Published online 2 December 2005
Published in Crop Sci 46:131-135 (2006)
© 2005 Crop Science Society of America
677 S. Segoe Rd., Madison, WI 53711 USA
CROP BREEDING,GENETICS & CYTOLOGY
Gamete Selection for Resistance to Common and Halo Bacterial Blights in Dry Bean Intergene Pool Populations
M. Carmen Asensio-S.-Manzaneraa,
Carmen Asensioa and
Shree P. Singhb,*
a Instituto Tecnológico Agrario de Castilla y León, Apdo.172, 47080 Valladolid, Spain
b Univ. of Idaho, 3793N 3600E, Kimberly, ID 83341-5076
* Corresponding author (singh{at}kimberly.uidaho.edu).
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ABSTRACT
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The common [caused by Xanthomonas campestris pv. phaseoli (Smith) Dye (Xcp) and X. campestris pv. phaseoli var. fuscans (Xcpf)] and halo bacterial blights [caused by Pseudomonas syringae pv. phaseolicola (Burkh.) Young et al. (Psp)] are seed-borne diseases that cause severe yield losses in dry and snap bean (Phaseolus vulgaris L.) worldwide. Use of cultivars resistant to these diseases is pivotal for their integrated control and to facilitate production and distribution of pathogen-free seed. Our objective was to use gamete selection for resistance to both bacterial blights. Two intergene pool four-way crosses, namely ZARA III = Wilkinson 2/‘Montcalm’//‘Casasola’/‘Harris’ and ZARA IV = ‘Edmund’/Wilkinson 2//Casasola/BRB 131 were made. Selection for resistance to both bacterial blights was practiced from F1 to F4 in the greenhouse or field at Valladolid, Spain. The F4–derived F5 breeding lines resistant to both blights were screened for Bean common mosaic virus (BCMV), Bean common mosaic necrosis virus (BCMNV), and common bacterial blight in the greenhouse at Kimberly, ID, and for halo blight at Filer, ID, in 2001. They were also evaluated for the two bacterial blights, growth habit, seed color, and 100-seed weight in the field at Valladolid in 2002. The proportion of resistant, intermediate, and susceptible plants was similar in both F1, and selection was effective from the F1 to F4 for both bacterial blights. Nonetheless, population ZARA IV had relatively lower halo blight scores than ZARA III (1.8–4.1 vs. 2.6–6.5). The contrary occurred for common bacterial blight. Five breeding lines resistant or intermediate to both diseases were obtained from two of 147 F1 plants in ZARA III. ZARA IV produced nine breeding lines resistant to both bacterial blights that originated from four of 128 F1 plants. Some breeding lines had a higher resistance to both bacterial blights than their parents indicating transgressive segregation, and all carried the I allele for resistance to BCMV. We suggest using gamete selection for introgression and pyramiding of resistance to both bacterial blights with multiple-parent populations in dry bean.
Abbreviations: BCMV, Bean common mosaic virus • BCMNV, Bean common mosaic necrosis virus • Psp, Pseudomonas syringae pv. phaseolicola • cfu, colony forming units • QTL, quantitative trait loci • Xcp, Xanthomonas campestris pv. phaseoli • Xcpf, X. campestris pv. phaseoli var. fuscans.
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INTRODUCTION
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YIELD LOSSES in dry bean because of common bacterial blight and halo bacterial blight may range from 10 to 40% depending on disease pressure, environmental condition, and cultivar. Both bacterial diseases also reduce seed and pod quality, market value, and are seed-transmitted. Attributing yield loss to either bacterial blight separately is not feasible when they occur in the same field at the same time such as in the north and central Spain.
Variation in virulence among isolates of Xcp and Xcpf is unclear. For example, Ekpo and Saettler (1976), among others, reported differences in virulence among Xcp isolates. In contrast, Jara et al. (1999) did not observe the host–pathogen interaction of any consequence after exposing 20 Xcp isolates of different geographical origin to the VAX breeding lines (Singh and Muñoz, 1999) that carry a high level of pyramided resistance from the common and tepary (P. acutifolius A. Gray) bean. Taylor et al. (1996a) reported nine races of Psp using eight differential cultivars. Asensio et al. (1998) also found pathogenic variation in Psp from central Spain.
