ISSN 1099-209X, Volume 87, Number 3

This article was published in the above mentioned Springer issue. The material, including all portions thereof, is protected by copyright; all rights are held exclusively by Springer Science + Business Media. The material is for personal use only; commercial use is not permitted. Unauthorized reproduction, transfer and/or use may be a violation of criminal as well as civil law. Am. J. Pot Res (2010) 87:261–276 Author's personal copy DOI 10.1007/s12230-010-9132-9

Common Scab Trials of Varieties and Advanced Selections at Three U.S. Locations

Kathleen G. Haynes & Leslie A. Wanner & Christian A. Thill & James M. Bradeen & Jeffrey Miller & Richard G. Novy & Jonathan L. Whitworth & Dennis L. Corsini & Bryan T. Vinyard

Published online: 24 April 2010 # Potato Association of America 2010

Abstract Common scab (CS), caused by Streptomyces was scored for the percent of surface area covered with spp., is a soil-borne bacterial disease of potato tubers which lesions and the type of lesion. These scores were converted may cause superficial, raised, or pitted lesions. The results to an area index (AI) and a lesion index (LI). AI, LI, and of screening potato germplasm for severity of CS can be the arcsine √ proportion scabby tubers (PS) were analyzed variable, necessitating testing over multiple environments. as normally distributed responses. There were significant The purposes of this study were to evaluate advanced differences among clones for AI in 2 years, LI in 5 years, germplasm from public potato breeding programs in and PS in 3 years. There were significant clone x location different regions of the United States for their reaction to interactions for AI and PS all 6 years, and LI in 5 years. CS, estimate broad-sense heritability for resistance, and Broad-sense heritability for AI, LI, and PS ranged from 0 to identify clones with stable resistance. Seventeen to 23 0.78, 0.49 to 0.90, and 0.30 to 0.80, respectively. clones per year were evaluated at each of three locations Evaluation at multiple sites remains important for charac- (ID, ME, MN) from 2002 to 2007. After harvest, each tuber terizing the reaction of potato germplasm to CS.

