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Published online 30 July 2007
Published in Crop Sci 47:1367-1374 (2007)
© 2007 Crop Science Society of America
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CROP BREEDING & GENETICS

Selecting Common Bean with Genes of Different Evolutionary Origins for Resistance to Xanthomonas campestris pv. phaseoli

Margarita Lema Marqueza,*, Henry Teránb and Shree P. Singhb

a Mision Biologica de Galicia, Carballeira 8, 36143 Salcedo, Pontevedra, Spain
b Plant, Soil and Entomological Sciences Dep., Univ. of Idaho, Kimberly Research & Extension Center, 3793 North 3600 East, Kimberly, ID 83341-5076

* Corresponding author (mlema{at}mbg.cesga.es).


   ABSTRACT
TOP
 NOTES
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
Common bacterial blight (CBB) is an important seed-borne disease of common bean (Phaseolus vulgaris L.). Low levels of resistance occur in the common and scarlet runner bean (Phaseolus coccineus L.), with higher levels available in the tepary bean (Phaseolus acutifolius A. Gray). Germplasm lines with CBB resistance separately from each of the three Phaseolus species and pyramided resistance are available. The objectives of this study were to: (i) determine the main and interaction effects of two isolates of Xanthomonas campestris pv. phaseoli (Xcp), one from Colorado and one from Wisconsin, and their inoculum densities with CBB resistance from the three species separately and pyramided; and (ii) identify the most useful germplasm for breeding for resistance. Thirty-one genotypes were evaluated at 14 and 21 d after inoculation (DAI) using two inoculum densities in 2005 and three in 2006 of each of the two Xcp isolates. Large differences in response to Colorado and Wisconsin Xcp isolates, densities, and evaluation time were observed. The resistance derived from the three species separately was not effective against the aggressive Wisconsin Xcp isolate at higher densities ≥108, especially at 21 DAI. Resistance pyramided with the tepary bean was the most effective. No crossover interactions were observed between the 31 common bean germplasm sources and the two Xcp isolates at any density and evaluation date. Use of only pyramided resistance for breeding is advised.

Abbreviations: CBB, common bacterial blight • DAI, days after inoculation • IBL, interspecific breeding line • RAPD, random amplified polymorphic DNA • Xcp, Xanthomonas campestris pv. phaseoli • Xcpf, X. campestris pv. phaseoli var. fuscans


   INTRODUCTION
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
COMMON BACTERIAL blight, caused by Xanthomonas campestris pv. phaseoli Smith (Dye) (Xcp, synonymous with X. axonopodis pv. phaseoli) and X. campestris pv. phaseoli var. fuscans (Xcpf), is a major production constraint of common bean (Phaseolus vulgaris L.) in most regions of the world. Common bacterial blight is a seed-borne disease causing 20 to 60% yield losses on susceptible cultivars, especially under relatively humid and warm growing conditions. Moreover, severe CBB adversely affects seed quality, including size, shape, color, and germination. Thus, the marketability of infected seed and its distribution out of the production region can be limited and seed may be heavily discounted.

Only low levels of CBB resistance occur in a few common bean landraces from Mexico (Singh and Muñoz, 1999) and the USA (Miklas et al., 2003). Some accessions of Phaseolus species of the common bean's secondary gene pool, such as P. coccineus (the scarlet runner bean), possess similar or slightly higher levels of resistance (Mohan, 1982). But P. acutifolius (the tepary bean), a member of the tertiary gene pool, has the highest levels of resistance (Coyne and Schuster, 1983; Singh and Muñoz, 1999; Zapata et al., 1985). Since the 1960s, researchers believed that CBB resistance of great northern Nebraska no. 1 Sel 27 (GN no. 1 Sel 27) was derived from the tepary bean (Coyne and Schuster, 1983; Coyne et al., 1965). Miklas et al. (2003) unequivocally demonstrated, however, that the common bean landrace great northern Montana no. 5, and not the tepary bean, was the source of CBB resistance of GN no. 1 Sel 27. Great northern Nebraska no. 1 Sel 27 and other sources of CBB resistance from the common bean landraces have been used for development of improved germplasm lines (e.g., BAT 93, XAN 91, and XAN 112) and cultivars (e.g., Montcalm, Tara, and Jules) since the 1960s. Because the levels of CBB resistance available from common bean landraces was inadequate under Midwestern growing conditions (Michigan, Minnesota, North Dakota, and Wisconsin) where severe disease pressure occurs, breeding progress has been slow.

