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Published March 28, 2014
RESEARCH
Introgressing White Mold Resistance
from Phaseolus coccineus PI 439534 to
Common Pinto Bean
Shree P. Singh,* Howard F. Schwartz, Diego Viteri, Henry Terán, and Kristen Otto
ABSTRACT
White mold [caused by Sclerotinia sclerotiorum
(Lib.) de Bary] is a devastating disease of common
bean (Phaseolus vulgaris L.) in cool- to moderatetemperature and wet-production regions worldwide. Use of resistant cultivars is crucial for effective and economical white mold control. Partial
resistance exists in cultivated and wild common
bean and Phaseolus species of the secondary
gene pool. The objectives were to (i) develop highly
resistant breeding lines (BL) from a recurrent interspecific backcross of common pinto bean ‘UI 320’
with P. coccineus PI 439534, and (ii) compare their
response with known sources of resistance. Five
pinto BL derived from UI 320 ´ 2/PI 439534 interspecific backcross population, the two parents,
nine known sources of resistance, and susceptible pinto ‘Othello’ were screened in the greenhouse. Sclerotinia sclerotiorum isolates ARS12D
and ND710 were used at the University of Idaho,
Kimberly, in 2012 and isolates CO467 and NY133 at
Colorado State University, Fort Collins, in 2013. All
five interspecific pinto BL (VC13-1, VC13-3, VC13-4,
VC13-5, VC13-6) in Idaho and three (VC13-4, VC135, VC13-6) in Colorado exhibited significantly (P £
0.05) higher levels of resistance than PI 439534.
Their resistance was either similar to (in Colorado)
or higher (in Idaho) than the highest levels available in other interspecific BL (92BG-7, I9365-31,
VCW 54, VRW 32) derived from the secondary gene
pool thus far, as well as medium- (USPT-WM-1) and
small- (‘ICA Bunsi’) seeded Middle American and
large-seeded Andean dry (G 122) and green (NY
6020-4) beans. The effectiveness of the five interspecific pinto BL for controlling white mold with and
without fungicides and other disease management
strategies should be performed. Genetics of resistance and tagging and mapping of new resistance
genes and/or quantitative trait loci should be performed. Also, high levels of resistance from the five
interspecific pinto BL should be pyramided across
Phaseolus species and/or transferred into cultivars.
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S. Singh and D. Viteri, Plant, Soil and Entomological Sciences Dep.,
Univ. of Idaho, Kimberly Research and Extension Center, 3793 North
3600 East, Kimberly, ID 83341–5076; H. Schwartz and K. Otto, Dep.
of Bioagr. Sciences and Pest Management, Colorado State Univ., Fort
Collins, CO 80523–1177; H. Terán, DuPont Pioneer, Carr # 1 Km.
154.9 Salinas, PR 00751. Received 24 July 2013. *Corresponding
author ([email protected]).
Abbreviations: BL, breeding line(s); QTL, quantitative trait loci.
T
he white mold fungus Sclerotinia sclerotiorum (Lib.) de Bary
infects over 400 plant species, mostly dicots (Boland and Hall,
1994; Purdy, 1979; Steadman and Boland, 2005). In common bean
(Phaseolus vulgaris L., both dry and green bean), white mold is one of
the most devastating diseases in the United States, Canada, Argentina, Brazil, and other cool- to moderate-temperature and wetproduction regions of the world (Schwartz and Singh, 2013). White
mold disease may occur on all aerial plant parts. Under cool moist
conditions, infected tissues may become slimy, eventually encompassing the entire organ. Affected tissues dry out and bleach to a
pale brown or white coloration that contrasts with the normal light
tan color of senescent tissue. Colonies of white mycelium (immature sclerotia) develop into hard, black sclerotia in and on infected
tissue. Entire foliage, branches, pods, or plants may be killed (Steadman and Boland, 2005). Under favorable weather conditions, 100%
crop loss may occur on susceptible cultivars (Schwartz and Singh,
2013; Singh and Schwartz, 2010). The fungus is endemic and seedtransmitted (Tu, 1988), and sclerotia survive in soil for five or more
years (Steadman and Boland, 2005).
Under severe weather conditions without resistant cultivars,
integrated management strategies (Schwartz and Singh, 2013)
Published in Crop Sci. 54:1026–1032 (2014).
doi: 10.2135/cropsci2013.07.0489
© Crop Science Society of America | 5585 Guilford Rd., Madison, WI 53711 USA
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has been obtained by the publisher.
