HORTSCIENCE 39(1):161–162. 2004. more prevalent and severe in areas with high relative humidity and periodic drought condi- tions. Water-stressed are usually the fi rst Screening for Powdery Mildew to show symptoms of powdery mildew disease (Agrios, 1997). Resistance in Although variation for resistance to pow- 1 dery mildew has been noted (Armitage, 1997; Kimberly H. Krahl DiSabato-Aust, 1998), no controlled study has Department of Landscape Architecture and Horticulture, Temple University, been conducted to evaluate lungwort species 480 Meetinghouse Road, Ambler, PA 19002 and for resistance to powdery mildew. If genetic resistance to powdery mildew can be Additional index words. lungwort, Bethlehem sage, powdery mildew disease, Pulmonaria identifi ed in lungwort, the potential exists to angustifolia, Pulmonaria longifolia, Pulmonaria offi cinalis, Pulmonaria rubra, Pulmonaria develop new cultivars with powdery mildew saccharata resistance. Abstract. A screening technique was developed for studying resistance to powdery mildew disease in 25 diverse Pulmonaria L. species and cultivars. Healthy Pulmonaria plants were Materials and Methods inoculated by drawing naturally infected of P. angustifolia ‘Blaues Meerʼ across the Twenty-fi ve lungwort cultivars and selec- abaxial surface of three healthy, mature leaves per test . Inoculated leaves were rated tions were screened for resistance to powdery for powdery mildew infection using a scale of 0–5, where 0 = no visible sign of infection, mildew in the Temple Univ. greenhouse in 1 = 1% to 20%; 2 = 20% to 40%; 3 = 40% to 60%; 4 = 60% to 80%; 5 = 80% to 100% Ambler, Pa., during Summer 2001. All plants of surface covered with white mycelial growth. Each genotype was inoculated and were grown in 15-cm-diameter plastic pots in a evaluated four times. The data revealed a wide and continuous range of variability for soilless medium (ProMix B, Premier Horticul- powdery mildew disease incidence in the 25 lungwort genotypes that may be indicative ture, Quebec, Canada) in a completely random of quantitative resistance. The majority of lungwort genotypes exhibited low levels of design. Plants were watered as needed with a resistance to powdery mildew. Four cultivars (P. hybrid ‘Spilled Milkʼ, P. hybrid ‘Ex- 120 mg·L–1 N solution of 20–10–20 soluble caliberʼ, P. rubra ‘Redstartʼ, and P. rubra ‘David Wardʼ) and one selection (P. longifolia fertilizer. Plants of P. angustifolia ‘Blaues ssp. cevennensis) exhibited high levels of resistance to powdery mildew. Since Pulmonaria Meerʼ were maintained separately in the species intercross readily, these genotypes may be useful in the future development of new greenhouse and allowed to develop powdery powdery mildew resistant Pulmonaria cultivars. mildew disease naturally. Heavily infected leaves of P. angustifolia ‘Blaues Meerʼ were Lungworts are outstanding spring-bloom- moisture, good drainage, and partial shade. used to inoculate test plants. Three test plants ing ornamental plants native to Europe and However, many lungwort cultivars and selec- per genotype were inoculated by gently draw- Asia belonging to the genus Pulmonaria. While tions are quite susceptible to powdery mildew ing naturally infected leaves of P. angustifolia these excellent plants have been utilized in disease. ‘Blaues Meerʼ across the abaxial surface of European and Asian gardens for many years, Powdery mildews are among the most three healthy, mature leaves (total of nine the American gardening public has become common and widespread of the fungal plant leaves inoculated each test date). After 3 fully aware of the outstanding ornamental diseases, affecting an extremely wide range of weeks, inoculated plants were evaluated for qualities of Pulmonaria species and cultivars plants, from grasses to tree species. Powdery powdery mildew development. Development fairly recently. Lungworts brighten the spring mildew is caused by many different species of of whitish mycelial growth on the leaf surface garden with their blue, pink, coral-red, or white fungi belonging to the Erysiphaceae family. was defi ned as powdery mildew infection. In- fl owers. Although lungworts provide attractive The species of fungus causing powdery mildew oculated leaves were rated for powdery mildew early fl oral color in the spring garden, they are disease in lungworts has yet to be identifi ed. infection using a scale of 0–5, where 0 = no grown primarily for their ornamental foliage. Powdery mildew fungi are obligate polycy- visible sign of infection; 1 = 1% to 20%; 2 = Many lungwort species and cultivars sport foli- clic parasites, overwintering as cleistothecia 20% to 40%; 3 = 40% to 60%; 4 = 60% to 80%; age that is dramatically spotted and splotched on living or dead plant tissue. Powdery mil- 5 = 80% to 100% of leaf surface covered with with silver and white. Lungworts are excel- dew disease is typifi ed by the appearance of white mycelial growth. Three different plants lent, easily grown shady garden groundcovers, patches of whitish mycelial growth on plant of each or selection were treated and lighting up darker corners of the garden with