Abstract
Magnolias (Magnolia sp.) are economically important woody ornamental plants; however, plant damage associated with frost and powdery mildew (Microsphaera alni and Phyllactinia corylea) disease is a major production challenge. To understand the tree architecture and powdery mildew resistance, 26 yellow-flowering magnolias (Magnolia sp.) were evaluated in McMinnville, TN, USA (USDA Plant Hardiness Zone 6b). One-year-old containerized trees were planted in a field plot during Mar 2006, with 4.6-m plant-to-plant and 3.7-m row-to-row spacing. The experiment was a completely randomized block design with three single-plant replications. Plant height and canopy diameter were measured on Dec 2016 and Feb 2018, and the apical dominance ratio (i.e., indicating tree architecture) was calculated by dividing the height by the canopy diameter. Plants were evaluated for powdery mildew severity and defoliation using a scale of 0% to 100% of the total plant canopy affected or defoliated, respectively, from Aug to Oct of 2016 and 2017. The area under the disease progress curve (AUDPC) was calculated for the evaluation period of each year. The plant apical dominance ratio ranged from 1 to 3, with ‘Gold Cup’ and ‘Sun Spire’ having the highest value, and ‘Lois’, ‘Gold Star’, ‘Golden Gala’, ‘Solar Flair’, ‘Stellar Acclaim’, ‘Sun Ray’, ‘Sunburst’, and ‘Sundance’ having the lowest value (i.e., relatively round shape). Of the 26 cultivars, Sundance, Sun Spire, Sun Ray, and Gold Cup had the lowest powdery mildew severity (10% to 33% in 2016 and 40% to 60% in 2017), AUDPC, and defoliation. Cultivars Anilou, Gold Star, Golden Pond, Golden Rain, Golden Sun, Green Bee, Honey Liz, Judy Zuk, Koban Dori, Lois, Solar Flair, Stellar Acclaim, and Yellow Bird were highly susceptible to powdery mildew (>80% disease severity) and had the highest AUDPC values. Results of this research may aid breeders, nursery producers, and landscapers when selecting yellow-flowering magnolia cultivars with desirable tree architecture and resistance to powdery mildew.
Magnolias (Magnolia sp.) are deciduous or evergreen flowering trees widely cultivated throughout the United States (Zagórska-Marek 2011). In 2019, approximately 1,100,000 magnolias were sold in the United States; furthermore, approximately 10% of nurseries that produce magnolia are located in Tennessee (National Agricultural Statistics Service 2020). They are valued for showy, sometimes fragrant flowers with various color options, including pink, yellow, orange, purple, pure white, creamy white, and blue–green (Callaway 1994). Recently, yellow-flowering magnolias have gained popularity because of their unique color palette (Knox 2002; Wojtania et al. 2020). Yellow-flowering magnolias bloom in spring from mid-March to early April (Fare 2011). Although the demand for yellow-flowering selections of magnolia has increased, their susceptibility to frost damage and disease issues are major production challenges that need to be addressed (Tubesing 1998).
Powdery mildew is one of the most destructive diseases of yellow-flowering magnolia (Cho et al. 2014; Glawe 2003). The disease is caused by fungal pathogens Microsphaera alni and Phyllactinia corylea (Hagan 2001; Knox et al. 2012). These are obligate biotrophic pathogens. Powdery mildew in magnolia develops when days are warm and dry and nights are cool (Smith et al. 1996). The disease first appears on the adaxial leaf surface as circular to irregular white patches that consist of mycelial and conidial growth of the fungus. As the fungal colonization progresses, the leaves become covered in white mildew and develop brown lesions and necrosis, leading to leaf curling at the site of infection and premature defoliation (Agrios 1997). Powdery mildew can reduce the aesthetic value of the plant as well as flower numbers and quality. Although fungicide application is the most common method of controlling powdery mildew (Knox et al. 2012), this is a tedious and expensive method. Even though planting resistant cultivars can be a cost-effective and sustainable strategy for disease management, no breeding programs are currently developing powdery mildew-resistant magnolia cultivars. Fare (2017) screened yellow-flowering magnolia cultivars in Tennessee and found variations in their growth and powdery mildew resistance. This study reported findings from a single-year evaluation. Because powdery mildew severity is highly dependent on weather conditions (Asalf et al. 2013; Legler et al. 2012; Marçais and Desprez-Loustau 2014), a multiyear evaluation would validate the conclusions made by Fare (2017).