Freytag et al. (1982), Miklas (1998), Miklas et al. (1994, 1999), and Park and Dhanvantari (1987) reported on CBB-resistant common bean germplasm lines derived from interspecific crosses between the common and scarlet runner bean. The CBB resistance of these germplasm lines was not high enough, however, to warrant their extensive exploitation in the breeding and genetics of common bean. Furthermore, no attempts were made to determine complementation and pyramiding between P. coccineus and P. vulgaris sources of CBB resistances.

Thomas and Waines (1980, 1984) were the first to successfully hybridize the common with tepary bean in the Americas, which led to the development of CBB-resistant interspecific breeding lines (IBLs). For example, McElroy (1985), using populations from Thomas and Waines (1980, 1984), was the first to develop CBB-resistant IBLs, namely XAN 159, XAN 160, and XAN 161. Subsequently, Scott (1988), Scott and Michaels (1992), and Mejía-Jiménez et al. (1994) also reported successful hybridization between the common and tepary bean that resulted in CBB-resistant IBLs. Singh and Muñoz (1999) selected CBB-resistant IBLs, namely VAX 1 and VAX 2, from the populations developed by Mejía-Jiménez et al. (1994). Wilkinson (unpublished data, 1985) performed the first pyramiding of CBB resistance using IBLs that were developed from crosses of the common bean with scarlet runner bean as well as with the tepary bean. Examples of germplasm lines that were selected for pyramided CBB resistance from Wilkinson's populations at the Centro Internacional de Agricultura Tropical (CIAT), Palmira, Colombia, include G 17341, G 17344, and Wilkinson 2. Subsequently, Temple (unpublished data, 1985) developed breeding lines such as XAN 263 and XAN 309 and Singh and Muñoz (1999) developed VAX 3, VAX 4, VAX 5, and VAX 6 that also carried pyramided CBB resistance.

Epiphytic populations (around 108 colony-forming units [cfu] kg–1 fresh weight) of pathogenic and nonpathogenic Xcp and Xcpf colonize common bean phyllosphere or aerial parts without causing CBB symptoms (Gent et al., 2005; Jacques et al., 2005). The solitary populations of bacteria on the leaf surface may increase or decrease with a corresponding change in humidity, but the biofilm population remains constant (Jacques et al., 2005). Under favorable climatic conditions, the pathogenic Xcp and Xcpf cause similar symptoms on susceptible common bean, and the production of the brown pigment that distinguishes Xcpf appears to be unrelated to pathogenicity (Gilbertson et al., 1991; Goodwin and Sopher, 1994). There is considerable molecular diversity between and within Xcp and Xcpf isolates (Gilbertson et al., 1991; Chan and Goodwin, 1999). Often the diversity is larger between than within the two xanthomonads (López et al., 2006; Mahuku et al., 2006; Mkandawire et al., 2004). Mkandawire et al. (2004) reported that the Xcp isolates from East Africa were distinct from those of the Americas. While no pathogenic specialization was detected among Xcpf isolates, the East African Xcp isolates were highly pathogenic on large-seeded (>40 g [100 seed weight]–1) Andean common bean and significantly less pathogenic on small-seeded (<25 g [100 seed weight]–1) Middle American common bean. In contrast, the Xcp isolates from the Americas were equally pathogenic on common bean from both gene pools. López et al. (2006) did not find any pathogenic specialization within or between the Xcp and Xcpf isolates from Spain. Mahuku et al. (2006) did not find any geographical differentiation or pathogenic specialization between 211 Xcp and 132 Xcpf isolates from around the world. But, in general, Xcpf was more frequent on the African continent, Xcp in the Caribbean, and both xanthomonads were about equally represented among isolates from the Americas. It should be noted that Mkandawire et al. (2004) and López et al. (2006) did not use any known source of CBB resistance in their pathogenicity studies. In contrast, a group of differential common bean cultivars (Zapata, 1997) and tepary bean accessions (Zapata and Vidaver, 1987) were used to identify distinct pathogenic races among Xcp isolates. Avila et al. (1998) also observed differences in pathogenicity among the Xcp and Xcpf isolates from Brazil and identified resistant and susceptible common bean. Similarly, Navarrete-Maya and Acosta-Gallegos (2005) reported pathogenic diversity among Mexican Xcp isolates.