Funded in part by the USDA/ARS Potato Special Grants Program. Resumen La roña común (CS), causada por Streptomyces Electronic supplementary material The online version of this article spp., es una enfermedad bacteriana de los tubérculos de la (doi:10.1007/s12230-010-9132-9) contains supplementary material, papa, que puede causar lesiones superficiales, elevadas o which is available to authorized users. punteadas. Los resultados en las evaluaciones del germo- K. G. Haynes (*) : L. A. Wanner plasma de papa pueden variar en severidad de CS, USDA/ARS, requiriéndose pruebas en múltiples ambientes. Los propó- Genetic Improvement of Fruits and Vegetables Laboratory, sitos de este estudio fueron evaluar germoplasma avanzado Beltsville, MD 20705, USA de programas públicos de mejoramiento de papa en e-mail: [email protected] diferentes regiones de Estados Unidos para su reacción a C. A. Thill : J. Miller CS, estimar la heredabilidad para la resistencia en un Department of Horticultural Sciences, University of Minnesota, sentido amplio, e identificar clones con resistencia estable. St. Paul, MN 55108, USA Se evaluaron anualmente de 17 a 23 clones en cada una de J. M. Bradeen tres localidades (ID, ME, MN) del 2002 al 2007. Después Department of Plant Pathology, University of Minnesota, de la cosecha, cada tubérculo fue cuantificado en porcentaje St. Paul, MN 55108, USA de área de la superficie cubierta con lesiones y de qué tipo. Estas evaluaciones se convirtieron a un índice de área (AI) R. G. Novy : J. L. Whitworth : D. L. Corsini USDA/ARS, Aberdeen Research & Extension Center, y a un índice de lesión (LI). Se analizaron AI, LI, y la Small Grains and Potato Germplasm Research Unit, proporción √ arcoseno de tubérculos con roña (PS) como Aberdeen, ID 83210, USA respuestas en una distribución normal. Hubo diferencias significativas entre clones para AI en dos años, LI en cinco B. T. Vinyard USDA/ARS, Biometrical Consulting Service, años, y PS en tres años. Hubo interacciones significativas Beltsville, MD 20705, USA de clon x localidad para AI y PS en los seis años, y LI en 262 Author's personal copy Am. J. Pot Res (2010) 87:261–276 cinco años. La heredabilidad en un amplio sentido para AI, LI, share the same mechanism for pathogenicity, based on the y PS fluctuó de 0 a 0.78, 0.49 a 0.90 y 0.30 a 0.80 expression of the phytotoxin thaxtomin (Goyer et al. 1998; respectivamente. La evaluación en sitios múltiples permanece Healy et al. 2000; King et al. 1991; Kinkel et al. 1998; importante para la caracterización de la reacción del germo- Loria et al. 1996). Biosynthesis of thaxtomin and possibly plasma de papa a CS. other pathogenicity factors are encoded on parts of the Streptomyces chromosome that have unique base composi- Keywords Streptomyces spp. . Pitted scab . Raised scab . tion and appear to be conserved between otherwise Genotype x environment interactions . Stability analysis . distantly-related plant pathogenic Streptomyces species. Broad-sense heritability Pathogenicity regions may be spread by horizontal gene transfer from pathogenic to formerly non-pathogenic Abbreviations Streptomycetes to create new scab-causing species or strains CS common scab (Bukhalid et al. 1998, 2002; Cameron et al. 2003; Healy et LI lesion index al. 1999, 2000). PS arcsine √ proportion scabby tubers A useful and important component of scab management AI area index based on Merz’ scale is the use of scab-resistant varieties (Loria 2001; Powelson H broad-sense heritability et al. 1993). Although there is no known immunity to CI confidence interval common scab in potatoes, there is variation in severity of the disease phenotype (Goth et al. 1995; McKee 1958; Powelson et al. 1993). Varieties ‘Ontario’ and ‘Krantz’ have low levels of common scab but are not widely grown Introduction (Goth et al. 1995). ‘Superior’, ‘’ and ‘Pike’ are three popular varieties that have less severe common Commonscabofpotato(Solanum tuberosum L.) is scab. However, higher levels of resistance need to be characterized by superficial, raised, or deeply pitted corky incorporated into new varieties along with other traits lesions on potato tubers (Labruyère 1971; Loria 2001). important for their particular marketing niche. Such lesions detract from the marketability of the crop, Resistance to common scab has been reported to be although shallow or raised lesions can be removed controlled by two independent loci (Alam 1972; Murphy et mechanically during processing when the periderm is al. 1995). Scab resistance at one locus is postulated to be removed. However, in cases where deeply pitted lesions due to the presence of a dominant gene, while resistance at occur, peeling losses can be substantial and can result in the second locus is postulated to be due to homozygous rejection of the shipment. In addition, with more processing recessive alleles. Although this seems to be simple genetic operations favoring leaving the periderm intact, even control, it is complicated by the tetraploid nature of superficial or raised lesions can present a problem. If the commercial potatoes. Unlike diploid random mating pop- lesions cover more than 5% of the surface, the potatoes fail ulations, the approach to Hardy-Weinberg equilibrium at to make U.S. No. 1 grade (USDA 1991). the tetraploid level is slow due to the potential of multiple Common scab has conventionally been considered a alleles at a locus and tetrasomic segregation following disease of warm, dry, coarse-textured soils, but scab has been meiosis (Wricke and Weber 1986). Thus, the probability of reported wherever potatoes are grown, including wet and dry maintaining a locus in a quadruplex recessive state following soils, and in soils ranging from pH 4.0 to above 9.0 (Doering- breeding does not depend solely on the frequency of the Saad et al. 1992; Goyer et al. 1996;LambertandLoria recessive alleles. This may partially explain why resistance to 1989a;Lindholmetal.1997;Parketal.2003). Traditional common scab is not found more widely in commercial management strategies have focused on maintaining soil varieties and why breeders have been frustrated in their efforts moisture during and after tuber initiation, and maintaining to develop new varieties with high levels of resistance. neutral to alkaline soil pH (Lambert and Loria 1989b; However, the phenotypic expression of scab symptoms more Powelson et al. 1993), but these strategies are inadequate for closely resembles a quantitatively inherited trait than a controlling scab in the varied environments in which it qualitatively inherited trait (Haynes et al. 1997, 2009). occurs. In addition, anecdotal reports of common scab in Although a number of laboratory and greenhouse carefully irrigated fields are on the increase. methods have been developed to screen potato germplasm Several morphologically and phylogenetically diverse for common scab phenotypes (Bjor and Roer 1980; Caligari Streptomyces species can cause common scab (Archuleta and Wastie 1985; Lawrence 1956; Lawrence et al. 1990; and Easton 1981; Bouchek-Mechiche et al. 2000; Doering- Loria and Kempter 1986; Wiersema 1974), field evaluation Saad et al. 1992; Faucher et al. 1993; Kreuze et al. 1999; is still necessary to determine the true value of resistance. In Locci 1994; Loria et al. 1997; Wanner 2006). All probably addition to the variation present within pathogenic soil Am. J. Pot Res (2010) 87:261–276 Author's personal copy 263