Yellow-flowering magnolia has been bred since the 1950s in the United States (Fare 2011; Fare 2017). Taxa that have been used to develop yellow-flowering magnolia cultivars are cucumber magnolia (M. acuminata), yulan magnolia (M. denudata), yellow cucumber magnolia (M. acuminata var. subcordata), kobus magnolia (M. kobus), and saucer magnolia (Magnolia ×soulangiana) (Dirr 2009; Knox 2001). Cultivars bred from M. acuminata are more cold-hardy and can be grown in a wide range of soil pH levels and soil types (Callaway 1994). Cultivars derived from M. denudata or M. liliflora offer yellow flower color with trees of different sizes and shapes (Fare 2017). In later years, numerous yellow-flowering magnolia cultivars with varying shape, sizes, and flower colors were developed (Held 2004; Knox 2001; Knox et al. 2012). We defined the tree apical dominance ratio (ADR) as the ratio of the plant height to the canopy diameter, indicating the plant architecture. The ADR may vary substantially among cultivars because of the numerous species that have been used to breed yellow-flowering magnolia. Because the ADR is an important criterion when selecting woody ornamental plants for landscapes (Pallardy 2010), defining the ADR of yellow-flowering magnolia cultivars may promote their utilization by landscape contractors and architects.
Understanding the individual tree ADR of different cultivars and their resistance to powdery mildew would help during the selection of suitable cultivars for landscaping and allow better preparation for management action. The objective of this study was to evaluate the ADR and powdery mildew resistance or susceptibility of yellow-flowering magnolia cultivars in McMinnville, TN, USA.
Materials and Methods
Twenty-six yellow-flowering magnolia cultivars (Table 1) with hybridization details (Lobdell 2021) were evaluated for powdery mildew severity at the Otis L. Floyd Nursery Research Center in McMinnville, TN, USA, which is located at the border of the United States Department of Agriculture Hardiness Zones 6 and 7 (lat. 35.7°N, long. 85.8°W). The materials and methods used for this research were similar to those described by Fare (2017). Bare-rooted yellow-flowering magnolia cultivars were purchased and grown in 11.4-L (#3) or 18.9-L (#5) nursery containers for 1 year. In Mar 2006, 1-year-old containerized plants were transplanted to the evaluation plots with Waynesboro silt loam soil at the. Plant-to-plant and row-to-row spacing were 4.6 m and 3.7 m, respectively. Plants were arranged in a completely randomized block design with three single-plant replications. Branches approximately 0.6 m above the soil line were pruned from the trunk at planting. In Mar 2007, several cultivars were killed or suffered severe dieback because of unseasonably warm temperatures followed by a hard freeze. Maximum and minimum temperatures and total rainfall were monitored during the evaluation seasons using a weather station (WatchDog 2700; Spectrum Technologies, Aurora, IL, USA) (Table 2).
List of yellow-flowering magnolia (Magnolia sp.) cultivars that were evaluated in McMinnville, TN, USA.
Weather variables recorded in 2015 and 2016, in McMinnville, TN, USA.
Plant height and canopy diameter were measured in Dec 2016 and Feb 2018. Plant height was measured from the ground to the tallest node. Canopy diameter was measured at the widest point and perpendicular to the widest point, and an average diameter was calculated for each plant as follows: [(canopy diameter at widest point + canopy diameter perpendicular) ÷ 2]. The plant ADR was calculated by dividing the plant height by the canopy diameter. Cultivars were evaluated to determine the powdery mildew percentage coverage of the total foliage area using a scale of 0% to 100% on 29 Aug, 21 Sep, and 5 Oct in 2016, and on 29 Aug, 29 Sep, and 5 Oct in 2017. The powdery mildew occurred naturally. Season-long disease progress was calculated using the following area under the disease progress curve (AUDPC) formula: ∑{[(xi + xi−1)/2](ti − ti−1)}, where xi is the powdery mildew severity rating at each evaluation time and (ti − ti−1) is the number of days between evaluations. The percent defoliation was also recorded using a scale of 0% to 100% foliage affected at the same time when powdery mildew was evaluated.