Researchers commonly use pathogenic Xcp isolates for breeding and genetics studies in the Americas. Aggour et al. (1989), Leyna and Coyne (1985), Lienert and Schwartz (1994), and Opio et al. (1994), among others, reported significant effects of bacterial isolate and density on common bean cultivar reactions. Bacterial densities of 107 to 5 x 108 cfu mL–1 have been used for molecular diversity studies (López et al., 2006; Mahuku et al., 2006; Mkandawire et al., 2004). Similar bacterial densities have also been used for germplasm screening (Avila et al., 1998; Navarrete and Acosta, 2000), inheritance studies (Miklas et al., 1996; Silva et al., 1989), and breeding common bean (Asensio-Manzanera et al., 2006; Singh and Muñoz, 1999). Some of the bacterial isolates and densities used, however, may not discriminate between susceptible and resistant common bean genotypes, especially if evaluations are delayed for three or more weeks. The objectives of this study were to: (i) determine the main and interaction effects of two Xcp isolates of different geographical origins within the USA, their inoculum densities, and host resistances of distinct evolutionary origins; and (ii) identify the most useful germplasm for breeding for CBB-resistant cultivars.


   MATERIALS AND METHODS
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 REFERENCES
 
Thirty-one common bean breeding lines and cultivars were evaluated with one Xcp isolate each from Colorado and Wisconsin in the greenhouse at Kimberly, ID. The 31 genotypes were comprised of four common bean landraces (Colima 9, Montana no. 5, Tamaulipas 9-B, and Tlalnepantla 64 [synonymous with G 1320]), three breeding lines (A 493, XAN 91, and XAN 112), and one cultivar (Montcalm) bred for CBB resistance. In addition, six were IBLs derived from crosses of common bean with P. coccineus (ICB 3, ICB 6, ICB 8, ICB 10, ICB 12, and TARS VCI-4B), four were derived from crosses of common bean with P. acutifolius (OAC 88-1, VAX 1, VAX 2, and XAN 159), nine carried pyramided CBB resistance (G 17341, USDK-CBB-15, USPT-CBB-1, VAX 3, VAX 4, VAX 5, VAX 6, XAN 309, and Wilkinson 2), and four were susceptible checks (ICA Pijao, UI 114, USPT 72, and USPT 73). A randomized complete block design was used. Each experimental unit consisted of a single plant sown in a 20.3-cm (8-inch) pot. Moreover, each combination of genotype, bacterial isolate, and inoculum density was replicated three times. The bacterial cultures were grown in nutrient glucose agar for 48 h. Inoculum densities of 5 x 107 and 5 x 109 cfu mL–1 were used in 2005. A density of 108 cfu mL–1 was added in 2006. Sequential inoculations on the primary and first trifoliate leaves were made 10 and 20 d after sowing, respectively. A sterilized "florists' frog" (i.e., multiple needles mounted in circles) was used for inoculation by pressing through the leaf onto a sponge submerged in the inoculum. Fourteen and 21 d after inoculation (DAI), disease evaluations were made on a 1 to 9 scale, where 1 = no visible CBB symptoms, 3 = an isolated, small chlorotic zone around necrotic lesions of <25% of the inoculated area, 5 = chlorotic zones around necrotic lesions joined within <50% of the inoculated area, 7 = complete chlorosis of inoculated area and chlorotic lesions extending beyond the inoculated area, and 9 = severely diseased with large chlorotic lesions also in uninoculated areas. On the evaluation day, the highest disease score for either inoculated leaf for each plant was recorded. Dry bean genotypes with mean CBB scores of 1 to 3 were considered resistant, 4 to 6 were intermediate or moderately resistant, and 7 to 9 were considered susceptible. Data for each year were analyzed separately using the SAS (Version 9.1.3) GLM procedure (SAS Institute, 2004). Also, simple phenotypic correlation coefficients among Xcp isolates, their densities, and the two evaluation dates were computed.