Streptomyces populations, field testing incorporates the Streptomyces and to different growing environments; (2) many other variables in nature that influence the severity to estimate broad-sense heritability for common scab of scab, such as soil moisture content and soil pH (Davis et phenotypes from a more diverse genetic background and al. 1974; Jellis 1975; Lapwood et al. 1973; Waterer 2002). in more diverse environments than a previous estimate by Scab symptom expression is extremely variable. With Haynes et al. (1997); and, (3) to determine the phenotypic the ANOVA models used to analyze AI and LI in field stability of the reaction of these clones to Streptomyces. studies in northern Maine and West Virginia, Haynes et al. (1997) were able to explain 74 and 77% of the total variation, respectively (computations from their data). Materials and Methods Wanner and Haynes (2009) attempted to reduce this variability using controlled growth chamber experiments with Seventeen to 23 tetraploid potato clones from various public- standardized inoculum levels. Unfortunately, even under such funded U.S. Potato Breeding Programs were included in this highly controlled conditions, the amount of variation unac- study each year (Table 1). Of these, a common set of four counted for in the ANOVA model was 45–50%. In their check varieties was grown each year. Seed (tubers) for the controlled growth chamber experiments, they inoculated four round, white-skinned check varieties [‘Atlantic’ (moderately potato varieties with one of six Streptomyces species. They susceptible) and ‘Superior’ (moderately resistant)] and the were able to partition the variation among the main and long, russet-skinned check varieties [‘’ (sus- interactive effects of the host-pathogen-environment disease ceptible) and ‘Russet Burbank’ (moderately resistant)] were triangle. After unexplained variation, the greatest sources of supplied by the USDA/ARS-Beltsville Potato Breeding variation were host x pathogen x environment (11%) and Program and the USDA/ARS-Aberdeen Potato Breeding host x pathogen (10–16%). Program, respectively. Seed for all the newer varieties and Goth et al. (1993) created two different indices for rating numbered selections were supplied by the originating scab severity based on the amount of surface area infected breeding programs. The nomenclature for clones from these with scab lesions using the Horsfall and Barratt (1945) Potato Breeding Programs is as follows: clones with an A rating system, referred to as the area index (AI), and the prefix originated from USDA/ARS-Aberdeen; AF and SC type of lesion, referred to as the lesion index (LI). Haynes prefixes from the University of Maine; a B prefix from et al. (1997) estimated broad-sense heritability for severity USDA/ARS-Beltsville; CO and VC prefixes from Colorado of common scab in a tetraploid population evaluated in State University; an MS prefix from Michigan State northern Maine and West Virginia to be 0.89 for AI and University; an MN prefix from the University of Minnesota; 0.93 for LI. Although genotype x environment interactions an ND prefix from North Dakota State University; an NDTX were significant for both of these indices, they accounted prefix represents a seedling originating from North Dakota for less than 10% of the overall observed variation on these State University and selected in the field by Texas A&M measures of scab severity. In addition, stability analysis University researchers; and a W prefix from the University indicated that clones with the least severe scab phenotypes of Wisconsin-Madison. A clone could have been evaluated were also the most phenotypically unstable. Haynes et al. one or more years depending on the request of the (2009) found that there was no additive genetic variance for originating breeder. resistance to common scab in a diploid population of Clones were evaluated from 2002–2007 in Aberdeen, potatoes, although high levels of resistance to common scab ID; Presque Isle, ME;, and Becker, MN. The planting and existed in the population. However, because the diploid harvest dates for these experiments are given in Table 2. tubers were much smaller than tetraploid tubers, they were The experimental design at all three locations was a only able to analyze the proportion of scabby tubers rather randomized complete block design with three replications. than AI and LI. Five-hill plots were planted in ID and MN and four-hill A number of factors have hampered the development of plots in ME. During the growing season, normal cultural scab resistant potato varieties, including variable effects of practices for the respective locations were used. All tubers environmental conditions, genetic variation within S. from the plots were harvested at all locations. Additional tuberosum, genetic variation within pathogen populations, details on soil type, soil pH, organic matter, water all two- and three-way interactions involving these factors, management, average monthly maximum and minimum and the choice of rating scale(s). The purposes of this temperatures, cropping history, and inoculation are given in study were threefold: (1) to evaluate the scab severity Table 3. The native populations of pathogenic Streptomyces phenotypes in potato varieties and advanced breeding in these field plots have been described (Wanner 2009). selections from public potato breeding programs in three different geographic areas of the United States, maximiz- Scoring Each tuber was examined and scored for the ing the exposure of these clones to different populations of percentage of surface area covered with scab lesions and 264 Author's personal copy Am. J. Pot Res (2010) 87:261–276

Table 1 Potato clones evaluated for resistance to common scab at three locations from 2002–2007

Clone Number 2002 2003 2004 2005 2006 2007

Alturas A82360-7 x x x Atlantic xxxxxx Bannock Russet A81473-2 x x x Blazer Russet A8893-1 x x Classic Russet A95109-1 x Clearwater Russet AOA95154-1 x Defender A90586-11 x Freedom Russet W1836-3rus x x x x Gem Russet A8495-1 x x GemStar Russet A9014-2 x x Harley Blackwell B0564-8 x x x Highland Russet A9045-7 x x Ivory Crisp NDO1496-1 x Kalkaska MSJ036-A x Liberator x x W1201 x x x Mountain Rose CO94183-1R/R x x Peter Wilcox B1816-5 x Premier Russet A93157-6LS x x x Purple Majesty CO94165-3P/P x x Ranger Russet A7411-2 xxxxxx Russet Burbank xxxxxx Summit Russet A84118-3 x Superior xxxxxx Villetta Rose x A95409-1 x A97066-42LB x AOA95155-7 x AF1758-7 x x AF1921-4 x AF2211-9 xx AF2215-1 x AF2291-10 xx B0766-3 x x x B1240-1 x B1952-2 x B1992-166 x B2152-17 x B2327-2 x B2445-6 x B2451-6 x B2486-4 x BNC41-8 x BNC48-3 x BNC49-1 x BNC49-2 x CO94035-15RU x x CO95051-7W x CO95172-3RU x Am. J. Pot Res (2010) 87:261–276 Author's personal copy 265