surfaces. Heavily infected plants can become evaluated four times (four replications) during their variously spotted and blotched foliage entirely covered with the whitish “powder” of Summer 2001. throughout the growing season (Lovejoy, 1993; thick mycelial growth. Not only does powdery Mean ratings for powdery mildew resis- Mathew, 1982). Although there are ≈12 species mildew disease greatly decrease the ornamental tance were analyzed using Proc ANOVA, of Pulmonaria, only four species are commonly value of affected plants, but it also has detri- with multiple comparisons determined using used horticulturally: P. angustifolia, P. longi- mental physiological effects. Infected plants Duncanʼs multiple range test (SAS Institute, folia, P. rubra, and P. saccharata. Lungwort may exhibit dwarfi ng and stunting, redden- Cary, N.C.). Spearmanʼs correlation coef- species hybridize freely and many of the most ing and curling of leaves, and deformation of fi cients were calculated to assess consistency popular cultivars are presumed to be interspe- fl ower buds (Agrios, 1997). Powdery mildew of genotype rank order over testing dates. cifi c hybrids (Armitage, 1997). decreases photosynthesis due to the thick felt Lungworts are generally quite tough produced by intertwining fungal mycelia on Results and Discussion garden plants, thriving when provided with leaf surfaces and inhibits plant growth due to a few simple cultural requirements: adequate withdrawal of plant storage food by the fungus Analysis of variance revealed signifi cant (Agrios, 1997). differences for resistance to powdery mildew Powdery mildew spores germinate under among the 25 lungwort genotypes (Table 1). conditions of high humidity (commonly pro- The genotype × date term was signifi cant and Received for publication 19 Nov. 2002. Accepted duced at the leaf surface as cool nights change thus was used as the error term in the analysis for publication 28 Apr. 2003. I thank the Perennial to warm days), when plants are crowded or of variance. Although a signifi cant interaction Plant Association, Hilliard, Ohio, for funding this research and Roslyn Gorin, Temple Univ., for sta- grown in shady environments without ad- occurred between genotype and testing date, tistical support. equate air circulation. These environmental the estimate of the variance component for 1To whom reprint requests should be addressed. conditions are typical in the shade garden genotype was almost 9.8 times greater than Current address: 699 Rheas Mill Rd., Farmington, and thus predispose lungworts to infection the variance component for genotype × date, AR 72730; e-mail: [email protected] by powdery mildew fungi. The disease is indicating that the contribution of testing date in

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Table 1. Analysis of variance for powdery genotypes in this study exhibited mid to high mitage, 1997). mildew disease incidence for 25 mean ratings for powdery mildew infection, The fi ve lungwort genotypes exhibiting Pulmonaria genotypes. indicating relatively low levels of resistance mean ratings of less than 1.00, indicating Source df MS to powdery mildew. However, four cultivars very high levels of powdery mildew resis- Genotypez 24 29.12*** (‘Spilled Milkʼ, ‘Excaliberʼ, ‘Redstartʼ, and tance, represent three different Pulmonaria Date 3 0.18 ‘David Wardʼ) and one selection (P. longifolia species (P. longifolia, P. rubra, and P. sac- Genotype × date 72 0.90*** ssp. cevennensis) exhibited mean ratings for charata), demonstrating that useful sources Error 200 0.19 powdery mildew infection of less than 1.00, of genetic resistance are not restricted to any zGenotype × date is the error term for testing indicating high levels of resistance to powdery particular species. Additionally, these fi ve genotype effect. mildew. For these fi ve genotypes the majority lungwort genotypes represent quite a range *** Signifi cant at P = 0.001. of inoculated leaves never developed any vis- of variability for ornamental attributes. Cul- ible signs of infection and when infection did tivars of P. rubra, such as ‘Redstartʼ, typically Table 2. Species, cultivar, and mean rating for powdery mildew disease incidence for 25 occur, less than 20% of the leaf surface showed have coral-red fl owers and unspotted foliage. Pulmonaria genotypes. evidence of powdery mildew mycelial growth. Pulmonaria rubra ‘David Wardʼ has the addi- The lungwort selection P. longifolia ssp. cev- tional ornamental value of sporting leaves that z y Genotype Mean rating ennensis showed no visible sign of infection are almost mint green in color with a distinct x P. longifolia Golden Haze 4.67 a throughout the entire study, suggesting that white margin. ‘Spilled Milkʼ, purported to be P. angustifolia Blaues Meer 4.56 a this selection has very high levels of resistance a P. saccharata hybrid (Armitage, 1997), has P. longifolia E.B. Anderson 4.50 a P. saccharata Roy Davidson 4.50 a to powdery mildew. In this study, the single heavily splotched foliage and pink fl owers. P. hybrid Majeste 4.31 a representative of the species P. angustifolia, Pulmonaria hybrid ‘Excaliberʼ, also