A repeated-measure analysis of variance (ANOVA) using SAS software 9.4 (SAS Inc., Cary, NC, USA) was performed to determine the interactive effects of year × cultivar on powdery mildew severity, AUDPC, defoliation, and ADR. When the interaction was significant, data were separately analyzed according to the evaluation year by performing a one-way ANOVA using SAS 9.4. The general linear model procedure (PROC GLM) was used to partition the variance of powdery mildew severity, AUDPC, defoliation, and ADR attributable to cultivars. The data satisfied the assumption of normal distribution and homogeneity. When the effects were significant, the post hoc Fisher’s least significant difference test was performed to compare means (α = 0.05). Pearson’s correlation coefficient (r) regression analysis was performed to determine the relationships between disease severity and ADR.
Results
Powdery mildew appeared naturally in all cultivars, and there were significant interactive effects of year × cultivar on powdery mildew severity and AUDPC (Table 3). Disease severity was significantly higher in 2016 than 2017. Similarly, AUDPC was significantly higher in 2016 compared with 2017. Because there was a significant year × cultivar interaction, data were analyzed separately for each year. There were significant differences in powdery mildew severity as well as AUDPC among cultivars in both years. In 2016, powdery mildew severity ranged from a minimum of 38% for ‘Carlos’ to a maximum of 100% for ‘Green Bee’ (Fig. 1). Other cultivars that had disease severity similar to that of Carlos were Sundance, Sun Ray, Sun Spire, Gold Cup, and Sunburst, which had 40%, 43%, 56%, 60%, and 63% powdery mildew coverage, respectively, in 2016. Cultivars, Anilou, Banana Split, Gold Star, Golden Gala, Golden Pond, Golden Rain, Golden Sun, Goldfinch, Honey Liz, Judy Zuk, Koban Dori, Lois, Petit Chicon, Solar Flair, Stellar Acclaim, Sunsation, Yellow Bird, and Yellow Lantern had the highest powdery mildew severity (>73%). In 2016, the AUDPC was lowest for ‘Sun Spire’, ‘Sundance’, ‘Carlos’, ‘Sun Ray’, and ‘Gold Cup’ (Table 4). The highest AUDPC was observed for ‘Anilou’, ‘Stellar Acclaim’, ‘Gold Star’, ‘Golden Rain’, ‘Green Bee’, ‘Honey Liz’, ‘Koban Dori’, ‘Solar Flair’, and ‘Sunsation’. In 2017, powdery mildew disease severity ranged from a minimum of 10% to 35% for ‘Sundance’, ‘Banana Split’, ‘Gold Cup’, ‘Sun Ray’, and ‘Sun Spire’ to a maximum of 65% to 96% for ‘Anilou’, ‘Carlos’, ‘Gold Star’, ‘Golden Gala’, ‘Goldfinch’, ‘Golden Pond’, ‘Golden Rain’, ‘Golden Sun’, ‘Green Bee’, ‘Honey Liz’, ‘Judy Zuk’, ‘Koban Dori’, ‘Lois’, ‘Solar Flair’, ‘Stellar Acclaim’, ‘Sunburst’, and ‘Yellow Bird’ (Fig. 2). ‘Elizabeth’, ‘Petit Chicon’, ‘Sunsation’, and ‘Yellow Lantern’ had moderate powdery mildew severity (53% to 55%). The lowest AUDPC was observed for ‘Sundance’, ‘Sun Spire’, ‘Banana Split’, ‘Sun Ray’, and ‘Gold Cup’ (Table 4). The highest AUDPC was observed for cultivars Anilou, Carlos, Gold Star, Golden Pond, Golden Rain, Golden Sun, Golden Gala, Green Bee, Honey Liz, Judy Zuk, Koban Dori, Lois, Solar Flair, Stellar Acclaim, and Sunburst.