Table 1 (continued)

Clone Number 2002 2003 2004 2005 2006 2007

MN00307-1 x MN00467-4 x MN18710 x MN96013-1 x MSG227-2 x x MSJ316-A x MSJ126-9Y x MSK061-4 x ND2470-27 x ND3196-1R x NDTX4271-1R x NDTX4304-6R x SC8801-2 x VC0967-2R/Y x x VC1002-3 W/Y x x VC1009-1 W/Y x W2133-1 x W2683-2Rus x for the most severe type of scab lesion observed. Percent- index (LI) was calculated as the sum of the individual tuber age surface area covered was rated based on the Merz 0–6 ratings of lesion type divided by six times the number of scale (Merz 2000), where 0 = none of the surface area tubers. Thus, each of these indices could range from zero to involved, 1=0–2%, 2=2–5%, 3=5–10%, 4=10–25%, 5= one. The proportion of scabby tubers in the plot was also 25–50%, and 6=>50% of the surface area covered with calculated. Analyses of variance on AI, LI, and the arcsine lesions. Type of scab lesion was rated on a 0–5 scale based √ proportion scabby tubers (PS) were conducted by year on the assessment key of James (1971): 0 = no scab, 1 = using the general linear models and mixed models superficial lesions <10 mm in diameter, 2 = superficial procedures in SAS, version 9.2 (SAS Institute Inc., Cary, lesions >10 mm in diameter, 3 = raised lesions <10 mm in NC). For these analyses, all sources of variation were diameter, 4 = raised lesions >10 mm in diameter, and 5 = considered random. Mean AI, LI and PS by location, by pitted lesions of all sizes. Each assessment value was increased clone, and by clone x location were also computed. by one; i.e. surface area covered was rated from 1 to 7, and Where significant clone x location interactions were lesion type from 1 to 6 to enable data transformations. found, these interactions were partitioned into stability- s2 variance components assignable to each clone before ( i ) 2 Statistical Analysis Three variables for each plot were and after (si ) heterogeneity due to location indices was calculated. An area index (AI) was calculated as the sum removed using the interactive matrix language procedure in of the individual tuber ratings of surface area infected SAS (Kang 1989). Non-significant variance values signify divided by seven times the number of tubers. A lesion stability. The vector of location indices was calculated as

Table 2 Planting and harvest dates for the three locations Aberdeen, Idaho Presque Isle, Maine Becker, Minnesota where potato germplasm was evaluated for resistance to Year Plant Harvest Plant Harvest Plant Harvest common scab from 2002–2007 2002 May 2 Oct 1 June 12 Sept 25 April 25 Sept 24 2003 May 1 Oct 16 June 5 Sept 16 April 24 Sept 19 2004 May 5 Sept 28 June 1 Sept 17 April 29 Sept 17 2005 May 21 Oct 11 June 20 Sept 19 April 28 Sept 14 2006 May 3 Sept 25 June 20 Sept 13 May 3 Sept 27 2007 May 3 Sept 12 June 7 Sept 5 May 1 Sept 25 266 Author's personal copy Am. J. Pot Res (2010) 87:261–276

Table 3 Soil type, soil pH, organic matter, water management, average monthly maximum and minimum temperatures, cropping history, and inoculation details for the three locations that evaluated potato germplasm for resistance to common scab from 2002–2007