   RESULTS AND DISCUSSION
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
REFERENCES
 
Mean squares due to common bean genotypes, Xcp isolates, and inoculum densities were highly significant (P ≤ 0.01) for both 14 and 21 DAI evaluations in 2005 and 2006 (Table 1), suggesting large effects of these factors on the CBB scores of the 31 common bean genotypes. The interaction of common bean genotypes with Xcp isolates was not significant (P > 0.05) for either evaluation date in 2005, but was highly significant for both evaluation dates in 2006. Similarly, common bean genotypes interacted with the bacterial densities only for the CBB evaluation made at 14 DAI in 2005. All other mean square values for their interaction were not significant. In contrast, the Xcp isolate x bacterial density interaction mean squares were highly significant for both evaluation dates in 2005 and 2006, and the second-order interaction mean squares were also highly significant for all evaluation dates except 21 DAI in 2006.


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  		Table 1. Mean squares from analysis of variance for 31 common bean (Phaseolus vulgaris L.) genotypes inoculated with different densities of Colorado and Wisconsin Xanthomonas campestris pv. phaseoli isolates and evaluated at 14 and 21 d after inoculation (DAI) in the greenhouse at Kimberly, ID, in 2005 and 2006.

 
Molecular diversity among and within Xcp and Xcpf isolates has been demonstrated through random amplified polymorphic DNA (RAPD), restriction fragment length polymorphism, and repetitive element–polymerase chain reaction (López et al., 2006; Mahuku et al., 2006; Mkandawire et al., 2004). There was also a relative predominance of a specific group of Xcpf isolates in East Africa (Mkandawire et al., 2004) that was also found in Spain (López et al., 2006), but not in the Americas. Similarly, López et al. (2006) and Mkandawire et al. (2004) reported the existence of considerable pathogenic diversity among Xcp and Xcpf isolates. For example, the Xcp isolates from East Africa were less pathogenic on the small-seeded Middle American common bean but highly pathogenic on the large-seeded Andean common bean; however, the Xcp isolates from the Americas were equally pathogenic on common bean of both gene pools. Avila et al. (1998) also reported pathogenic diversity among the Xcp and Xcpf isolates from Brazil. These results could provide a basis for grouping of the Xcp isolates into distinct races and for the identification of a useful set of cultivars of the common (Zapata, 1997) and tepary (Zapata and Vidaver, 1987) bean to differentiate those races.