Mean (±SE) powdery mildew severity (% of foliage covered) of yellow-flowering magnolia (Magnolia sp.) cultivars in McMinnville, TN, USA, evaluated on 5 Oct 2016. Values are the means of three single-plant replicates. Means followed by different lowercase letters above the bars are significantly different (P ≤ 0.05). A one-way analysis of variance was performed and means were compared using Fisher’s least significant difference test with an α = 0.05.
Citation: HortScience 58, 4; 10.21273/HORTSCI17036-22
Mean (±SE) powdery mildew severity (% of foliage covered) of yellow-flowering magnolia (Magnolia sp.) cultivars in McMinnville, TN, USA, evaluated on 5 Oct 2016. Values are the means of three single-plant replicates. Means followed by different lowercase letters above the bars are significantly different (P ≤ 0.05). A one-way analysis of variance was performed and means were compared using Fisher’s least significant difference test with an α = 0.05.
Citation: HortScience 58, 4; 10.21273/HORTSCI17036-22
Mean (±SE) powdery mildew severity (% of foliage covered) of yellow-flowering magnolia (Magnolia sp.) cultivars in McMinnville, TN, USA, evaluated on 5 Oct 2016. Values are the means of three single-plant replicates. Means followed by different lowercase letters above the bars are significantly different (P ≤ 0.05). A one-way analysis of variance was performed and means were compared using Fisher’s least significant difference test with an α = 0.05.
Citation: HortScience 58, 4; 10.21273/HORTSCI17036-22
Mean (±SE) powdery mildew severity (% of foliage covered) of yellow-flowering magnolia (Magnolia sp.) cultivars in McMinnville, TN, USA, evaluated on 5 Oct 2017. Values are the means of three single-plant replicates. Means followed by different lowercase letters above the bars are significantly different (P ≤ 0.05). A one-way analysis of variance was performed and means were compared using Fisher’s least significant difference test with an α = 0.05.
Citation: HortScience 58, 4; 10.21273/HORTSCI17036-22
Mean (±SE) powdery mildew severity (% of foliage covered) of yellow-flowering magnolia (Magnolia sp.) cultivars in McMinnville, TN, USA, evaluated on 5 Oct 2017. Values are the means of three single-plant replicates. Means followed by different lowercase letters above the bars are significantly different (P ≤ 0.05). A one-way analysis of variance was performed and means were compared using Fisher’s least significant difference test with an α = 0.05.
Citation: HortScience 58, 4; 10.21273/HORTSCI17036-22
Mean (±SE) powdery mildew severity (% of foliage covered) of yellow-flowering magnolia (Magnolia sp.) cultivars in McMinnville, TN, USA, evaluated on 5 Oct 2017. Values are the means of three single-plant replicates. Means followed by different lowercase letters above the bars are significantly different (P ≤ 0.05). A one-way analysis of variance was performed and means were compared using Fisher’s least significant difference test with an α = 0.05.
Citation: HortScience 58, 4; 10.21273/HORTSCI17036-22
Main and interactive effects of year and cultivar of yellow-flowering magnolia (Magnolia sp.) on powdery mildew severity, area under the disease progress curve (AUDPC), and defoliation.
Mean (±SE) area under the disease progress curve (AUDPC) and defoliation caused by powdery mildew of yellow-flowering magnolia (Magnolia sp.) cultivars in McMinnville, TN, USA.
Because there was no year × cultivar interaction (Table 3), defoliation values were pooled across evaluation years. Defoliation was significantly higher in 2017 than in 2016. There was a significant difference in defoliation among cultivars (Table 4). ‘Goldfinch’ and ‘Solar Flair’ had the highest defoliation (>80%). ‘Banana Split’, ‘Carlos’, ‘Elizabeth’, ‘Gold Cup’, ‘Gold Star’, ‘Golden Gala’, ‘Golden Rain’, ‘Golden Sun’, ‘Judy Zuk’, ‘Lois’, ‘Petit Chicon’, ‘Sun Spire’, ‘Sunburst’, ‘Sundance’, ‘Sunsation’, ‘Yellow Bird’, and ‘Yellow Lantern’ exhibited the lowest defoliation rate (<15%). There was also a difference in defoliation between years (F = 5.27; P = 0.024), with significantly higher defoliation in 2017 (25.1%) than in 2016 (17.6%) when pooled across cultivars.