Resistance to common bacterial blight can be monogenic dominant (Urrea et al., 1999), recessive (Adams et al., 1988), or inherited quantitatively (Silva et al., 1989; Urrea et al., 1999). There are >20 resistance quantitative trait loci (QTL) of large and small effects distributed across all 11 chromosomes (see review by Kelly et al., 2003). One of the major QTL found in Great Northern Nebraska #1 Sel 27 (GNN #1 Sel 27) and linked with SCAR marker SAP6 was derived from the great northern dry bean landrace Montana 5 and not the tepary bean as previously thought (Miklas et al., 2003). Furthermore, because GNN #1 Sel 27 has only moderate level of common bacterial blight resistance and has been the most commonly used source, very little progress was achieved after decades of breeding. However, breeding lines such as XAN 159, Wilkinson 2, and VAX 1 to VAX 6 are now available, some of which have pyramided resistance from common and tepary bean (Singh and Muñoz, 1999).
The Psp race-specific resistance to halo blight can be inherited quantitatively or by a single dominant or recessive allele (Asensio et al., 1993; Taylor et al., 1978, 1996b). Ariyarathne et al. (1999) reported resistance QTL in BelNeb-RR-1/A 55 dry bean population. Using the same population, Fourie et al. (2004) identified three independent dominant genes, namely Pse-1 (for Psp Races 1, 7, and 9), Pse-3 (for Psp Races 3 and 4), and Pse-4 (for Psp Race 5) that mapped to the same genomic region as three of the QTL. None of the race-specific genes impart resistance to the most widely distributed and virulent Psp Race 6. Race-nonspecific resistance was found in cultivars such as GNN #1 Sel 27 and PI 150414 (Taylor et al., 1978, 1996b).
BCMV is a seed-transmitted disease, and infected plants may be stunted, show mosaic in the leaves, and/or possess fewer, smaller, and deformed pods (Strausbaugh et al., 2003). Yield losses from BCMV average 50% but may reach up to 100% depending on cultivar and the stage of crop infected. The strains BCMNV (e.g., NL-3, NL-5) also produce similar symptoms on susceptible cultivars lacking the dominant (I) and recessive (bc-1, bc-12, bc-2, bc-22, and bc-3) resistance alleles (Drijfhout, 1978). But, they produce local, venal, and systemic top necrosis and eventual plant death of genotypes that possess only the dominant I allele. The dominant I allele imparts resistance to all known BCMV strains and prevents their systemic infection or movement in the plant. All recessive resistance alleles except bc-3 confer strain-specific resistance. The bc-3 imparts resistance to all BCMV and BCMNV strains. The bc-u allele is not strain specific and has no effect by itself, but it is necessary for the expression of the other recessive bc alleles including bc-3, especially in the absence of the I gene. Molecular markers for the I and some recessive resistance alleles including bc-3 are available (see review by Kelly et al., 2003).
The small- (<25 g 100-seed weight–1) and medium-seeded (25–40 g 100-seed weight–1) Middle American dry bean often yield significantly higher than their large-seeded (>40 g 100-seed weight–1) Andean counterparts (White et al., 1992). They also possess more favorable alleles and QTL that impart higher level of resistance to drought (Terán and Singh, 2002), low soil fertility (Singh et al., 2003), BCMV and BCMNV (Drijfhout, 1978), common bacterial blight (Singh and Muñoz, 1999), halo blight (Taylor et al., 1978, 1996b), and other biotic and abiotic stresses (see review by Singh, 2001). However, the intergene pool transfer of favorable alleles and QTL can be challenging because of the increased genetic distance and associated poor combining ability and incompatibility problems (Singh, 2001).
