In 2003 and 2004, field studies were conducted at six sites across Canada to ..... 1776c. 2221ab. 1548b. Navigator. 3842ab. 2101d. 4530a. 2277c. 1965bc.
The performance of dry bean cultivars with and without common bacterial blight resistance in field studies across Canada C. L. Gillard1, R. L. Conner2, R. J. Howard3, K. P. Pauls4, L. Shaw5, and B. Taran6 1
University of Guelph, Ridgetown Campus, Ridgetown, Ontario, Canada N0P 2C0; 2Agriculture Agri-Food Canada, Morden, Manitoba, Canada R6M 1R1; 3Alberta Agriculture CDC South, Brooks, Alberta, Canada TIR IE6; 4 University of Guelph, Guelph, Ontario, Canada N1G 2W1; 5Agriculture Agri-Food Canada CSIDC, Saskatoon, Saskatchewan, Canada S0L 2N0; and 6University of Saskatchewan CDC, Saskatoon, Saskatchewan, Canada S7N 5A8. Received 19 March 2008, accepted 16 October 2008. Gillard, C. L., Conner, R. L., Howard, R. J., Pauls, K. P., Shaw, L. and Taran, B. 2009. The performance of dry bean cultivars with and without common bacterial blight resistance in field studies across Canada. Can. J. Plant Sci. 89: 405410. Common bacterial blight (CBB) is a serious seed-borne disease in dry beans (Phaseolus vulgaris). Plant breeders have focused on genetic resistance to control this disease, and this led to the release of the first resistant cultivar (OAC Rex) in 2002. In 2003 and 2004, field studies were conducted at six sites across Canada to measure the impact of CBB resistance on dry bean seed yield. Two resistant and four susceptible cultivars were evaluated in noninoculated and inoculated experiments at each site. In the noninoculated experiments, the CBB incidence was very low and there were no treatment differences for measurements of leaf disease. Significant disease pressure occurred in the inoculated experiments at 7 of 12 site-years. Both resistant cultivars usually had less leaf disease than the susceptible cultivars. Yield comparisons between the inoculated and noninoculated experiments were conducted using a yield index calculation to estimate the impact of CBB on the yield of the cultivar. OAC Rex and HR67 had a mean yield advantage of 23.1 and 13.8%, respectively, compared with the mean of the four susceptible cultivars. This is similar to the yield advantage previously reported in the literature. Key words: Dry bean, Phaseolus vulgaris, Xanthomonas axonopodis pv. phaseoli, resistance, yield Gillard, C. L., Conner, R. L., Howard, R. J., Pauls, K. P., Shaw, L. et Taran, B. 2009. Performance des cultivars de haricots re´sistants ou pas a` la bruˆlure bacte´rienne dans les champs expe´rimentaux du Canada. Can. J. Plant Sci. 89: 405410. La bruˆlure bacte´rienne est une grave maladie du haricot (Phaseolus vulgaris) ve´hicule´e par la semence. Pour en venir a` bout, les obtenteurs se sont tourne´s vers la ge´ne´tique, ce qui a de´bouche´ sur l’homologation du premier cultivar re´sistant (OAC Rex) en 2002. En 2003 et 2004, des e´tudes sur le terrain effectue´es a` six endroits disse´mine´s au Canada devaient e´tablir l’incidence de cette re´sistance ge´ne´tique sur le rendement grainier du haricot. A` chaque site, les auteurs ont e´value´ les deux varie´te´s re´sistantes et quatre cultivars sensibles lors d’expe´riences incluant ou pas l’inoculation de la maladie. Sans inoculation, l’incidence de la bruˆlure bacte´rienne e´tait tre`s faible et les auteurs n’ont note´ aucune diffe´rence entre les traitements quant a` la surface des feuilles attaque´es par la maladie. Sur les parcelles ou` il y avait eu inoculation, la maladie a exerce´ une pression sensible sur la culture sept anne´es-sites sur douze. Le feuillage des deux cultivars re´sistants pre´sentait toutefois moins de dommages que celui des cultivars sensibles. Les auteurs ont compare´ le rendement des parcelles avec et sans inoculation au moyen d’un indice permettant d’estimer les effets de la bruˆlure bacte´rienne sur le rendement du cultivar. Au niveau du rendement, OAC Rex et HR67 jouissent d’un avantage moyen respectif de 23,1% et de 13,8% comparativement aux quatre cultivars sensibles. Ces re´sultats concordent avec l’avantage de rendement signale´ ante´rieurement dans la litte´rature. Mots cle´s: Haricot, Phaseolus vulgaris, Xanthomonas axonopodis pv. phaseoli, re´sistance, rendement
Infection of the pods results in the formation of sunken dark red-brown lesions and may cause a discoloration of the seed (Scott and Michaels 1992; Singh and Munoz 1999). Traditional control methods include (1) production of ‘‘clean’’ seed from regions presumed to be disease free, (2) antibiotic seed treatments and (3) foliar bacteriacides such as copper sulphate (Schwartz et al. 2005). In Canada, the use of clean seed is considered to be the primary control method (Bailey et al. 2003). Canadian seed production regions typically have heavy rainfall and high humidity, which favours the build up