Based on the individual CBB scores as well as the overall mean of the 31 common bean genotypes for bacterial densities and DAI evaluations, it is evident that the Wisconsin Xcp isolate was far more aggressive than the Colorado Xcp isolate (Table 2). Furthermore, at least in 2006, there was highly significant interaction between common bean genotypes and Xcp isolates (Table 1). These results should provide further credence and support for classification of Xcp isolates into distinct races based on their pathogenicity on the common (Zapata, 1997) and tepary (Zapata and Vidaver, 1987) bean. The significant common bean genotype x Xcp isolate interactions could be due, however, to either non-crossover or crossover interactions. Upon close examination of the CBB scores in Table 2, it is evident that several common bean genotypes (e.g., XAN 112, ICA Pijao, ICB 6, USDK-CBB-15, and USPT 73) were susceptible to the Wisconsin Xcp isolate at all densities and DAI evaluations in 2005 and 2006. They were resistant (disease score ≤3) or intermediate (disease score 4–6), however, to the Colorado Xcp isolate for both evaluation dates, at least at the lowest bacterial density (5 x 107 cfu mL–1) in 2005 or 2006. In contrast, no common bean genotype resistant to the Wisconsin Xcp isolate even at the lowest bacterial density at both DAI evaluations in 2005 or 2006 was susceptible to the Colorado Xcp isolate at any density or DAI evaluation. Thus, there were no crossover interactions between the 31 common bean genotypes and Xcp isolates. Therefore, despite large quantitative differences in aggressiveness between the two Xcp isolates, there was no evidence of crossover interactions in pathogenicity to warrant classification of the Xcp isolates into races, and there was no indication of a differential set of common bean cultivars.


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  		Table 2. Mean common bacterial blight score (1–9) for 31 common bean genotypes inoculated with different densities of Colorado and Wisconsin Xanthomonas campestris pv. phaseoli isolates and evaluated at 14 and 21 d after inoculation in the greenhouse at Kimberly, ID, in 2005 and 2006.

 
Because both Xcp and Xcpf pathogens may occur in the same production region and large quantitative differences in aggressiveness could be found between their pathogenic isolates, a periodic survey and characterization of the bacterial population should be performed and the most aggressive isolates used for germplasm screening, breeding, and genetics studies. For example, until recently we were using the Colorado Xcp isolate that was collected from one of the highest yielding pinto bean cultivars, Bill Z (Singh et al., 2007). Since 2005, however, we have been using the Wisconsin Xcp isolate in our routine breeding program. Thus, some germplasm lines (e.g., USDK-CBB-15, Miklas et al., 2006) and cultivars (e.g., Montcalm) that were considered resistant or intermediate were found to be susceptible when inoculated with the Wisconsin Xcp isolate (Table 2). Continued use of a weaker isolate such as the Colorado Xcp could have led to development of CBB-resistant germplasm and cultivars with limited adaptation and demand by common bean producers in the USA and elsewhere if more aggressive isolates of Xcp occur there. Researchers using aggressive strains in the greenhouse must take necessary precautionary measures, however, to avoid its escape into the open. For example, because of the strict seed laws and zero tolerance for bacterial diseases in Idaho, it is not possible to carry out field evaluations. The greenhouse screening of bacterial, fungal, and viral diseases is carried out between November and March, and all infected plants and soils are autoclaved before disposing of them in safe dumpsters. Furthermore, a second crop is taken of harvested plants in the pathogen-free greenhouse before field plantings.