There was no interactive effect of year × cultivar on ADR (F = 0.18; P = 1.000); therefore, pooled ADR values are presented. There was a significant cultivar effect on ADR (Fig. 3). The ADR ranged from 1 to 3 among cultivars; Gold Cup and Sun Spire had the highest value and Lois had the lowest value. Cultivars Gold Star, Golden Gala, Solar Flair, Stellar Acclaim, Sun Ray, Sunburst, and Sundance, had ADRs similar to that of Lois. We did not find a correlation between powdery mildew severity and ADR (r = 015 and P = 0.946 in 2016; r = −0.148 and P = 0.245 in 2017).
Mean (±SE) apical dominance ratio of yellow-flowering magnolia (Magnolia sp.) cultivars in McMinnville, TN, USA. Values are the means of three single-plant replicates. Means followed by different lowercase letters above the bars are significantly different (P ≤ 0.05). A one-way analysis of variance was performed and means were compared using Fisher’s least significant difference test with an α = 0.05. Because there was no interactive effect of year × cultivar, values were pooled across the evaluation years. Plant height and canopy diameter were measured in Dec 2016 and Feb 2018, and the apical dominance ratio was calculated by dividing the height by the canopy diameter.
Citation: HortScience 58, 4; 10.21273/HORTSCI17036-22
Mean (±SE) apical dominance ratio of yellow-flowering magnolia (Magnolia sp.) cultivars in McMinnville, TN, USA. Values are the means of three single-plant replicates. Means followed by different lowercase letters above the bars are significantly different (P ≤ 0.05). A one-way analysis of variance was performed and means were compared using Fisher’s least significant difference test with an α = 0.05. Because there was no interactive effect of year × cultivar, values were pooled across the evaluation years. Plant height and canopy diameter were measured in Dec 2016 and Feb 2018, and the apical dominance ratio was calculated by dividing the height by the canopy diameter.
Citation: HortScience 58, 4; 10.21273/HORTSCI17036-22
Mean (±SE) apical dominance ratio of yellow-flowering magnolia (Magnolia sp.) cultivars in McMinnville, TN, USA. Values are the means of three single-plant replicates. Means followed by different lowercase letters above the bars are significantly different (P ≤ 0.05). A one-way analysis of variance was performed and means were compared using Fisher’s least significant difference test with an α = 0.05. Because there was no interactive effect of year × cultivar, values were pooled across the evaluation years. Plant height and canopy diameter were measured in Dec 2016 and Feb 2018, and the apical dominance ratio was calculated by dividing the height by the canopy diameter.
Citation: HortScience 58, 4; 10.21273/HORTSCI17036-22
Discussion
Powdery mildew patches were initially observed in the adaxial leaf surface of yellow-flowering magnolias in mid Aug, which rapidly developed and covered leaf surfaces by the end of Sep or early Oct in susceptible cultivars. The weather during Aug to Oct in Tennessee, which is characterized by warm, dry days and cool nights, is ideal for spore germination and powdery mildew development (Smith et al. 1996). When a large portion of the foliage was covered by powdery mildew in susceptible cultivars during fall, the disease reduced the aesthetic value of the plants.