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crop science, vol. 54, may– june 2014
often are inadequate to control white mold (Agrios,
2005; del Río et al., 2004; Schwartz and Steadman, 1989;
Steadman and Boland, 2005). Plant architectural traits
that impart a tall, upright growth habit, and porous plant
canopy may help avoid white mold incidence and severity under low to moderate disease pressure in common
bean (Ando et al., 2007; Ender and Kelly, 2005; Miklas
et al., 2013). But use of cultivars with physiological resistance (i.e., ability of the host genotype to stop white mold
pathogen infection and disease in the greenhouse either
before reaching to or at the first post-inoculation node
on the main stem and branches) is crucial for adequate
control of severe white mold outbreaks and to reduce or
eliminate the use of fungicide (Miklas et al., 2013).
Partial white mold resistance is found in small-seeded
(<25 g 100 seeds-1) Middle American (e.g., ‘ICA Bunsi’,
which is synonymous with ‘Ex-Rico 23’) (Ender and Kelly,
2005; Miklas et al., 1999; Mkwaila et al., 2011) and largeseeded (>40 g 100 seeds−1) Andean (e.g., A 195, G 122,
NY6020-4, VA 19) common bean (Maxwell et al., 2007;
McCoy et al., 2012; Miklas et al., 1999, 2001; Mkwaila et
al., 2011; Singh et al., 2007a) and wild bean (e.g., PI 318695)
(Mkwaila et al., 2011; Terpstra and Kelly, 2008). But higher
levels of resistance occur in Phaseolus species of the common
bean secondary gene pool such as P. coccineus L. (e.g., G
35172, PI 255956, PI 439534), P. polyanthus Greenman (synonymous with P. dumosus, e.g., G 35877), and P. costaricensis
Freytag and Debouck (e.g., G 40604) (Gilmore et al., 2002;
Schwartz et al., 2006; Singh et al., 2009a, 2012).
Physiological white mold resistance and plant architectural avoidance traits in common bean are quantitatively
inherited with low to moderate heritability (Miklas et al.,
2004; Park et al., 2001). Chung et al. (2008), Mkwaila et
al. (2011), and Soule et al. (2011) reported higher heritability for physiological resistance on the basis of greenhouse
tests than those based on field evaluations, with low correlations between the two tests. Soule et al. (2011) reported
35 quantitative trait loci (QTL) for physiological resistance
(of which 26 were previously known) that coalesced into 21
distinct regions across nine linkage groups. Furthermore,
Miklas et al. (2013) integrated 27 QTL for physiological
resistance, 36 for disease avoidance traits, and 16 for root
traits using comparative mapping. Thirty-six disease avoidance QTL coalesced into 18 genomic regions, influencing
plant architectural traits such as canopy height, internode
length, canopy porosity, and lodging. Thirteen of these
regions co-located with 13 physiological resistance QTL.
Readers interested in more information on avoidance
and resistance QTL and their map positions should refer
to Miklas et al. (2013), Mkwaila et al. (2011), Pérez-Vega
et al. (2012), and Soule et al. (2011). In addition, Genchev
and Kiryakov (2002) reported that a single recessive allele
controlled resistance to white mold in the greenhouse
straw test in A 195/‘Lime Light’ inter-gene-pool dry bean
crop science, vol. 54, may– june 2014 population. But a dominant allele controlled resistance in
the field test. Abawi et al. (1978) and Schwartz et al. (2006)
also reported a single dominant gene controlling resistance
in P. vulgaris/P. coccineus interspecific populations.
Hunter et al. (1982) reported a group of F5 breeding
lines (BL) and Miklas et al. (1998) reported four interspecific BL, namely I9365-3, I9365-5, I9365-31, and 92BG-7,
derived from P. vulgaris/P. coccineus populations that possessed moderate to high levels of white mold resistance.
Singh et al. (2009a,b) developed BL VCW 54 and VCW 55
by congruity backcrossing between a tropical small-seeded
black dry bean cultivar ICA Pijao and P. coccineus accession
G 35172. VCW 54 has a high level and VCW 55 an intermediate level of resistance. However, introgressing white
mold resistance from P. coccineus G 35171 and PI 433246
and P. polyanthus G 35877 was not successful. Elimination
of whole chromosomes and/or segments carrying resistance or desired genes or QTL and related incompatibility
problems are common in interspecies crosses (Manshardt
and Bassett, 1984; Singh et al., 2009a). Singh et al. (2009a,
2012) developed resistant BL VRW 32 by recurrent backcrossing of ICA Pijao with P. costaricensis G 40604. Miklas
et al. (1998) and Singh et al. (2009a,b, 2012) selected neither the parental genotypes of the secondary gene pool
used in crosses nor the early generation populations and
families for white mold resistance. Only advanced generation BL were screened for white mold response.