The common and halo bacterial blights and BCMV are major production constraints of dry and snap bean worldwide. While there has been a remarkable progress in breeding for resistance to BCMV in most market classes of dry and snap bean, cultivars resistant to both bacterial blights with or without BCMV resistance are not yet available. In Spain, BCMV is present in all dry bean production areas (Saíz et al., 1995), and the common and halo bacterial blights occur in the north and central regions (Asensio et al., 1998). The pedigree method of selection was used to introgress resistance to BCMV and halo blight from great northern ‘Jules’ into local landraces with some success (Asensio et al., 1993). The objective of this research was to use gamete selection (Singh, 1994) in intergene pool populations for simultaneous improvement of resistance to common and halo bacterial blights. Subsequently, the resulting F4–derived F5 breeding lines were also evaluated for BCMV and BCMNV.
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MATERIALS AND METHODS
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Two intergene pool four-way crosses, namely ZARA III = Wilkinson 2/Montcalm//Casasola/Harris, and ZARA IV = Edmund/Wilkinson 2//Casasola/BRB 131 were developed for this experiment. Wilkinson 2 has resistance to common bacterial blight and BCMV, a determinate upright growth habit Type I, and medium-sized white seed (Table 1). Montcalm has a Type I growth habit, large dark red kidney seed, I resistance allele for BCMV, and low level of resistance to common bacterial blight. Casasola has resistance to common bacterial blight, growth habit Type I, and large white seed. Great northern Harris has low level of resistance to halo blight and an indeterminate prostrate growth habit Type III. White small-seeded Edmund has growth habit Type I, I allele, and intermediate level of resistance to halo blight controlled by a recessive gene (Taylor et al., 1996b). Breeding line BRB 131 has the I and recessive bc-3 resistance alleles for BCMV and BCMNV.
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Table 1. Growth habit, seed color, 100-seed weight, and reaction to BCMV, BCMNV, and the common and halo bacterial blights of F4–derived F5 dry bean breeding lines selected from two intergene pool four-way crosses ZARA III and ZARA IV and parents evaluated in the greenhouse at Filer and Twin Falls, ID, in 2001 and in the field at Valladolid, Spain, in 2002.
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All six parents and the F1 of the two intergene pool four-way crosses were inoculated in the greenhouse for selection for the common and halo bacterial blights at Valladolid, Spain. A mixture of Psp isolates SITA630 and SITA654 were used to inoculate the two primary leaves according to Taylor et al. (1978). The Xcp isolate SITA659 was inoculated in the first trifoliolate leaf using the multiple-needle technique (Singh and Muñoz, 1999). In all inoculations, the pathogen concentration used was 1 x 103 cfu/mL. The disease evaluation was made 7 to 10 d after each inoculation on a 1-to-9 scale whereby plants scoring 1 to 3 were considered resistant, 4 to 6 intermediate, and 7 to 9 susceptible (Aggour et al., 1989). The F1 plants with intermediate or resistant reaction (scores 1 to 6) to both bacterial blights were harvested individually. The F1–derived F2 (F1:2) families were evaluated for both bacterial blights in the field. Inoculation and evaluation for both pathogens in the field were compatible and no apparent interference observed. An average of ten plants per F1:2 family were evaluated. Field inoculation for halo blight was made at the first trifoliolate leaf stage and for common bacterial blight at bloom with a backpack solo sprayer. One week later, one trifoliolate leaf per plant was also inoculated for common bacterial blight by the multiple-needle technique. Evaluation for both bacterial diseases was done 14 to 21 d after each inoculation. Selection between and within families was made, harvesting individually the two plants with the lowest disease score from each selected family. A progeny test for each disease separately was performed in the greenhouse in F3. All F2:3 families susceptible to either disease were eliminated. Ten plants per selected F4 family were evaluated simultaneously in the field for both blights. Parents and the F4–derived F5 breeding lines with the lowest scores for both bacterial blights were evaluated separately for common bacterial blight, BCMV, and BCMNV in the greenhouse at the University of Idaho, Kimberly, and for halo bacterial blight at the Seminis Vegetable Seeds Co., Filer, ID, in 2001. An average of six plants per genotype was evaluated for each disease. Inoculation and evaluation for BCMV (US-6 strain) and BCMNV (NL-3K strain) were made according to Strausbaugh et al. (2003). They were also evaluated for the two bacterial blights, growth habit, seed color, and 100-seed weight in the field at Valladolid in 2002. The LSD (P = 0.05) was used to test differences between families, breeding lines, or populations. All data were analyzed by a SAS PROC GLM statistical package (SAS Institute, 1985).