Yellow-flowering magnolia cultivars varied in powdery mildew resistance or susceptibility and season-long AUDPC. Of the 26 cultivars, Sundance, Sun Spire, Sun Ray, and Gold Cup demonstrated the lowest powdery mildew severity and AUDPC in both years. However, they were not completely free of powdery mildew; a portion of foliage (10% to 33% in 2016 and 40% to 60% in 2017) was covered by powdery mildew, indicating moderate resistance. Similar to our observation, cultivars Sundance, Sun Spire, and Sun Ray had the lowest powdery mildew during the 2015 evaluation by Fare (2017). Fare (2017) observed the lowest powdery mildew in additional cultivars, such as Banana Split, Carlos, Elizabeth, Golden Gala, Golden Pond, Golden Sun, Goldfinch, Judy Zuk, Lois, Solar Flair, and Yellow Lantern. Surprisingly, we observed the highest powdery mildew severity in some of those cultivars, such as Golden Gala, Golden Pond, Golden Sun, Goldfinch, Judy Zuk, Lois, Petit Chicon, Solar Flair, and Yellow Lantern during years 2016 and 2017. In brief, a greater number of cultivars demonstrated resistance to powdery mildew during the 2015 evaluation than during 2016 and 2017. We observed higher disease severity and disease progress in 2016 than in 2017; this was likely associated with weather variability (Grove 1991; Marçais and Desprez-Loustau 2014; Schnathorst 1965). Total rainfall in 2017 (171.3 cm) was higher than that in 2016 (116.3 cm). The excessive rainfall in 2017 might have washed off the spores and damaged the mycelium on the leaf surface (Jarvis et al. 2002; Marçais and Desprez-Loustau 2014). Dry conditions are necessary for conidia to release into the atmosphere (Glawe 2008; Jarvis et al. 2002), and a “moderate” level of growing season precipitation (70–80 mm per month) favors the germination (Marçais and Desprez-Loustau 2014).
The yellow-flowering magnolia cultivars evaluated during this trial was bred for flower color and other important horticultural traits such as cold-hardiness and adaptability to broader range of soil conditions (Callaway 1994; Fare 2017; Knox 2001), but not specifically for powdery mildew resistance. Accordingly, these moderately resistant cultivars may have inherited resistance, by chance, from their parental lines. Even though the exact mechanisms of the resistance or moderate resistance to powdery mildew are not clear, leaf orientation, cuticle thickness, and other host defense mechanisms might be responsible for developing resistance (Agrios 1997; Jhooty 1965).
‘Sundance’ was developed by crossing M. acuminata with M. denudata, and ‘Sun Ray’ was derived as an induced polyploid of ‘Sundance’ (Lobdell 2021; Magnolia Society International 2020). These two cultivars exhibited the least powdery mildew severity and disease progress. Interestingly, the other cultivars that were derived from the same crosses were highly susceptible to powdery mildew. For example, although cultivars Elizabeth, Golden Gala, Golden Pond, Golden Sun, and Petit Chicon were derived from M. acuminata × M. denudata, they were completely covered by powdery mildew (up to 90%). Furthermore, ‘Sun Spire’, which was created by M. ×brooklynensis ‘Woodsman’ × ‘Elizabeth’, was moderately resistant to powdery mildew; however, ‘Sunsation’, which is a cross of those same parental lines, was highly susceptible. It is possible that one or both the parents had resistant genes that were inherited by some of the progeny during hybridization, but not of others. A few cultivars had variations in powdery mildew coverage in different years. For example, ‘Carlos’ had the lowest powdery mildew severity (38%) and AUDPC in 2016, but severe powdery mildew (82%) and high AUDPC in 2017. Likewise, ‘Banana Split’ had minor powdery mildew severity (16%) and low AUDPC in 2017, but it was highly susceptible to powdery mildew in 2016, with 76% plant canopy coverage. Both cultivars had 20% plant canopy coverage by powdery mildew during the evaluation in 2015 by Fare (2017).
The tree form is one of the five primary elements of design that landscape architects use to construct a unified landscape. Because some yellow-flowering magnolia cultivars have a rounded canopy (height-to-canopy diameter ratio of ∼1.5) and others have a narrow oval canopy (height-to-canopy diameter ratio of ∼3), yellow-flowering magnolias have broad landscape applications. Cultivars with round canopies and moderate powdery mildew resistance include Sun Ray and Sundance, whereas Gold Cup and Sun Spire have narrow oval canopies and moderate powdery mildew resistance.
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