sullivan et al. (2002) found that 84 h of leaf wetness was associated with maximum white rust severity in spinach. Although there was less rain and slightly lower relative humidity in the 2022 trial than in the 2021 trial, the slightly lower relative humidity in the 2022 trial may not have limited the durations of leaf wetness enough to prevent infection by A. occidentalis, especially when combined with the use of overhead irrigation.

Reactions of spinach cultivars to white rust and Stemphylium leaf spot were not correlated significantly in any of the three trials in Texas. Cultivars resistant or moderately resistant to both diseases in at least two trials included Colusa, Kodiak, PV-1569, and PV-1664, whereas cultivars susceptible or moderately susceptible to both diseases included Kona, Lakeside, Magnetic, and Seaside. Cultivars resistant or moderately resistant to white rust but susceptible or moderately susceptible to Stemphylium leaf spot in at least two trials included Hammerhead, whereas cultivars susceptible or moderately susceptible to white rust but resistant or moderately resistant to Stemphylium leaf spot included C2–606, Parakeet, and SV6203VB. When white rust ratings were compared with Stemphylium leaf spot ratings across trials, the only significant correlation was between the white rust ratings in the 2022 trial and Stemphylium leaf spot ratings in the 2021 trial for the 46 cultivars common to both trials (ρ = 0.415; P = 0.004). Oddly, there was no significant correlation between Stemphylium leaf spot ratings in the 2022 trial and white rust ratings in the 2021 (ρ = −0.077; P = 0.612). The overall lack of significant correlations between white rust and Stemphylium leaf spot ratings suggests that genetic resistance to the two diseases is not related. Linkage of resistance has been documented in some spinach cultivars for white rust and certain races of the downy mildew pathogen Peronospora effusa (synonym P. farinosa f. sp. spinaciae) (Brandenberger et al. 1991, 1994). A similar relationship was found in Arabidopsis for resistance to white rust caused by A. candida and downy mildew caused by P. parasitica (Borhan et al. 2001). The apparent independence of genes associated with resistance in spinach to white rust compared to Stemphylium leaf spot caused by S. vesicarium could be beneficial for breeders because resistance to one disease did not appear to be related to susceptibility to the other; in other words, there is greater likelihood that resistance genes to both diseases can be incorporated independently into spinach cultivars. Future research should map the resistance genes to the two diseases by comparing the genetics of cultivars resistant and those susceptible to each disease and determine the number of genes associated with resistance to each disease and how resistance to each disease is inherited.

In conclusion, this study identified spinach cultivars resistant to Stemphylium leaf spot caused by S. vesicarium and spinach cultivars resistant to white rust. The results provide spinach growers with information for selecting resistant cultivars suitable for their regions of production. Resistance to S. vesicarium may be needed, particularly in areas where resistance to FRAC group 11 fungicides has been documented in populations of S. vesicarium pathogenic to spinach (e.g., southern states of spinach production in the United States) (Raid et al. 2018; Spawton et al. 2019). Resistance to white rust may not be needed in areas where the disease is not prevalent (e.g., west coast states in the United States) (Correll et al. 1994, 2011, 2017; Putnam 2020). Populations of S. vesicarium on spinach could develop resistance to fungicides in other FRAC groups, particularly as spinach growers switch to using fungicides with other modes of action to replace the use of fungicides in FRAC group 11, as has been documented in populations of S. vesicarium pathogenic to other crops (e.g., S. vesicarium isolates from pear) with reduced sensitivity to fungicides in FRAC groups 2 (dicarboxamides) (Alberoni et al. 2005) and 11 (Alberoni et al. 2010), and in isolates from onion with reduced sensitivity to fungicides in FRAC groups 2 (Hoepting 2019), 3 (quinone inside inhibitors) (Hoepting et al. 2021a, 2021b), 7 (succinate-dehydrogenase inhibitors), 9 (anilino-pyrimidines), and 11 (Hay et al. 2019, 2021). The ability to select spinach cultivars with resistance to Stemphylium leaf spot caused by S. vesicarium and cultivars with resistance to white rust provides a valuable tool for the management of these important diseases of spinach.

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  • Fig. 1.