purported P. saccharata Dora Bielefeld 4.14 ab the cultivar ‘Blaues Meerʼ, exhibited a very to be a P. saccharata hybrid (Armitage, 1997), P. hybrid Ocupol (Opal) 4.08 ab high mean rating (4.56) for powdery mildew has leaves that are almost solid silver with a P. longifolia Bertram Anderson 4.00 abc development, indicating a very low level of thin green margin and rose-colored fl owers. P. hybrid Merlin 3.89 a–d resistance to powdery mildew. The two repre- Pulmonaria longifolia ssp. cevennensis, a se- P. offi cinalis Sissinghurst White 3.89 a–d sentatives of the species P. rubra, the cultivars lection from Cevennes, France, has long, nar- P. hybrid Smokey Blue 3.31 b–e ‘Redstartʼ and ‘David Wardʼ, exhibited very row, heavily spotted leaves, vigorous growth, P. saccharata Pierreʼs Pure Pink 3.17 c–e low mean ratings for powdery mildew infec- and deep violet-blue fl owers. Other than the P. vallarsae Marjorie Fish 3.11 de P. saccharata Mrs. Moon 3.08 de tion (0.25 and 0.11, respectively), indicating cultivar David Ward, which is purported to be P. hybrid Coral Springs 2.83 ef high levels of resistance to powdery mildew. sterile (S. Cooperman, Crown Oak Nursery, P. hybrid Milky Way 2.64 ef (It would be interesting to examine whether Downingtown, Pa., personal communica- P. offi cinalis White Wings 2.5 efg other cultivars of P. angustifolia and P. rubra tion), this group of lungwort genotypes may P. saccharata British Sterling 2.11 fg would also exhibit these respective low and provide useful sources of genetic resistance to P. longifolia Dordogne 1.78 g high levels of resistance.) Lungwort genotypes powdery mildew. Since Pulmonaria species P. hybrid Raspberry Splash 1.75 g with P. longifolia parentage exhibited the ex- intercross readily, these resistant genotypes P. hybrid Spilled Milk 0.42 h tremes of resistance from high to low. While may be useful to introgress powdery mildew P. hybrid Excaliber 0.39 h the selection P. longifolia ssp. cevennensis resistance into diverse lungwort germplasm P. rubra Redstart 0.25 h P. rubra David Ward 0.11 h exhibited the lowest mean rating (0.00) or that may have high ornamental value but P. longifolia subsp. cevennensis 0.00 h highest resistance of all the genotypes tested, little powdery mildew resistance. The future zNomenclature as per Hoffman et al., 2000. another P. longifolia cultivar, ‘Golden Hazeʼ, is bright for the development of new powdery yMean rating based on a scale of 0–5: 0 = no visible exhibited the highest mean rating (4.67) of mildew resistant lungwort cultivars with all sign of infection;1 = 1% to 20%; 2 = 20% to 40%; 3 all tested genotypes, indicating extremely the ornamental attributes we now enjoy in this = 40% to 60%; 4 = 60% to 80%; 5 = 80% to 100% of low resistance to powdery mildew. Pulmo- fabulous genus. leaf surface covered with white mycelial growth. naria longifolia ‘Dordogneʼ and P. hybrid x Mean separation by Duncanʼs multiple range test, ‘Raspberry Splashʼ, which is purported to be Literature Cited P = 0.05; n = 3 for each genotype. a P. longifolia hybrid (Armitage, 1997), also exhibited relatively low mean ratings (1.78 Agrios, G.N. 1997. Plant disease caused by fungi. In: the genotypic expression for powdery mildew and 1.75, respectively), indicating moderately Plant pathology. Academic Press, New York. Armitage, A.M. 1997. Pulmonaria. In: Herbaceous resistance was small. high levels of resistance to powdery mildew. perennial plants. Stipes Publ. Co., Champaign, The data revealed a wide and continu- Lungworts with P. saccharata parentage Ill. ous range of variability for infection and exhibited the entire range of variability for DiSabato-Aust, T. 1998. Encyclopedia of perennials. development of powdery mildew disease in resistance to powdery mildew. Five of the 10 In: The well-tended perennial garden. Timber the 25 lungwort genotypes (Table 2). The lungwort cultivars with a mean rating over 3.50, Press, Portland, Ore. continuous range of variability suggests that indicating very low levels of resistance, are of Hoffman, M.H.A., H.J. van de Laar, G. Fortgens, resistance to powdery mildew in lungworts known or purported P. saccharata parentage and P.C. de Jong. 2000. List of names of peren- may be quantitative. Spearmanʼs correla- (‘Roy Davidsonʼ, ‘Majesteʼ, ‘Dora Bielefeldʼ, nials. Appl. Res. for Nursery Stock, Boskoop, tion coeffi cients among testing dates were ‘Opalʼ, and ‘Merlinʼ) (Armitage, 1997; Hoff- the Netherlands. Lovejoy, A. 1993. Pulmonarias. Horticulture 71: signifi cant (ranging from r = 0.77 to 0.89), man et al., 2000). Conversely, two of the fi ve 54–58. indicating relatively high levels of genotype lungwort genotypes exhibiting a mean rating Mathew, B. 1982. Pulmonaria in gardens. The rank order consistency among testing dates of less than 1.00, indicating very high levels Plantsman 4:100–111. (ranging from 59% to 79% rank order consis- of resistance, are purported to be P. saccharata SAS Institute, 2001. Release 8.2. SAS Inst., Cary, tency among dates). The majority of lungwort hybrids (‘Spilled Milkʼ and ‘Excaliberʼ) (Ar- N.C.

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