Medium-seeded (25 to 40 g 100 seeds−1) pinto bean
is by far the most important market class of dry bean in
North America (Singh et al., 2007b). Pinto bean with low
to moderate levels of resistance such as ‘Chase’ (Coyne
et al., 1994) and USPT-WM-1 (Miklas et al., 2006) had
limited effectiveness against white mold. However, using
USPT-WM-1, Kelly et al. (2012) developed ‘Eldorado’
and Miklas et al. (2012) developed USPT-WM-12 solely
on the basis of field tests under white mold pressure that
exhibited higher levels of resistance than USPT-WM-1 in
the greenhouse straw test (McCoy et al., 2012).
Gilmore et al. (2002) screened the United States P.
coccineus collection for white mold response. Subsequently,
Schwartz et al. (2006) screened their 13 resistant P. coccineus accessions in the greenhouse at Fort Collins, CO. Two
of these accessions, PI 433246 and PI 439534, were used
in an inheritance study. Pinto ‘Othello’ was crossed and
backcrossed with PI 433246 and pinto ‘UI 320’ with PI
439534 to determine inheritance of white mold resistance
(Schwartz et al., 2006). Also, 482 early generation families and BL derived from both groups of crosses and backcrosses were systematically screened in the greenhouse in
Idaho beginning in 2007 to transfer white mold resistance
in pinto bean. But by F5 (Othello/PI 433246) and BC1F4
(Othello ´ 2/PI 433246) none of the PI 433246–derived
families or breeding lines or those from UI 320/PI 439534
with white mold resistance survived, probably because of
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incompatibility problems common in interspecies crosses
(Manshardt and Bassett, 1984; Singh et al., 2009a). The
objectives of this study were to (i) develop highly resistant pinto BL from a recurrent interspecific backcross of
pinto UI 320 with P. coccineus PI 439534, and (ii) compare
their disease response with known sources of resistance to a
range of S. sclerotiorum isolates with varying aggressiveness.
MATERIALS AND METHODS
Development of Five White-Mold-Resistant
Interspecific Pinto Bean Breeding Lines
From the recurrent interspecific backcross population UI 320 ×
2/PI 439534, approximately 110 early generation (BC1F2:4) families were developed. Pinto UI 320 has medium-sized seeds, an
indeterminate prostrate growth habit Type III (Singh, 1982), and
the I gene for Bean common mosaic virus (an aphid-vectored potyvirus) resistance (Myers et al., 2001). PI 439534 has indeterminate
strong climbing growth habit Type IV, extra-large (>60 g 100
seed weight) reddish-brown mottled seeds, and sensitivity to long
photoperiod such that it would not flower during the summer
months in the field in the temperate United States (Schwartz et
al., 2006). Thus, the initial interspecific cross and recurrent backcross were made under short-day (£12 h day length) conditions.
During and after completing the inheritance study (Schwartz
et al., 2006), all early generation families were screened in the
greenhouse in Idaho from 2007 to 2011. A completely random
design without replications and the moderately aggressive S.
sclerotiorum isolate CO-S20 (Schwartz et al., 2006; Singh et al.,
2009a,b; Terán and Singh, 2009) were used in 2007 and 2008.
White mold resistant Andean A 195 (Singh et al., 2007a) and G
122 (Maxwell et al., 2007; Miklas et al., 2001) and susceptible
pinto ‘Bill Z’, Othello, and/or UI 320 were used as checks in all
screenings. Three plants were grown in a 15-cm diameter pot,
and three pots genotype-1. For plant inoculation, mycelium was
produced from a single conditioned sclerotium as described by
Schwartz et al. (2006) and Singh et al. (2009a). The main stem
for the first inoculation was cut at the fifth node with a 2.5- to
3.0-cm long inter-node left intact. Two mycelial plugs stacked
together from a 48-h-old S. sclerotiorum culture were punched
into an eppendorf tip and capped over the cut-stem internode
(Terán et al., 2006). The eppendorf tip was allowed to stay on the
inoculated cut-stem internode until the plant died or matured,
or eppendorf tip dropped off naturally. A second inoculation was
made a week later on a branch of those plants with a resistant
disease score of £4 (see below). Two or three portable humidifiers and wetting of the greenhouse floor two to three times per
day maintained high humidity in the greenhouse. Thus, relative humidity in the greenhouse was kept above 80%, and mean
temperature fluctuated between 16 and 22°C. The white mold
reaction was scored at a weekly interval using the modified 1 to
9 scale (Terán et al., 2006). Selection for white mold resistance
was made between and within families and BL, and only highly
resistant plants (score of £4) were harvested individually for the
subsequent screenings.