For germplasm screening, genetics, and breeding purposes, common bean researchers have used Xcp and Xcpf at 107 to 5 x 108 cfu mL–1 (Asensio-Manzanera et al., 2006; Navarrete and Acosta, 2000; Miklas et al., 1996). Except for 5 x 107 cfu mL–1 of the Colorado Xcp isolate in 2005, highly significant positive phenotypic correlations between the Xcp isolates, densities, and DAI evaluations were recorded (Table 3). From these results, it may be tempting to conclude that similar results will be expected irrespective of the Xcp isolates, densities, and DAI evaluations used. From closer examination of Table 2, however, it should be obvious that a density of 5 x 107 cfu mL–1 or less of weak Xcp isolates may not differentiate among CBB susceptible, intermediate, and resistant common bean genotypes in some greenhouse environments (e.g., 2005). Similarly, dry bean genotypes may be falsely classified when CBB evaluations are made at 14 DAI or fewer days even when inoculated with a more aggressive Xcp isolate. For example, the landrace great northern Montana no. 5 was classified as intermediate in both 2005 and 2006 at 5 x 107 cfu mL–1 of the Wisconsin Xcp isolate when evaluated at 14 DAI (Table 2), but it had a susceptible reaction at 21 DAI. Under field conditions once the crop becomes infected, the pathogen may survive and later cause more severe infection. Thus, if an early infection occurs and environmental conditions are favorable, disease severity may continue to increase; higher levels of CBB resistance would be required. Breeders using greenhouse or field environments should not rely on a limited-term resistance but select for resistance that lasts throughout the growing season. Similarly, use of an adequate inoculum density of a pathogenic Xcp isolate that maximizes differences among common bean genotypes is essential. The use of too high a density, such as 5 x 109 cfu mL–1, of a highly aggressive Xcp isolate may eliminate potentially good germplasm. Thus, the choice of pathogen isolates, their densities, and timing of CBB evaluations are crucial for common bean germplasm screening, genetics, and breeding. These factors should, therefore, be determined carefully for the targeted production region before initiating any study.


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  		Table 3. Phenotypic correlation coefficients for common bacterial blight reaction between and within Xanthomonas campestris pv. phaseoli isolates from Colorado and Wisconsin inoculated at different densities and evaluated at 14 and 21 d on 31 common bean genotypes in the greenhouse at Kimberly, ID, in 2005 (above diagonal) and 2006 (below diagonal).

 
Twenty-seven of the 31 genotypes represented the most diverse group of CBB-resistant common bean germplasm identified or developed during the past 65 yr in the Americas (Table 2). Eight were common bean landraces or improved breeding lines or cultivars, six were derived from interspecific crosses between the common and scarlet runner bean, four were derived from interspecific crosses between the common and tepary bean, and nine possessed pyramided CBB resistance from two or more Phaseolus species. Furthermore, the small-seeded (e.g., Colima 9, G 1320, and Tamaulipas 9-B) and medium-seeded (25–40 g [100 seed weight]–1; e.g., Montana no. 5) common bean, scarlet runner bean, and tepary bean imparting any levels of CBB resistance are all of Mexican or Central American origins. Beaver et al. (1992) reported field resistance in eight indeterminate red mottled landraces from the Caribbean. Under heavy disease pressure in the field at Santander de Quilichao, Colombia, however, large-seeded common bean landraces of Andean origin possessing CBB resistance were not found despite searching through thousands of germplasm accessions (Singh and Muñoz, 1999). Thus, unlike Colletotrichum lindemuthianum (Sacc. & Magn.) Bri. & Cav. (the cause of anthracnose), and Uromyces appendiculatus (Pers.) Ung. (the cause of common bean rust), it is highly unlikely that Xcp and Xcpf co-evolved or developed affinity with two common bean gene pools in the Americas. Until unequivocal evidence for the existence of CBB resistance genes in the Andean counterparts is found, the claim (Mkandawire et al., 2004) and search for the host–pathogen co-evolution would be unfounded, at least in the Americas. The Americas are the primary centers of origin and domestication of all Phaseolus species (Debouck, 1999; Freytag and Debouck, 2002).

From CBB scores in Table 2, the following conclusions may follow. First, the level of CBB resistance was low in common bean landraces, breeding lines, and cultivars. Similarly, the six IBLs derived from crosses of the common bean with scarlet runner bean had low levels of CBB resistance. Second, the four IBLs derived from tepary bean had relatively higher levels of CBB resistance than that of the common bean or IBLs derived from the scarlet runner bean. Third, the tepary-bean-derived IBLs did not have as high CBB resistance as would have been expected or needed to provide adequate protection against a heavy pressure of an aggressive Xcp pathogen. Fourth, as would be expected, common bean genotypes with pyramided resistance from the tepary and one or more Phaseolus species had the highest levels of CBB resistance. For production regions such as Wisconsin, where aggressive Xcp pathogens are endemic, and for broader adaptation to production regions where the Xcp and Xcpf variability is unknown, breeders should only deploy pyramided CBB resistance. Furthermore, because some tepary bean accessions have exceptionally high levels of CBB resistance (Singh and Muñoz, 1999; Urrea et al., 1999; Zapata et al., 1985), concerted efforts would be justified to introgress higher levels of CBB resistance from the tepary to the common bean.