Location Aberdeen, ID Becker, MN Presque Isle, E

Soil type Declo sandy loam Hubbard sandy loam (Udic Haploborall) Caribou silt-loam (fine-loamed mixed frigid Typic Haplorthod) Soil pH 8.0 5.5 6.5 Organic matter 1.2–1.5% 1.8–2.0% 0.3% Water management Irrigated: 3.6–4.1cm every 7days Irrigated: 0.8–1.5cm every 3–4days—as Not irrigated supplement to natural precipitation Average maximum and May: 20.6 and 2.8 April: 15.0 and 1.1 May: 17.3 and 4.8 minimum temperature June: 26.7 and 7.2 May: 21.7 and 6.7 June: 23.4 and 10.4 July: 32.2 and 11.1 June: 226.7 and 12.8 July: 25.6 and 13.6 Aug: 28.9 and 5.6 July: 29.4 and 15.0 Aug: 24.8 and 12.4 Sept: 24.4 and 3.9 Aug: 27.2 and 13.3 Sept: 21.2 and 8.3 Sept: 23.3 and 9.4 Cropping history Three year rotation: Two year rotation: No rotation: One year: Scab trial One year: Scab trial Scab trial every year Second year: green manure crop Second year: Third year: grain crop Inoculum added No No 2002: a, b 2003: a, b 2004: c (mixture of 10 isolates, ca. 1×1012 CFU total) 2005: c (mixture of 3 isolates, 10×1010 CFU total) 2006: c (mixture of 2 isolates, 1.2×1012 CFU total) 2007: no additional inoculum added a cow manure in spring b ground up peeled skin of scabby potatoes from previous season, applied at a rate of ca. 1 cup (250cc) per hill c each hill planted with 1/2 cup (ca. 125cc) soil containing fresh vermiculite cultures of Streptomyces previously isolated from this field the mean AI, LI, or PS of all clones in each location minus amount of the tuber surface area affected by scab, type of the mean AI, LI, or PS of all clones in all locations, lesion, and proportion of scabby tubers. This study resulted respectively. The ME 2006 evaluation site was lost due to in 17 location-year data sets, which are plotted in Figs. 1, 2, tuber late blight before the tubers could be scored for 3, 4, 5 and 6. Untransformed proportion scabby tubers common scab. Therefore, there were no degrees of freedom (mean incidence) was plotted in the figures for visual available for testing the significance of the stability- clarity, rather than the arcsine √ proportion scabby tubers variance components after removal of environmental (PS) used in statistical analysis, as data points overlapped heterogeneity in 2006. too much when plotting PS. Data from the ME 2006 Estimates of the clone, clone x location, and residual location were lost to tuber late blight before the tubers variances were obtained from the mixed models analyses could be evaluated. and used to calculate broad-sense heritability (H) on a mean Although there was a wide range in AI, LI, and PS basis (Nyquist 1991). A 95% confidence interval on H was across locations each year (Figs. 1, 2, 3, 4, 5 and 6), calculated from the type III mean squares obtained from the these differences were not significant (Table 3). This general linear models analyses (Knapp et al. 1985). could be due to a combination of the extremely variable nature of symptom expression and the lack of statistical power for testing, as there were only two and six degrees Results and Discussion of freedom in the numerator and denominator of the applicable F-test. Potato clones were grown in common scab test fields in ID, There were significant differences among clones for AI ME, and MN from 2002 to 2007, and were evaluated for in only 2 years (2003, 2005), LI in 5 years (all but 2005), Am. J. Pot Res (2010) 87:261–276 Author's personal copy 267

Fig. 1 Mean AI, LI, and Atlantic untransformed proportion IDAHO 2002 Ranger Russet scabby tubers (mean incidence) 0.9 Russet Burbank Superior for all clones evalulated for CS AF1758-7 in 2002, with the cube of LI as Alturas the size of the bubble B0766-3 0.7 B1240-1 Bannock Russet Defender Gem Russet Harley Blackwell 0.5 Ivory Crisp Liberator MSG227-2 SC8801-2 mean area affected Summit Russet

0.3

0.1 0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0 1.1 mean incidence D

Atlantic MAINE 2002 Ranger Russet 0.9 Russet Burbank Superior AF1758-7 Alturas B0766-3 B1240-1 0.7 Bannock Russet Defender Gem Russet Harley Blackwell Ivory Crisp Liberator 0.5 MSG227-2 SC8801-2 Summit Russet mean area affected

0.3

0.1 0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0 mean incidence

MINNESOTA 2002 Atlantic Ranger Russet 0.9 Russet Burbank Superior AF1758-7 Alturas B0766-3 B1240-1 0.7 Bannock Russet Defender Gem Russet Harley Blackwell Ivory Crisp Liberator 0.5 MSG227-2 SC8801-2 Summit Russet mean area affected

0.3

0.1 0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0 mean incidence 268 Author's personal copy Am. J. Pot Res (2010) 87:261–276

Fig. 2 Mean AI, LI, and Atlantic untransformed proportion IDAHO 2003 Ranger Russet scabby tubers (mean incidence) 0.9 Russet Burbank Superior for all clones evalulated for CS AF1758-7 in 2003, with the cube of LI as Alturas the size of the bubble B0766-3 0.7 A93157-6LS Bannock Russet AF1921-4 ND2470-27 Harley Blackwell 0.5 Megachip Liberator MSG227-2

mean areamean affected ND3196-1R NDTX4304-6R 0.3 W1836-1rus

0.1 0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0 1.1 mean incidence

MAINE 2003 Atlantic Ranger Russet 0.9 Russet Burbank Superior AF1758-7 Alturas B0766-3 A93157-6LS 0.7 Bannock Russet AF1921-4 ND2470-27 Harley Blackwell Megachip 0.5 Liberator MSG227-2 ND3196-1R mean areamean affected NDTX4304-6R W1836-1rus 0.3

0.1 0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0 1.1 mean incidence

MINNESOTA 2003 Atlantic 0.9 Ranger Russet Russet Burbank Superior AF1758-7 Alturas B0766-3 0.7 A93157-6LS Bannock Russet AF1921-4 ND2470-27 Harley Blackwell 0.5 Megachip Liberator MSG227-2 mean areamean affected ND3196-1R NDTX4304-6R W1836-1rus 0.3