Common bacterial blight (CBB) is a serious seed-borne disease in the dry bean (Phaseolus vulgaris L.) production regions in Canada (Bailey et al. 2003) and throughout the world (Coyne and Schuster 1974). The causal agent of this disease is Xanthomonas axonopodis pv. phaseoli (Smith) Vauterin et al. (Xap) [syn. X. campestris pv. phaseoli (E.F. Smith) Dye]. Common bacterial blight attacks all the aerial parts of the bean plant (Schwartz et al. 2005). Initially, CBB first appears on the leaves as water soaked lesions that eventually turn brown and are surrounded by a chlorotic border. 405
406 CANADIAN JOURNAL OF PLANT SCIENCE
of CBB in seed lots, which in turn limits the number of generations of seed production. Sectors of the dry bean industry have forsaken Canadian seed production and spend millions of dollars each year, purchasing clean seed from US seed production regions (Coyne and Schuster 1973a; Scott and Michaels 1992). Recent increases in transportation costs, along with other importation issues, have dramatically increased the cost of imported seed. To remain globally competitive, Canadian growers need a solution to this problem. The development of CBB-resistant cultivars will allow for local seed production, which will reduce seed costs and pesticide use while maintaining the seed yield and quality commonly associated with US seed. The development of resistant cultivars is considered to be the most effective method for reducing seed yield and quality losses caused by CBB (Singh and Munoz 1999). Many North American dry bean breeders are currently developing CBB-resistant cultivars. These cultivars provide a new method of disease control. The most resistant cultivars are derived from crosses between P. vulgaris and Phaseolus acutifolius A. Gray (Coyne and Schuster 1973b). In Ontario, two breeding programs are using this genetic material to develop resistant lines. Most of the initial lines had some undesirable agronomic or quality characteristics (Coyne and Schuster 1973a; Park et al. 1998) that possibly were inherited from P. acutifolius. HR67 is a resistant navy bean line from Agriculture and Agri-Food Canada at Harrow Ontario (Yu et al. 2000). It was derived from a cross with XAN159, which was developed from an interspecific cross between P. vulgaris and P. acutifolius (accession PI31943; Thomas and Waines 1984). OAC Rex was developed from a similar cross between P. vulgaris and P. acutifolius (accession PI440795; Parker 1985; Scott and Michaels 1992). The resistant navy bean line OAC 95-4 had superior yield and acceptable cooking quality. This line was registered in 2002 as OAC Rex, and became the first CBB-resistant cultivar in Canada (Michaels et al. 2006). In the future as new resistant cultivars are released, Canadian-based seed multiplication will expand and seed costs should decrease. In preparation for this, the value of CBB resistance needs to be determined. The purpose of this study was to document the impact of CBB resistance on disease development and dry bean performance in field studies across Canada. MATERIALS AND METHODS In 2003 and 2004, field studies were established each year at six sites (Brooks, AB; Outlook and Saskatoon, SK; Morden, MB; and Exeter and Elora, ON) in cooperation with scientists at these sites. These locations are representative of the major dry bean production regions in Canada. Two separate experiments were conducted at each location. The first experiment was inoculated with a mixture of four strains of Xap to produce CBB infection. The second experiment was not
inoculated, and every attempt was made to keep it disease free. The experiments were physically separated by at least 20 m. This distance minimized the chance of infection in the disease-free experiment, and yet gave similar environmental conditions for each experiment. The treatments included two resistant (HR 67 and OAC Rex) and four susceptible (AC Compass, Envoy, Navigator, and CDC White Cap) navy bean cultivars. Cultivars were selected based on their relative maturity, plant architecture, availability and popularity with dry bean growers. Each experiment was set up as a randomized complete block design with four replications. A non-host crop for CBB (e.g., soybeans) was planted between successive plots and between blocks, to minimize any secondary disease