For the greenhouse screenings in 2009 and 2010, the pathogen
isolate and screening methods were the same as in 2007 and 2008.
But an average of 18 plants were used for each genotype. Furthermore, no selection for seed type or any other trait was practiced
1028
from 2007 to 2010. For the greenhouse screenings between October 2011 and May 2012, pathogen isolates CO-S20 and ND710
(McCoy et al., 2012; Otto-Hanson et al., 2011; Schwartz et al.,
2006) in that order on the same plant, and one to three inoculations per plant at a weekly interval were used as needed to identify
resistant plants. The isolate CO-S20 was replaced with the more
aggressive isolate ARS12D in the summer planting (June to September) in 2012. Response to white mold was scored on a single
plant basis at a weekly interval beginning 7 d post the first inoculation until 35 d, followed by verification of resistance response
at maturity. All intermediate (white mold scores > 4 to < 7) and
susceptible (white mold scores ³ 7 to 9) plants were discarded.
Thus, five resistant pinto BL, namely VC13-1, VC13-3, VC13-4,
VC13-5, and VC13-6, were developed.
Comparative Trial of Five White Mold
Resistant Interspecific Common Pinto
Bean Breeding Lines
The five interspecific common pinto bean BL (VC13-1, VC133, VC13-4, VC13-5, and VC13-6), their two parents (UI 320
and PI 439534), and nine reported resistant checks (A 195,
Chase, G 122, ICA Bunsi, USPT-WM-1, 92BG-7, I9365-31,
VCW 54, and VRW 32), and susceptible Othello were evaluated in the greenhouse at the University of Idaho, Kimberly,
Research and Extension Center in 2012 (October to December) and at Colorado State University, Fort Collins, in 2013
( January to March). A randomized complete block design with
six replications was used. Each plot consisted of three plants per
replicate for each genotype, planted in a 15-cm diameter pot.
Pathogen isolates (McCoy et al., 2012; Otto-Hanson et al.,
2011; Steadman et al., 2006) ARS12D and ND710 were used in
Idaho and CO467 and NY133 were used in Colorado. The purpose was to challenge the five interspecific pinto BL, their parents,
and resistant and susceptible checks to assess the breadth and level of
resistance response to a range of pathogen isolates varying in their
aggressiveness. Inoculum multiplication, inoculation method, and
disease ratings were as described above. However, 1 wk after the
first inoculation, plants with a resistant white mold score £4 were
again inoculated. Similarly, 2 wk after the first inoculation (and 1
wk after the second inoculation) plants with score £4 were inoculated the third time. Disease evaluations were made at 7, 14, 21,
28, and 35 d post-inoculation in Idaho and at 7, 14, and 21 d in
Colorado, using the 1 to 9 scale described by Terán et al. (2006).
Although mean white mold scores significantly increased from 7
to 28 d post-inoculation in Idaho, only differences in mean scores
between 7 and 21 d were significant (P < 0.05) in Colorado. Also,
the latter values were higher; therefore, only scores at 21 d postinoculation in both greenhouses were considered for this study.
Data for each pathogen isolate and greenhouse separately and combined were analyzed using PROC-GLM statistical package (SAS
Institute, 2004). The range, frequency of resistant plants, mean
score for each genotype, and Fisher’s least significant difference
were calculated.
RESULTS
The range, percentage of resistant plants, and mean scores
are good measures of the response of common bean genotypes to pathogens, especially for quantitatively inherited
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crop science, vol. 54, may– june 2014
Table 1. Seed type and the range, mean score, and percentage of white-mold-resistant plants for the parents, interspecific breeding lines derived from UI 320 × 2/PI 439534, and resistant and susceptible checks, evaluated at 21 d post-inoculation in the greenhouse against Sclerotinia sclerotiorum isolates ARS12D and ND710 in Idaho in 2012 and CO467 and NY133 in Colorado in 2013.