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RESULTS AND DISCUSSION
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The six parents used in the two intergene pool four-way crosses were resistant to BCMV (Table 1). Inoculation with BCMNV further indicated that Edmund and Montcalm had the I allele, and Wilkinson 2 and BRB 131 had a recessive resistance allele in addition to I. Harris and Casasola had only recessive resistance. Wilkinson 2 had the highest level of resistance to common bacterial blight in the greenhouse and field. BRB 131 and Edmund were highly susceptible to common bacterial blight in both the greenhouse and field. Thus, none of the six parents possessed a high level of resistance to all three diseases.
Plants with a susceptible, intermediate, or resistant reaction to both bacterial blights were observed in the F1 of both populations (Table 2). This segregation facilitated selection of 39% of F1 plants from ZARA III and 38% from ZARA IV with a resistant or intermediate reaction to both bacterial blights (Table 3). Similar segregation for both bacterial blights occurred within the F1-derived families in F2 and subsequent generations, although at a reduced level as the filial generations advanced. Because single-plant selection for both bacterial blights was made between and within families from the F1 to F4, and only a few plants with the lowest disease scores were saved, there was a drastic reduction in the number of plants and families selected (Table 3). Had selection not been practiced in the F1, a much larger number of families (at least 60% more) would have been advanced from the F1 to the subsequent generations, requiring considerably more resources and space to manage the two populations.
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Table 2. Frequency of resistant, intermediate, and susceptible plants and mean disease rating for the common and halo bacterial blights in the F1 of two intergene pool four-way crosses ZARA III and ZARA IV of dry bean evaluated at Valladolid, Spain, in 1998.
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Table 3. Number and mean disease score for F1–plants and their derived families selected for resistance to the common and halo bacterial blights in the F2, F3, and F4 of two intergene pool four-way crosses ZARA III and ZARA IV of common bean at Valladolid, Spain, from 1998 to 2001.
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In general, mean population score for common bacterial blight increased in the field and decreased in the greenhouse, while for halo blight, it was just the opposite (Table 3). Baggett and Frazier (1967) also found halo blight more severe in the greenhouse than in the field after inoculating the same cultivars. Coyne et al. (1967) reported that some genotypes susceptible to halo blight in the greenhouse were resistant in the field. Environmental conditions in the field are also known to influence common bacterial blight reaction (Silva et al., 1990). Bacterial disease scores often are higher with multiple-needle than with aspersion method of inoculation (Aggour et al., 1989). However, the use of multiple-needle inoculation is more labor intensive and time consuming, and, therefore, not suitable for large-scale germplasm screening in the field. In a sequential screening program in the field, Singh and Muñoz (1999) used first the aspersion method to discard all susceptible genotypes. They subsequently used the multiple-needle and razorblade inoculation techniques to develop dry bean breeding lines with the highest level of resistance to common bacterial blight from the common x tepary bean interspecific populations. In our study, the mean score in both the greenhouse and field environments seemed to have stabilized for both bacterial blights in F4 and F5 (Tables 1 and 3). The proportion of selected F3:4 families with regard to the number of selected F1 plants, were similar in both populations. Nonetheless, mean common bacterial blight score for ZARA IV tended to be higher than for ZARA III across all filial generations. On the contrary, the mean halo blight scores for ZARA IV were lower than that of ZARA III (Table 3). Selected F5 breeding lines, in general, had higher level of resistance to both bacterial blights than their parents in the greenhouse and field (Table 1), suggesting occurrence of transgressive segregation. Thus, Casasola, Montcalm, and Wilkinson 2 for common bacterial and Casasola, Edmund, Harris, and Wilkinson 2 for halo bacterial blight used in the intergene pool four-way populations very likely contributed different complementary resistance alleles and QTL that produced transgressive segregation. Valladares-Sánchez et al. (1979) also reported transgressive segregation for common bacterial blight resistance.