transmission. Seed was obtained from a diseasefree source and was treated with streptomycin sulphate and diazinon/captan/thiophanate-methyl or DCT (Norac Concepts, Guelph, ON, Canada) to minimize the development of any seed-borne diseases. Each cooperator planted the experiments using their normal seeding methods and equipment. This resulted in some differences between sites. The Morden and Saskatoon sites used four row plots, while the other sites used two row plots. Row length varied from 3.0 m at Outlook to 6.0 m at Brooks, Elora and Exeter. The row spacing varied from 0.30 m (Morden and Saskatoon) to 0.60 m (Outlook, Brooks and Elora) to 0.75 m (Exeter). The seeding rate was 4756 seeds m 2 at the narrow row sites, and 2732 seeds m 2 at the wide row sites. Each cooperator was allowed to make their own crop management decisions, including weed control and fertility, while ensuring that the experiment was grown under recognized dry bean production practices for their region of the country. Initial cultures of the four Xap strains collected from Ontario dry bean fields were used at each location to produce CBB inoculum, using standard methods for Xap (Park and Dhanvantari 1987). The four Xap strains were not considered to be different pathotypes. The susceptible cultivars in this study were susceptible to each strain, and the resistant cultivars were resistant to each strain. The cultures were diluted with nonclorinated tap water to produce a bacterial concentration, which corresponds to 1.0 108 colony forming units mL 1. Inoculation began at the fourth trifoliate leaf stage and was applied using flat fan sprayer nozzles at a rate between 120 and 167 mL m 1 of row0.2% Sylgard 309 (Dow Corning Inc., Midland, MI). Four sites (Exeter, Saskatoon, Outlook and Brooks) repeated the inoculation at the sixth trifoliate leaf stage in each year of the study. To enhance disease infection, cooperators applied the inoculum at night, when the canopy humidity was high. At each site except Morden, supplemental irrigation was applied before inoculation to increase canopy humidity. Leaf disease incidence was measured as the percentage of leaves infected. Leaf disease severity was measured
GILLARD ET AL. * COMMON BACTERIAL BLIGHT RESISTANCE
using a 05 scale, where 0no infection, 1 B510%, 3 1025%, 4 2550%, 550100% lesion area on the infected leaves (Mutlu et al. 2005). Seed yield (adjusted to 18% moisture) was measured and used to calculate a yield index, which was used to compare the difference in yield of the noninoculated and inoculated experiments. The index measures the treatment response to CBB infection, while removing the yield effects from other factors such as genetic yield potential. It was calculated using the following formula: Yield from noninoculated plot yield from inoculated plot100 Yield from noninoculated plot
Small yield differences between the noninoculated and inoculated plots for an individual cultivar would result in a low index value, while large yield differences between the noninoculated and inoculated plots would result in a high index value. If there was little disease pressure in the noninoculated experiment, and moderate to severe disease pressure in the inoculated experiment at the same site, then a cultivar with a low index value should have some resistance to CBB, while a cultivar with a relatively high index value should be considered susceptible to CBB. A cultivar could have a negative index value if the yield in the inoculated plot was higher than the yield in the noninoculated plot. This occurred at sites with low disease pressure in the inoculated experiment. The statistical analysis used the mixed procedure in SAS version 9.1 (SAS Institute, Cary NC). After an initial analysis, 5 site-years (Elora 2003 and 2004, Brooks 2004 and Saskatoon 2003 and 2004) were excluded because of incomplete data sets. For the remaining 7 site-years, the noninoculated and inoculated experiments were analyzed separately. RESULTS AND DISCUSSION The leaf ratings for disease incidence and severity are presented in Tables 1 and 2, respectively. In the noninoculated experiment, most of the sites were disease free. At sites with low disease levels, there were no significant (P B0.05) treatment differences. Slight anomalies appear in the data set in the inoculated experiments at the Exeter and Outlook sites in 2003 (Table 2). At both sites there was no disease incidence, but low ratings for disease severity were recorded in Envoy and AC Compass at the Exeter site and in HR67 at the Outlook site. It is likely that a few disease lesions were observed in the affected plots, but the disease incidence was below the level of detection presented in Table 1. In the inoculated experiments the disease pressure was much higher, and large treatment differences were observed at most sites. Three sites (Exeter, Morden and Outlook) have data presented from both years of the study. Each of these sites had slightly higher disease pressure in 2003 than in 2004. Based on a review of the mean monthly maximum and minimum tempera-