Genotype
Seed
type
ARS12D
ND710
CO467
NY133
Overall
Range Mean
RP†
Range Mean
RP
Range Mean
RP
Range Mean
RP
Mean
RP
—— score ——
%
—— score ——
%
—— score ——
%
—— score ——
%
score
%
Pinto
4–9
7.2
5.9
6–9
7.6
0.0
1–9
6.6
33.3
3–9
6.8
11.1
7.0
13.0
Reddishbrown
mottled
3–7
5.6
25.0
4–9
6.2
7.1
3–8
5.7
17.6
3–8
4.4
42.9
5.5
23.0
4.2
66.7
4–9
5.9
16.7
4.8
56.9
Parents
UI 320
PI 439534
White-mold-resistant interspecific breeding lines derived from UI 320 × 2/PI 439534
VC13-1
Pinto
2–4
3.8
100.0
4–7
5.3
44.4
VC13-3
Pinto
3–6
3.8
88.9
VC13-4
Pinto
2–9
4.1
88.9
VC13-5
Pinto
3–4
3.7
VC13-6
Pinto
3–7
4.3
2–7
4–7
4.9
55.6
2–9
4.0
88.9
2–8
4.9
55.6
4.4
72.2
4–7
5.2
44.4
3–6
4.5
55.6
3–7
3.8
83.3
4.4
68.1
100.0
4–7
4.7
66.7
2–9
4.0
77.8
2–6
4.0
66.7
4.1
77.8
83.3
4–6
4.7
66.7
3–5
4.0
83.3
3–7
4.1
83.3
4.3
79.2
White-mold-resistant interspecific breeding line controls
92BG-7
Black
4–7
5.7
27.8
6–9
7.2
0.0
4–9
7.2
5.9
5–9
6.9
0.0
6.8
8.5
I9365-31
Black
4–7
5.8
31.3
4–8
6.7
5.9
3–9
7.3
11.8
3–9
6.0
35.3
6.5
20.9
VCW 54
Black
4–6
4.4
76.5
4–8
5.6
22.2
3–8
5.8
23.5
3–7
4.1
77.8
5.0
50.0
VRW 32
Grayish
brown
4–8
6.0
27.8
4–8
6.6
5.6
4–9
6.3
27.8
3–8
5.2
33.3
6.0
23.6
White-mold-resistant Middle American common bean controls
Chase
Pinto
6–9
7.8
0.0
8–9
8.9
0.0
4–9
7.2
18.8
4–9
7.7
5.9
7.9
6.2
USPT-WM-1
Pinto
7–9
8.3
0.0
4–9
8.5
5.9
4–9
6.5
22.2
3–9
5.3
38.9
7.1
17.6
ICA Bunsi
Navy
6–9
7.1
0.0
7–9
7.8
0.0
4–9
7.3
6.3
4–9
7.7
6.3
7.5
3.0
White mold resistant Andean common bean controls
A195
Beige
4–6
4.1
94.1
4–8
4.4
83.3
3–6
4.8
33.3
4–8
5.9
16.7
4.8
56.3
G122
Cranberry
4–7
4.5
72.2
4–9
5.5
44.4
3–9
6.6
22.2
4–9
6.4
16.7
5.8
38.9
White-mold-susceptible common bean control
7–9
8.6
0.0
8–9
8.8
0.0
8–9
8.9
0.0
3–9
8.2
5.6
8.6
1.4
Mean
Othello
–
5.6
48.3
–
6.4
26.6
–
5.9
35.0
–
5.7
35.0
5.9
36.3
LSD (P £ 0.05)
–
0.9
–
–
0.6
–
–
1.5
–
–
1.3
–
0.6
–
†
Pinto
RP, resistant (white mold score £4.0, which is white mold pathogen infection and disease in the greenhouse stopping either before reaching or at the first post-inoculation
node on the main stem and branches) plants.
disease resistances such as white mold. White mold scores
at 21 d post-inoculation ranged from 1 to 9 for pinto
UI 320 for isolate CO467 to 8 to 9 for susceptible check
pinto Othello for isolates CO467 and ND710 (Table 1).