Despite the fact that gamete selection drastically reduced the population size from the F1 onward such that only two of 147 F1 plants gave rise to five breeding lines resistant to both bacterial blights in population ZARA III and only four of 128 F1 plants resulted in nine similar breeding lines in ZARA IV, the method was effective in introgressing and pyramiding a higher level of resistance to both bacterial blights from the Andean and Middle American parents that individually possessed a lower level of resistance (Table 1). Although it could not be known which recessive and/or dominant resistance allele or QTL were contributed by which parent, only retainment and accumulation of such favorable complementary genes from the F1 to F4 would have resulted in transgressive segregation for either bacterial blight despite the fact that in the F1 gamete selection would not have been effective on recessive resistance genes. As reviewed earlier quantitative as well as monogenic dominant and recessive resistance to common bacterial blight (Adams et al., 1988; Silva et al., 1989; Urrea et al., 1999) and halo bacterial blight (Ariyarathne et al., 1999; Asensio et al., 1993; Fourie et al., 2004; Taylor et al., 1978, 1996b) have been reported in common bean. Because selection for resistance to both bacterial blights was practiced from the F1 and only <5% F1 plants eventually produced breeding lines resistant to both diseases, to attain a higher proportion of resistant breeding lines a much higher number of F1 plants would have to be screened. Similarly, proportionately a higher number of F1 plants would need to be screened as the number of traits to be simultaneously improved increases.
In population ZARA III, 100-seed weight of all breeding lines except ZARA III-394–2-6–22–3 was smaller (Table 1) than what is often desired in Spain (>50 g). Nonetheless, all had growth habit Type I, and three also had white seed color desired in Spain and elsewhere in Europe, West Asia, and North Africa. In general, 100-seed weight of the nine breeding lines from ZARA IV population was much smaller than their large-seeded Andean parents, although all had white seed color and growth habit Type I. Thus, as would be expected, from such genetically broad-based intergene pool populations one would mostly obtain improved breeding lines that must be subsequently crossed with popular cultivars and elite breeding lines for development of new cultivars (Kelly et al., 1998; Singh, 2001). Moreover, no selection was practiced for seed characteristics, growth habit, or any other agronomic traits except resistance to diseases in any generation. For simultaneous improvement of seed, plant, maturity, and other agronomic traits for new cultivar development selected plants in the F1 or subsequent generation of ZARA III and ZARA IV should have been crossed with cultivars such as Casasola, Riñon or other popular white kidney bean. Also, for production regions where a lower level of resistance to either bacterial blight may suffice, selection for the respective level of resistance from the early generation should produce a larger number of breeding lines for subsequent evaluation for other agronomic traits and identification of new cultivars. Alternatively, gamete selection for simultaneous improvement of several traits would need to be practiced in multiple-parent crosses involving only closely related (e.g., within the same market class) elite breeding lines and cultivars.
Although no selection for BCMV or BCMNV was practiced from the F1 to F4, all 14 breeding lines were resistant to BCMV (Table 1). Because they exhibited a systemic necrosis and eventual plant death when inoculated with the BCMNV strain NL-3K, it is inferred that each carried the dominant I allele for BCMV resistance (Drijfhout, 1978). Three of the four parents in each population possessed the I allele, which produced exceptionally higher number of BCMV resistant breeding lines without any selection in early generations. In contrast, none of 14 breeding lines had a recessive resistance allele present in BRB 131, Harris, and Wilkinson 2. Because gamete selection based on direct disease screening would be ineffective in retaining such recessive resistance alleles, use of molecular markers would be advisable for their selection. Furthermore, all 14 breeding lines may need to be evaluated for maturity, yield, and other agronomic traits across contrasting environments before they are used for development of new cultivars.
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ACKNOWLEDGMENTS
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This research was a part of the doctoral dissertation submitted to the Universidad de Lerida (Spain) by M.C. Asensio-S.-Manzanera, who was funded by a fellowship from the Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA). This research was supported with grant number 1FD97-0308-C03-02 from the FEDER (European Union) and Fondo Nacional de I+D (Spain). We are very grateful to Dr. David Webster for permission to use the greenhouse of the Seminis Vegetable Seeds Co., Filer, ID, and providing Psp inoculum.
Received for publication March 8, 2005.
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REFERENCES
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ABSTRACT
INTRODUCTION