407
tures and precipitation for July and August, it was found that each site was slightly drier and warmer in 2003. These environmental conditions generally would not be conducive for disease development and yet the results in Tables 1 and 2 clearly demonstrate strong disease development. A detailed review of the weather data during critical times such as disease inoculation could provide some answers, but this was beyond the scope of this study. One site-year (Brooks 2003) did not provide good treatment separation for disease incidence and severity. This site is in a dry land region where irrigation is needed for crop production. In 2003, this site had low precipitation and only a small amount of irrigation was applied during the inoculation period. These factors resulted in poor disease development at the Brooks 2003 site. At most of the remaining sites, OAC Rex and HR67 had lower values than the susceptible cultivars for disease incidence and severity. This implies that OAC Rex and HR67 have resistance to CBB. In several instances, OAC Rex had slightly lower values than HR67, which suggests some differentiation between the resistant lines. The difference might be evidence that different resistance genes were contributed by the two P. acutifolius lines used to create HR67 (Yu et al. 2000) and OAC Rex (Parker 1985; Scott and Michaels 1992) or may reflect differences in gene expression conditioned by the different genome locations of the resistance genes introgressed into HR67 and OAC Rex. The major gene for resistance in OAC Rex was mapped to linkage group B5 (Ta’ran et al. 2002), whereas the major gene for resistance in HR67 is linked to the V gene on B6 (Yu et al. 2000). In all but 1 site-year (Outlook 2004), the susceptible cultivar Envoy had the highest disease incidence and severity. All four Xap strains used in this study were collected in Ontario, but they were not considered to be different pathotypes based on their reactions on the resistant and susceptible cultivars. In a recent study, Mutlu et al. (2008) stated that they have identified Xap isolates from various regions of the world that differed in their virulence on CBB-resistant cultivars. If differences in pathotypes in Xap exist in Canada, it could complicate breeding for CBB resistance and affect the durability of CBB-resistant cultivars. In the noninoculated experiments, there were significant differences between cultivars for seed yield at 6 of the 7 site-years (Table 3). At least one susceptible cultivar had yields equal to or higher than those of OAC Rex and HR67 at 6 of the 7 site-years. OAC Rex at the Outlook 2004 site is an obvious outlier in this data set. Light frost damage was recorded at this site on 2004 Aug. 20. Since OAC Rex was the latest maturing cultivar, the authors suggest this as a reason for its low yield. In the inoculated experiments, significant treatment differences for seed yield were detected at all 7 site-years. The resistant cultivars tended to have higher yields than the susceptible cultivars under high disease pressure. This trend was more evident with
408 CANADIAN JOURNAL OF PLANT SCIENCE Table 1. Leaf ratings for common blight incidence (%) for two resistant and four susceptible white pea bean cultivars at seven sites in 2003 and 2004 2003 Cultivar Noninoculated experiment OAC Rex HR67 Navigator CDC Whitecap Envoy AC Compass Inoculated experiment OAC Rex HR67 Navigator CDC Whitecap Envoy AC Compass
2004
Brooks
Exeter
Morden
Outlook
Exeter
Morden
Outlook
0.0 0.0 0.0 0.0 0.0 0.0
0.0 0.0 0.0 0.0 0.0 0.0
0.5a 0.0a 0.3a 0.0a 0.3a 0.5a
0.0 0.0 0.0 0.0 0.0 0.0
0.0 0.0 0.0 0.0 0.0 0.0
0.0a 0.0a 0.0a 0.5a 0.5a 0.0a
0.0 0.0 0.0 0.0 0.0 0.0
10.0b 23.8ab 23.8ab 16.2ab 32.5a 21.2ab
40.0c 55.0b 80.0a 80.0a 85.0a 80.0a
10.0d 12.5d 23.8c 47.5b 72.5a 40.0b
25.0c 20.0c 45.0b 60.0b 100.0a 55.0b
0.0d 2.5c 17.5b 17.5b 37.5a 17.5b
7.5d 22.5c 27.5bc 32.5b 47.5a 26.2bc
3.8b 7.5b 20.0a 17.5a 15.0a 7.5b
ac Means within an experiment followed by the same letter are not significantly different, using a protected least significant difference at a 5% level of significance.