0.1 0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0 1.1 mean incidence Am. J. Pot Res (2010) 87:261–276 Author's personal copy 269 Fig. 3 Mean AI, LI, and untransformed proportion IDAHO 2004 Atlantic scabby tubers (mean incidence) 0.9 Ranger Russet Russet Burbank for all clones evalulated for CS Superior in 2004, with the cube of LI as CO94035-1Rus the size of the bubble Alturas 0.7 B0766-3 MN96013-1 Bannock Russet CO94183-1R/R Gem Russet Harley Blackwell 0.5 Megachip Freedom Russet Gem Star Russet

mean area affected CO94165-3P/P VC0967-2R/Y VC1002-3WY 0.3 Villetta Rose

0.1 0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0 mean incidence

0.9 MAINE 2004 Atlantic Ranger Russet Russet Burbank Superior CO94035-1Rus 0.7 Alturas B0766-3 MN96013-1 Bannock Russet CO94183-1R/R 0.5 Gem Russet Harley Blackwell Megachip Freedom Russet

mean area affected Gem Star Russet 0.3 CO94165-3P/P VC0967-2R/Y Villetta Rose VC1002-3WY

0.1 0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0 mean incidence

MINNESOTA 2004 0.9 Atlantic Ranger Russet Russet Burbank Superior CO94035-1Rus 0.7 Alturas B0766-3 MN96013-1 Bannock Russet CO94183-1R/R 0.5 Gem Russet Harley Blackwell Megachip Freedom Russet mean area affected Gem Star Russet 0.3 CO94165-3P/P VC0967-2R/Y VC1002-3WY Villetta Rose 0.1 0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0 mean incidence and PS in 3 years (2003, 2005, 2007) (Table 4). In terms of check clone ‘Russet Burbank’. Therefore, several clones all three measurements of tolerance (AI, LI, PS), no clones were more resistant in terms of LI and PS than ‘Superior’ were significantly more tolerant to CS than ‘Russet these 2 years. Burbank’ and no clones were more susceptible than Clone x location interactions were significant for all ‘Ranger Russet’. However, in 2006 and 2007, LI and PS three measurements of resistance in all years, except for were significantly greater in the moderately resistant check LI in 2003 (Table 4), indicating that the performance of at clone ‘Superior’ than in the other moderately resistant least some of the clones varied across these three locations 270 Author's personal copy Am. J. Pot Res (2010) 87:261–276 Fig. 4 Mean AI, LI, and IDAHO 2005 Atlantic untransformed proportion Ranger Russet scabby tubers (mean incidence) 0.9 Russet Burbank for all clones evalulated for CS Superior CO94035-1Rus in 2005, with the cube of LI as A8893-1 the size of the bubble A9045-7 0.7 A93157-6LS AF2211-9 CO94183-1R/R AF2291-10 B1952-2 Megachip 0.5 Freedom Russet Gem Star Russet

mean area affected CO94165-3P/P VC0967-2R/Y B1992-166 0.3 Peter Wilcox

0.1 0.00.10.20.30.40.50.60.70.80.91.01.1 mean incidence Atlantic MAINE 2005 Ranger Russet 0.9 Russet Burbank Superior CO94035-1Rus A8893-1 A9045-7 0.7 A93157-6LS AF2211-9 CO94183-1R/R AF2291-10 B1952-2 0.5 Megachip Freedom Russet

mean area affected Gem Star Russet CO94165-3P/P 0.3 VC0967-2R/Y B1992-166 Peter Wilcox

0.1 0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0 1.1 mean incidence

MINNESOTA 2005 Atlantic 0.9 Ranger Russet Russet Burbank Superior CO94035-1Rus A8893-1 A9045-7 0.7 A93157-6LS AF2211-9 CO94183-1R/R AF2291-10 B1952-2 0.5 Megachip Freedom Russet Gem Star Russet CO94165-3P/P mean area affected VC0967-2R/Y B1992-166 0.3 Peter Wilcox

0.1 0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0 1.1 mean incidence each year. Overall, slightly more than half the clones were 5, 6). There were two exceptions to this general trend. stable for any one of the three measures of resistance In 2003 more than half the clones were unstable before either before or after removal of location heterogeneity removal of location heterogeneity for both AI and (Electronic Supplementary Information Tables 1, 2, 3, 4, PS. Am. J. Pot Res (2010) 87:261–276 Author's personal copy 271 Fig. 5 Mean AI, LI, and untransformed proportion IDAHO 2006 Atlantic 0.9 Ranger Russet scabby tubers (mean incidence) Russet Burbank for all clones evalulated for CS Superior in 2006, with the cube of LI as A95109-1 the size of the bubble Blazer Russet 0.7 A9045-7 A93157-6LS AF2211-9 AF2215-1 AF2291-10 0.5 CO95172-3Ru MSJ036-A MSJ126-9Y mean area affected MSJ316-A MSK061-4 0.3 VC1009-1W/Y VC1002-3WY CO95051-7W

0.1 0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0 1.1 mean incidence

Atlantic MINNESOTA 2006 Ranger Russet 0.9 Russet Burbank Superior A95109-1 Blazer Russet A9045-7 0.7 A93157-6LS AF2211-9 AF2215-1 AF2291-10 0.5 CO95172-3Ru MSJ036-A MSJ126-9Y MSJ316-A mean area affected MSK061-4 0.3 VC1009-1W/Y VC1002-3WY CO95051-7W