    Mean severity of Stemphylium leaf spot caused by Stemphylium vesicarium for each of 79 spinach cultivars evaluated during a field trial in 2021 (A), 87 cultivars evaluated during a field trial in 2022 (B), and 63 cultivars evaluated during a field trial in 2023 (C) near Crystal City, TX, USA. Disease severity was rated using a scale of 1 to 10 (1 = no symptoms and 10 = 90%–100% of the canopy with symptoms). Each cultivar was planted in three replicate plots at ∼6.2 million seed/ha, except for six processing cultivars (denoted with an asterisk) planted in the 2022 trial at ∼1.2 million seed/ha: 308, Baboon, Molokai, Solomon, SV3580VC, and Vancouver. Each plot had a length of 3.0 m and width of 1.6 m. Plants were inoculated with three isolates of S. vesicarium obtained originally from symptomatic spinach crops in Texas. Ratings are color-coded based on the disease severity category of each cultivar (resistant, moderately resistant, moderate, moderately susceptible, and susceptible) determined using the z-scores for mean disease severity in each trial.

  • Fig. 2.

    Mean severity of white rust caused by Albugo occidentalis for each of 79 spinach cultivars planted during a field trial in 2021 (A) and 87 spinach cultivars planted during a field trial in 2022 (B) near Crystal City, TX, USA. Disease severity was rated using a scale of 1 to 10 (1 = no symptoms and 10 = 90%–100% of the canopy with symptoms). Each cultivar was planted in three replicate plots at ∼6.2 million seed/ha, except for six processing cultivars (denoted with an asterisk) planted in 2022 at ∼1.2 million seed/ha: 308, Baboon, Molokai, Solomon, SV3580VC, and Vancouver. Each plot had a length of 3.0 m and width of 1.6 m. White rust developed as a result of natural infection. White rust mean severity ratings are color-coded based on the disease category (resistant, moderately resistant, moderate, moderately susceptible, and susceptible) determined using the z-scores calculated for each cultivar in each trial.

  • Fig. 3.

    Mean severity of Stemphylium leaf spot for 46 spinach cultivars planted during both the 2021 and 2022 field trials (A), 26 cultivars planted during both the 2021 and 2023 field trials (B), and 27 cultivars planted during both the 2022 and 2023 field trials (C) near Crystal City, TX, USA. Disease severity was rated using a scale of 1 to 10 (1 = no symptoms and 10 = 90%–100% of the canopy with symptoms). Each cultivar was planted in three replicate plots at ∼6.2 million seed/ha. Plots were inoculated with three isolates of Stemphylium vesicarium obtained originally from spinach crops in Texas. Ratings for cultivars are color-coded based on the disease severity category (resistant, moderately resistant, moderate, moderately susceptible, and susceptible) determined using the z-scores calculated for each cultivar in each trial.

  • Fig. 4.

    Mean severity of Stemphylium leaf spot for 15 spinach cultivars planted during each of the 2021 (A), 2022 (B), and 2023 field trials (C) near Crystal City, TX, USA. Disease severity was rated using a scale of 1 to 10 (1 = no symptoms and 10 = 90%–100% of the canopy with symptoms). Each cultivar was planted in three replicate plots at ∼6.2 million seed/ha. Plots were inoculated with three isolates of Stemphylium vesicarium obtained originally from spinach crops in Texas. Ratings for cultivars are color-coded based on the disease severity category (resistant, moderately resistant, moderate, moderately susceptible, and susceptible) determined using the z-scores calculated for each cultivar in each trial.

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Supplementary Materials

Kayla A. Spawton Department of Plant Pathology, Washington State University Northwestern Washington Research and Extension Center, 16650 State Route 536, Mount Vernon, WA 98273, USA

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Larry A. Stein Department of Horticultural Sciences, Texas A&M Agrilife Research and Extension Center, 1619 Garner Field Road, Uvalde, TX 77801, USA

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Lindsey J. du Toit Department of Plant Pathology, Washington State University Northwestern Washington Research and Extension Center, 16650 State Route 536, Mount Vernon, WA 98273, USA

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Contributor Notes

This work was funded by the Texas Wintergarden Spinach Producers’ Board, Alfred Christianson Distinguished Professor Endowment, Everette J. and Helen G. Kreizinger Endowed Scholarship, Judy and Floyd Rogers Fellowship from the Seattle Chapter of the Achievement Rewards for College Scientists Foundation (ARCS), and Hatch Project No. WNP0010 of the Washington State University College of Agricultural, Human, and Natural Resource Sciences.