OAC Rex, and less clear with HR67. The seed yield for HR67 was very low at the Exeter site in 2004. This cultivar became quite stunted following the inoculum application. This may have been due to an adverse reaction to the surfactant (Sylgard 309), which was applied with the inoculum. However, this reaction was not observed again during this study. It should be noted that the disease symptoms were quite low on HR67 at this site compared with the susceptible cultivars. In order to compare the results of the noninoculated and the inoculated experiments, a yield index was calculated (Table 4). For each cultivar, the yield difference between the noninoculated and inoculated experiments was due to disease pressure, and well as
other environmental factors such as small differences in soil conditions. Assuming each cultivar responded similarly to the other environmental factors in each experiment, then a comparison of their index values can be used to compare their response to disease pressure. The authors suggest that this is a useful method to evaluate the field performance of resistant and susceptible cultivars, until the release of near-isogenic breeding lines that differ only in their resistance/susceptibility to common bacterial blight. Treatment differences for yield index were observed at six sites. The Brooks site in 2003 had no treatment differences for yield index, but it was noted earlier that this site had poor treatment separation for leaf disease scores as well. For the Morden site in
Table 2. Leaf ratings for common blight severityz for two resistant and four susceptible white pea bean cultivars at seven sites in 2003 and 2004 2003 Cultivar
Brooks
2004
Exeter
Morden
Outlook
Exeter
Morden
Outlook
Noninoculated experiment OAC Rex HR67 Navigator CDC Whitecap Envoy AC Compass
0.0 0.0 0.0 0.0 0.0 0.0
0.0a 0.0a 0.0a 0.0a 0.3a 0.3a
0.5a 0.0a 0.5a 0.0a 0.3a 0.3a
0.0a 0.5a 0.0a 0.0a 0.0a 0.0a
0.0 0.0 0.0 0.0 0.0 0.0
0.0a 0.0a 0.0a 0.5a 0.5a 0.0a
0.0 0.0 0.0 0.0 0.0 0.0
Inoculated experiment OAC Rex HR67 Navigator CDC Whitecap Envoy AC Compass
0.5b 0.8ab 0.8ab 0.6ab 1.0a 0.9ab
3.0b 3.0b 4.0a 4.0a 4.0a 4.0a
2.0d 2.0d 3.0c 4.0b 4.8a 4.0b
1.5b 1.5b 3.0a 2.8ab 3.2a 3.1a
0.0d 1.0c 3.0b 3.0b 4.0a 3.0b
2.0c 2.2c 3.0b 3.5ab 4.0a 3.5ab
0.9c 2.1bc 3.0ab 3.7a 2.4ab 2.8ab
z
Severity of leaf disease was measured using a 05 scale, where 0no infection, 1B510%, 31025%, 42550%, 550100% lesion area on the infected leaves. ac Means within an experiment followed by the same letter are not significantly different, using a protected least significant difference at a 5% level of significance.