0.1 0.00.10.20.30.40.50.60.70.80.91.01.1 mean incidence

Location-specific difference in the behavior of the check respectively (Table 4). The estimates of broad-sense varieties in three locations compared to the overall mean is heritability for AI and LI were lower in this study than in shown in Fig. 7. Of the round, white-skinned check the earlier study by Haynes et al. (1997). They may be varieties tested across all locations all 6 years, ‘Atlantic’ lower because of the greater diversity in environments in tended to be more stable both before and after removal of this study, a (presumably) greater diversity in Streptomyces location heterogeneity than ‘Superior’. The stabilities of the (Wanner 2009), greater diversity in the genetic composition long, russet-skinned check varieties ‘Ranger Russet’ and of the germplasm being evaluated, the fact that tubers at ‘Russet Burbank’ were similar: approximately half the time each location were scored by a researcher at that location they were stable and half the time unstable. Among the (variation in researchers’ perception even though the same other clones tested more than 1 year only ‘Alturas’ was rating scale was used) or various two- and three-way stable for all measures of resistance in 2002 and 2004. interactions involving all of these factors. Differences in ‘GemStar Russet’ was stable for all measures of resistance Streptomyces strains have been previously documented in 2004 and 2005 with the exception that it was unstable for (Wanner 2007). Furthermore, the amount of the tuber AI in 2004 before removal of location heterogeneity. surface area affected by scab, though not the most severe CO94035-15RU was stable for all measures of resistance type of lesion, increases with increasing concentration of in 2004 and 2005 with the exception that it was unstable for pathogenic Streptomycetes (Wanner unpublished). It is PS in 2004 before removal of location heterogeneity. unlikely that there is a uniform concentration of pathogenic Estimates of broad-sense heritability ranged from 0 to Streptomyces in the soil. The proportion of the surface area 0.78, 0.49 to 0.90, and 0.30 to 0.80 for AI, LI, and PS, affected may be primarily due to the concentration of 272 Author's personal copy Am. J. Pot Res (2010) 87:261–276 Fig. 6 Mean AI, LI, and untransformed proportion IDAHO 2007 Atlantic Ranger Russet scabby tubers (mean incidence) 0.9 Russet Burbank for all clones evalulated for CS Superior in 2007, with the cube of LI as A95409-1 the size of the bubble A97066-42LB AOA95154-1 0.7 AOA95155-7 B2152-17 B2327-2 B2445-6 B2451-6 Freedom Russet 0.5 B2486-4 BNC41-8

mean area affected BNC48-3 BNC49-1 BNC49-2 MN00307-1 0.3 MN00467-4 MN18710 W2133-1 W2683-2Rus

0.1 0.00.10.20.30.40.50.60.70.80.91.0 mean incidence

Atlantic MAINE 2007 Ranger Russet 0.9 Russet Burbank Superior A95409-1 A97066-42LB AOA95154-1 AOA95155-7 0.7 B2152-17 B2327-2 B2445-6 B2451-6 Freedom Russet 0.5 B2486-4 BNC41-8 BNC48-3

mean area affected BNC49-1 BNC49-2 MN00307-1 0.3 MN00467-4 MN18710 W2133-1 W2683-2Rus

0.1 0.00.10.20.30.40.50.60.70.80.91.01.1 mean incidence

MINNESOTA 2007 Atlantic Ranger Russet 0.9 Russet Burbank Superior A95409-1 A97066-42LB AOA95154-1 AOA95155-7 0.7 B2152-17 B2327-2 B2445-6 B2451-6 Freedom Russet B2486-4 0.5 BNC41-8 BNC48-3

mean area affected BNC49-1 BNC49-2 MN00307-1 0.3 MN00467-4 MN18710 W2133-1 W2683-2Rus

0.1 0.00.10.20.30.40.50.60.70.80.91.01.1 mean incidence m .PtRs(00 87:261 (2010) Res Pot J. Am. Table 4 Estimates of the variance components from the analysis of variance on mean area index (MI), mean lesion index (LI) and arcsine √ proportion scabby tubers (PS) for the three locations where potato germplasm was evaluated for resistance to common scab, estimates of broad-sense heritability (H) for resistance to common scab, and the 95% confidence interval (CI) on H for each year

Source 2002 2003 2004

MI LI PS MI LI PS MI LI PS

Location 0.02543 0.00383 0.0429 0.03256 0.00672 0.1793 0.0423 0.0154 0.1407 Rep(location) 0.00026 0.00227 0.0022 0.00302 0.00021 0.0000 0.0003 0.0011 0.0037 –