We thank the Texas Wintergarden Spinach Producers for planting and maintaining the field trials, especially Ed Ritchie and Paige Ritchie of Tiro Tres Farms, Jimmy Crawford of Crawford Farms, and their respective teams. We thank Mike Phillips for his technical assistance with inoculating the trials, and Michael Derie, Tomasita Villaroel, and Paul Morgan of the Vegetable Seed Pathology program at Washington State University for additional technical support. We thank Kai Battenberg for assistance with data visualization and Beiquan Mou and Sanjaya Gyawali for providing valuable feedback regarding the manuscript.

L.d.T. is the corresponding author. E-mail: dutoit@wsu.edu.

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  • Fig. 1.

    Mean severity of Stemphylium leaf spot caused by Stemphylium vesicarium for each of 79 spinach cultivars evaluated during a field trial in 2021 (A), 87 cultivars evaluated during a field trial in 2022 (B), and 63 cultivars evaluated during a field trial in 2023 (C) near Crystal City, TX, USA. Disease severity was rated using a scale of 1 to 10 (1 = no symptoms and 10 = 90%–100% of the canopy with symptoms). Each cultivar was planted in three replicate plots at ∼6.2 million seed/ha, except for six processing cultivars (denoted with an asterisk) planted in the 2022 trial at ∼1.2 million seed/ha: 308, Baboon, Molokai, Solomon, SV3580VC, and Vancouver. Each plot had a length of 3.0 m and width of 1.6 m. Plants were inoculated with three isolates of S. vesicarium obtained originally from symptomatic spinach crops in Texas. Ratings are color-coded based on the disease severity category of each cultivar (resistant, moderately resistant, moderate, moderately susceptible, and susceptible) determined using the z-scores for mean disease severity in each trial.

  • Fig. 2.

    Mean severity of white rust caused by Albugo occidentalis for each of 79 spinach cultivars planted during a field trial in 2021 (A) and 87 spinach cultivars planted during a field trial in 2022 (B) near Crystal City, TX, USA. Disease severity was rated using a scale of 1 to 10 (1 = no symptoms and 10 = 90%–100% of the canopy with symptoms). Each cultivar was planted in three replicate plots at ∼6.2 million seed/ha, except for six processing cultivars (denoted with an asterisk) planted in 2022 at ∼1.2 million seed/ha: 308, Baboon, Molokai, Solomon, SV3580VC, and Vancouver. Each plot had a length of 3.0 m and width of 1.6 m. White rust developed as a result of natural infection. White rust mean severity ratings are color-coded based on the disease category (resistant, moderately resistant, moderate, moderately susceptible, and susceptible) determined using the z-scores calculated for each cultivar in each trial.

  • Fig. 3.

    Mean severity of Stemphylium leaf spot for 46 spinach cultivars planted during both the 2021 and 2022 field trials (A), 26 cultivars planted during both the 2021 and 2023 field trials (B), and 27 cultivars planted during both the 2022 and 2023 field trials (C) near Crystal City, TX, USA. Disease severity was rated using a scale of 1 to 10 (1 = no symptoms and 10 = 90%–100% of the canopy with symptoms). Each cultivar was planted in three replicate plots at ∼6.2 million seed/ha. Plots were inoculated with three isolates of Stemphylium vesicarium obtained originally from spinach crops in Texas. Ratings for cultivars are color-coded based on the disease severity category (resistant, moderately resistant, moderate, moderately susceptible, and susceptible) determined using the z-scores calculated for each cultivar in each trial.

  • Fig. 4.

    Mean severity of Stemphylium leaf spot for 15 spinach cultivars planted during each of the 2021 (A), 2022 (B), and 2023 field trials (C) near Crystal City, TX, USA. Disease severity was rated using a scale of 1 to 10 (1 = no symptoms and 10 = 90%–100% of the canopy with symptoms). Each cultivar was planted in three replicate plots at ∼6.2 million seed/ha. Plots were inoculated with three isolates of Stemphylium vesicarium obtained originally from spinach crops in Texas. Ratings for cultivars are color-coded based on the disease severity category (resistant, moderately resistant, moderate, moderately susceptible, and susceptible) determined using the z-scores calculated for each cultivar in each trial.

 

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