GILLARD ET AL. * COMMON BACTERIAL BLIGHT RESISTANCE
409
Table 3. Seed yield (kg ha 1) for two resistant and four susceptible white pea bean cultivars at seven sites in 2003 and 2004 2003
2004
Cultivar
Brooks
Exeter
Morden
Outlook
Exeter
Morden
Outlook
Noninoculated experiment OAC Rex HR67 Navigator CDC Whitecap Envoy AC Compass
3794ab 3590ab 3842ab 3509ab 3203b 4254a
2648b 1976d 2101d 2619b 2340c 2840a
4177a 4101a 4530a 4321a 3916a 4206a
2815bc 3157ab 2277c 3300ab 3782a 3121ab
1826c 1776c 1965bc 2186ab 1780c 2375a
1589c 2221ab 2379a 2554a 1895bc 2288ab
806c 1548b 1342b 2192a 1661b 1529b
Inoculated experiment OAC Rex HR67 Navigator CDC Whitecap Envoy AC Compass
4085a 3744a 4366a 3642ab 2637b 3740a
1531a 1102c 1054c 1416ab 1116bc 1275abc
4102a 3800ab 3591ab 3676ab 3098b 3094b
2318a 2330a 736c 1419b 1606b 1713ab
1416a 545c 1240ab 1151b 719c 714c
1627b 2167a 2101a 2103a 1650b 2300a
316b 564a 250b 624a 504a 566a
ac Means within an experiment followed by the same letter are not significantly different, using a protected least significant difference at a 5% level of significance.
2004, cold growing conditions would have placed the two CBB-resistant cultivars, which are later maturing than the better adapted susceptible cultivars, at a disadvantage for optimum yield. For this reason, even though the yield indices for OAC Rex and HR67 were lower than the susceptible cultivars at the Morden site in 2004, the differences were not significant (P B0.05) (Table 4). The resistant cultivars had lower yield indexes at most of the remaining sites. This was particularly evident at the Morden and Outlook sites in 2003 and the Exeter site in 2004. The one exception is HR67 at the Exeter site in 2004. Its high yield index is a direct result of low yield recorded in the inoculated experiment, as previously discussed. Compared with the mean of the susceptible cultivars, the yield index advantage for OAC Rex ranged from 8.5 to 39.6% with a mean of 23.1%. If the Exeter 2004 site was excluded for HR67, its yield index advantage ranged from 6.4 to 33.9%, with a mean of 13.8%. For OAC Rex, this response is similar to the 25% yield response reported by Scott and Michaels (1992), using similar genetic material. Wallen and Jackson (1975) reported a yield reduction of 38% in
an artificially inoculated study of the bean cultivar Saranac in Ontario, while Yoshii et al. (1976) determined that Duva had a yield reduction of 22% in naturally inoculated experiments, and 45% in artificially inoculated experiments. Compared with OAC Rex, HR67 appears to be slightly more susceptible to the common bacterial blight isolates evaluated. This resulted in slightly lower yields for HR67, and a higher yield index. CONCLUSIONS Under disease-free conditions, CBB-resistant cultivars and susceptible cultivars have similar seed yields. However, under moderate to severe disease pressure, the resistant cultivars usually have much less leaf disease. This was particularly evident for OAC Rex. This difference in disease incidence and severity translated into an average mean yield advantage of 23.1% for OAC Rex, which is similar to the yield response reported in the scientific literature. The yield advantage for HR67 was somewhat less at 13.8%.
Table 4. Yield index for two resistant and four susceptible white pea bean cultivars at seven sites in 2003 and 2004 2003
2004
Cultivar
Brooks
Exeter
Morden
Outlook
Exeter
Morden
Outlook
OAC Rex HR67 Navigator CDC Whitecap Envoy AC Compass
7.5a 4.4a 15.2a 5.0a 18.6a 0.2a
42.3b 44.2ab 50.0ab 45.8ab 52.5ab 55.0a
0.8c 7.1bc 20.8ab 15.1ab 20.0ab 25.8a
11.9b 17.6b 58.2a 55.2a 57.2a 35.3ab
21.0d 69.4a 36.2c 47.2bc 57.7ab 69.4a
15.8a 0.9a 11.6a 17.4a 11.7a 1.4a
61.1b 63.5ab 80.6a 70.8ab 69.6ab 58.6b
Means within an experiment followed by the same letter are not significantly different, using a protected least significant difference at a 5% level of significance.