Clone 0.00000 0.02129* 0.0102 0.00536* 0.01657** 0.0357** 0.0013 0.0070* 0.0057 276 Location x clone 0.01407** 0.01291** 0.03024** 0.00200* 0.00189 0.0124* 0.0029** 0.0063** 0.0263** Error 0.01047 0.01241 0.03291 0.00734 0.01127 0.0422 0.0030 0.0090 0.0254 H 0.00 0.79 0.43 0.78 0.90 0.80 0.51 0.69 0.33 95% CI 0.00, 0.60 0.53, 0.92 0.00, 0.78 0.53, 0.91 0.78, 0.96 0.57, 0.92 0.00, 0.79 0.31, 0.87 0.00, 0.71 Author's copy personal Source 2005 2006 2007

MI LI PS MI LI PS MI LI PS

Location 0.0199 0.0133 0.1179 0.0010 0.0206 0.0006 0.0077 0.0004 0.0696 Rep(location) 0.0003 0.0000 0.0000 0.0001 0.0006 0.0037 0.0005 0.0002 0.0041 Clone 0.0047* 0.0045 0.0189* 0.0008 0.0106* 0.0102 0.0022 0.0163** 0.0271* Location x clone 0.0031** 0.0106** 0.0174** 0.0098** 0.0111** 0.0412** 0.0063** 0.0076** 0.0406** Error 0.0034 0.0102 0.0276 0.0022 0.0078 0.0220 0.0025 0.0066 0.0296 H 0.77 0.49 0.68 0.13 0.61 0.30 0.49 0.83 0.62 95% CI 0.51, 0.91 0.00, 0.79 0.32, 0.87 0.00, 0.67 0.00, 0.85 0.00, 0.73 0.00, 0.76 0.67, 0.92 0.21, 0.82

**, * Significant at the 5% and 1% level, respectively 273 274 Author's personal copy Am. J. Pot Res (2010) 87:261–276 Fig. 7 Mean AI, LI, and MEAN for checks Superior (6) untransformed proportion 0.9 MEAN for checks 0.9 scabby tubers (mean incidence) all locations, all years ID, all years Russet Burbank (6) Atlantic (6) for the four check varieties Superior (6) 0.7 evalulated for CS from Russet Burbank (6) 0.7 Ranger Russet (6) 2002–2007, with the cube of LI Atlantic (6) as the size of the bubble 0.5 Ranger Russet (6) 0.5

0.3 0.3 mean area affected mean area affected

0.1 0.1 0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0 0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0 mean incidence mean incidence

MEAN for checks MEAN for checks Superior (6) 0.9 0.9 ME, all years MN, all years Russet Burbank (6) Atlantic (6) Ranger Russet (6) 0.7 Superior (6) 0.7 Russet Burbank (6) Atlantic (6) 0.5 0.5 Ranger Russet (6)

0.3 0.3 mean area affected mean area affected

0.1 0.1 0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0 0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0 mean incidence mean incidence

pathogenic Streptomyces around the developing tuber, In studies such as these, potato germplasm is grown rather than the genetic composition of the tuber. under a wide range of environmental conditions, and The results of this study have interesting implications for exposed to likely diversity in both pathogen populations quantifying resistance to common scab and classifying and concentrations. Thus, this information is useful for potato germplasm for its reaction to CS. Good visual determining broad-based common scab disease phenotypes comparisons of the three indices for rating scab symptoms, of potato germplasm and can be used by growers whose with the cube of LI as the size of the bubble, and where fields have a history of common scab to choose potato mean incidence indicates the non-transformed proportion of varieties to minimize the deleterious effects of scab. This scabby tubers, are presented in Figs. 1, 2, 3, 4, 5, 6 and 7. information can also be used by breeders to choose parental In this study, the amount of surface area affected (AI) for materials with broad-based, durable response to the any given clone was the least discriminating variable for pathogen to develop varieties showing less scab damage. determining levels of resistance among clones: in only two The information on clones which are phenotypically of the 6 years were there significant differences among unstable for disease phenotype can also be utilized by clones for AI. The proportion of scabby tubers produced pathologists to determine the nature and components of was only slightly better than AI for discriminating among specific responses. clones: in three of the 6 years there were significant Potato breeders have to consider many attributes besides differences among clones for PS. The most severe type of resistance to CS in the decision whether or not to release a lesion produced in reaction to Streptomycetes turned out to new variety. Many of the clones evaluated in this study be the best variable for discriminating among clones: in five have been named and released as indicated in the of the 6 years there were significant differences among Electronic Supplementary Information Tables. It is encour- clones for LI. This index should then be utilized for aging to note that most of the new varieties are as resistant classification purposes. Earlier studies by Goth et al. (1993) to CS as the moderately resistant standard ‘Russet had suggested that both AI and LI be utilized in clustering Burbank’, although some clones behave better in some clones into resistant, intermediate and susceptible catego- locations than in others. It would appear that greater ries. It remains to be seen whether the results of this test emphasis now needs to be placed on breeding clones with represent an anomaly, or whether only LI will be needed to stable resistance across a wide range of conditions. Studies categorize clones when evaluating severity over a diverse such as this will help breeders to identify stable, resistant geographic area. germplasm for future breeding efforts. Am. J. Pot Res (2010) 87:261–276 Author's personal copy 275

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