Drijfhout and Blok (1987), Freytag (1989), and Urrea et al. (1999) reported monogenic or digenic dominant control of CBB resistance in tepary bean. Moreover, McElroy (1985) and Urrea et al. (1999) also reported quantitative inheritance with a few quantitative trait loci (QTL) with small and large effects responsible for CBB resistance in tepary bean. Resistance to CBB in common bean, however, is quantitatively inherited (Aggour and Coyne, 1989; Silva et al., 1989) and controlled by >20 QTL with small to medium effects distributed across most of the 11 common bean chromosomes (Miklas et al., 1996; Park et al., 1998; Tar'an et al., 2001; also see review by Kelly et al., 2003; Miklas and Singh, 2006). This may partially explain why not a single common bean genotype with CBB resistance derived from the three Phaseolus species of the primary, secondary, and tertiary gene pool alone provided resistance to the more aggressive Xcp isolate from Wisconsin, especially at higher densities or when evaluated at 21 DAI. Furthermore, because no crossover interactions were observed between the Xcp isolates and common bean genotypes, and only genotypes with pyramided CBB resistance offered protection against the more aggressive Xcp isolate, the search for identification of races among Xcp pathogens using currently known common bean genotypes would be difficult if not impossible.

Yu et al. (2000) compared the cost of direct disease vs. indirect screening using RAPD and sequence characterized amplified region (SCAR) markers of 138 F5 breeding lines derived from ‘Envoy’/HR67 common bean population. The marker-assisted screening was about 33% cheaper than the direct disease screening. Furthermore, prediction for CBB resistance with BC420 SCAR marker was 94.2% accurate. The presence of SAP6 marker derived from great northern Montana no. 5 (Miklas et al., 2003) was confirmed in USPT-CBB-1 (Miklas et al., 2001), which was also believed to have CBB resistance from the scarlet runner bean. The USDK-CBB-15 breeding line (Miklas et al., 2006) was the first with pyramided CBB resistance that was developed using molecular markers; however, the levels of CBB resistance of USPT-CBB-1 and USDK-CBB-15 were not as high or as effective against the two Xcp isolates as the other seven breeding lines (G 17341, VAX 3, VAX 4, VAX 5, VAX 6, Wilkinson 2, and XAN 309) carrying the pyramided resistance developed through direct selection. Duncan et al. (2006), using a double-cross population, also showed that direct selection was more effective for breeding for the highest levels of CBB resistance than marker-assisted selection. Thus, depending on the quality and number of available markers, caution must be exercised while using marker-assisted selection alone. The use of much larger populations, simultaneous selection for maximum number of markers linked with small- and large-effect QTL controlling CBB resistance, and alternative breeding methods such as gamete selection (Asensio-Manzanera et al., 2006; Singh, 1994) or recurrent selection (Singh et al., 1999) may be required. Also, marker-assisted selection may need to be combined with periodic direct disease screening to expedite introgression and pyramiding of the high levels of CBB resistance into common bean germplasm lines and cultivars.


   ACKNOWLEDGMENTS
 
We thank Howard Schwartz and David Webster for reviewing the manuscript and Howard Schwartz, Robert Gilbertson, and Robert Duncan for supplying the bacterial isolates.


   NOTES
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 NOTES
ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
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Received for publication December 6, 2006.


   REFERENCES
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 MATERIALS AND METHODS
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