410 CANADIAN JOURNAL OF PLANT SCIENCE
ACKNOWLEDGEMENTS We thank T. Smith, C. Shropshire, D. Depuydt, S. Willis, L.M.Yager and D.B. Stoesz for their technical assistance, and we acknowledge funding from the Alberta Pulse Growers Association, the Manitoba Pulse Growers Association, the Ontario White Bean Producers’, the Ontario Coloured Bean Growers Association and the Saskatchewan Pulse Growers. We also are grateful to Dr. S.J. Park of the Agriculture and AgriFood Canada, Greenhouse and Processing Crops Research Centre at Harrow, ON for providing the X. axonopodis isolates used in this study. Bailey, K. L., Gossen, B. D., Gugel, R. K. and Morrall, R. A. A. 2003. Diseases of field crops in Canada. 3rd ed. University Extension Press, University of Saskatchewan, Saskatoon, SK. 290 pp. Coyne, D. P. and Schuster, M. L. 1973a. Inheritance and linkage relations of reaction to Xanthomonas phaseoli (E.F. Smith) Dowson (common blight) stage of plant development and plant habit in Phaseolus vulgaris L. Euphytica 23: 195204. Coyne, D. P. and Schuster, M. L. 1973b. Phaseolus germplasm tolerant to common blight bacterium (Xanthomonas phaseoli). Plant Dis. Rep. 57: 111114. Coyne, D. P. and Schuster, M. L. 1974. Differential reaction of pods and foliage of beans (Phaseolus vulgaris) to Xanthomonas phaseoli. Plant Dis. Rep. 58: 278282. Michaels, T. E., Smith, T. H., Larsen, J., Beattie, A. D. and Pauls, K. P. 2006. OAC Rex common bean. Can. J. Plant Sci. 86: 733736. Mutlu, N. Miklas, P., Reiser, J. and Coyne, D. 2005. Backcross breeding for resistance to common bacterial blight in pinto bean (Phaseolus vulgaris L.). Plant Breed. 124: 282287. Mutlu, N. Vidaver, A. K., Coyne, D. P., Steadman, J. R., Lambrecht, P. A. and Reiser, J. 2008. Differential pathogenicity of Xanthomonas campestris pv. phaseoli and X. fuscans subsp. fuscans strains on bean genotypes with common blight resistance. Plant Dis. 92: 546554.
Park, S. J. and Dhanvantari, B. N. 1987. Transfer of common blight (Xanthomonas campestris pv. phaseoli) resistance from Phaseolus coccineus Lam. to P. vulgaris L. through interspecific hybridization. Can. J. Plant Sci. 67: 685695. Park, S. J., Michaels, T. E. and Dhanvantari, B. N. 1998. Breeding for resistance to common bacterial blight and its effects on agronomic performance and processing quality in dry bean. Annu. Rep. Bean Improv. Coop 41:2526. Parker, J. P. K. 1985. Interspecific transfer of common bacterial blight resistance from Phaseolus acutifolius A. Gray to P. vulgaris L. M.S. thesis, University of Guelph, Guelph, ON. Schwartz, H. F., Steadman, J. R., Hall, R. and Forster, R. L. 2005. Compendium of bean diseases. 2nd ed. APS Press, St. Paul, MN. 109 pp. Scott, M. E. and Michaels, T. E. 1992. Xanthomonas resistance of Phaseolus interspecific cross selections confirmed by field performance. Hortscience 27: 348350. Singh, S. P. and Munoz, C. G. 1999. Resistance to common bacterial blight among Phaseolus species and common bean improvement. Crop Sci. 39: 8089 Ta’ran, B., Michaels, T. E. and Pauls, K. P. 2001. Mapping genetic factors affecting the reaction to Xanthomonas axonopodis pv. phaseoli in Phaseolus vulgaris L. under field conditions. Genome 44: 10461056. Thomas, C. V. and Waines, J. G. 1984. Fertile backcross and allotetraploid plants from crosses between tepary beans and common beans. J. Hered. 75: 9398. Wallen, V. R. and Jackson, H. R. 1975. Model for yield loss determination of bacterial blight of field beans utilizing aerial infrared photography combined with field plot studies. Phytopathology 65: 942948. Yoshii, K., Galvey, G. E. and Alvarez, A. 1976. Estimation of yield losses in beans caused by common blight. Proc. Am. Phytopathol. Soc. 3: 298299. Yu, K., Park, S. J. and Poysa, V. 2000. Marker-assisted selection of common beans for resistance to common bacterial blight: Efficacy and economics. Plant Breed. 119: 411415.