Thus, the percentage of resistant plants (scores £4) was
0.0 for Othello for isolates ARS12D, ND710, and CO467;
Chase and ICA Bunsi for ARS12D and ND710; and
USPT-WM-1 for ARS12D. In contrast, all genotypes had
one or more resistant plants against the isolate NY133. For
example, Othello had 5.6% resistant plants even at 21 d
post-inoculation to isolate NY133 (Table 1). Interspecific
pinto BL VC13-1 had a range of 2 to 4 and VC13-5 a
range of 3 to 4 for isolate ARS12D. Thus, these two pinto
BL had 100% resistant plants to ARS12D. But these two
BL had some plants with an intermediate and/or susceptible response to the other three isolates. Nonetheless,
crop science, vol. 54, may– june 2014 the five interspecific pinto BL, in general, had the highest percentages of resistant plants to all four isolates. Dry
bean breeding line A 195 (Singh et al., 2007a) and previously developed interspecific BL VCW 54 (Singh et al.,
2009a,b) followed by G 122 (Maxwell et al., 2007; Miklas
et al., 2001) also had considerably higher percentages of
resistant plants for the four isolates.
The mean white mold score for the susceptible check
pinto Othello ranged from 8.2 against isolate NY133 to
8.9 for isolate CO467, with an overall mean of 8.6 for
the four isolates (Table 1). Mean scores were also susceptible for Chase and ICA Bunsi to all four isolates, and
USPT-WM-1 to all except NY133. The mean score of
USPT-WM-1 for NY133 isolate was 5.3 (Table 1). Largeseeded Andean breeding line A 195 had resistant or nearresistant mean scores against isolates ARS12D and ND710
www.crops.org1029
in Idaho, and intermediate scores against isolates CO467
and NY133 in Colorado.
Pinto bean cultivar UI 320 used to develop the five
interspecific pinto bean BL had susceptible mean scores
(6.6–7.6) in both greenhouse tests (Table 1). The mean
score for the second parent of the five pinto BL, P. coccineus
PI 439534, varied from 4.4 for NY133 to 6.2 for ND710.
Of the previously developed interspecific BL, 92BG-7 and
I9365-31 derived from P. coccineus (Miklas et al., 1998) and
VRW 32 derived from P. costaricensis (Singh et al., 2012)
had intermediate to susceptible mean scores to the four
isolates (Table 1). VCW 54 had resistant or near-resistant
scores against isolates NY133 and ARS12D and intermediate scores against isolates ND710 and CO467. All five
interspecific pinto BL had resistant or near-resistant mean
scores against isolates ARS12D and CO467, and three
(i.e., VC13-4, VC13-5, VC13-6) also against NY133
(Table 1). All other mean scores of these five BL were
intermediate. Thus, these five interspecific pinto bean BL
in general, and VC13-5 and VC13-6 in particular, were
the most resistant among all genotypes tested against the
four isolates across both greenhouse environments.
DISCUSSION
The Colombian small white bean cultivar ICA Bunsi was
among the first Middle American sources of white-moldresistant common beans identified in North America (Tu
and Beversdorf, 1982). Since then, directly or indirectly,
ICA Bunsi has been extensively used in genetic and breeding studies (Ender and Kelly, 2005; Kolkman and Kelly,
2003; Miklas et al., 2004, 2007), germplasm enhancement
(Miklas et al., 2006, 2012), and cultivar development (Kelly
et al., 2012; Michaels et al., 2006). Although ICA Bunsi
was well accepted in Ontario, Canada, its widespread adoption in North America was limited, probably because of
its indeterminate prostrate growth habit Type III, which is
unsuitable for direct harvest, and low to moderate levels of
white mold resistance. In our study, ICA Bunsi had susceptible mean scores (7.1–7.8) against all four isolates. From this
and other studies (McCoy et al., 2012; Otto-Hanson et al.,
2011; Singh et al., 2009a,b; Steadman et al., 2001, 2006) it
was obvious that ICA Bunsi exhibited only zero to moderate levels of physiological resistance in the greenhouse.
Of the previously known white-mold-resistant interspecific BL derived from the Phaseolus species of the secondary gene pool, 92BG-7 and I9365-31 (Miklas et al.,
1998) and VRW 32 (Singh et al., 2009a,b, 2012) had intermediate to susceptible mean scores in this study. Only the
BL VCW 54 had resistant or near-resistant mean scores
against isolates NY133 and ARS12D and intermediate
scores against ND710 and CO467. Furthermore, all previously developed resistant BL derived from the secondary gene pool Phaseolus species thus far have small black
and other colored seeds resembling the common bean race
1030
Mesoamerica (Singh et al., 1991). Thus, given the importance of medium-seeded pinto bean (Singh et al., 2007b)
and white mold (Schwartz and Singh, 2013; Singh and
Schwartz, 2010) in North America there was a strong justification to introgress yet higher levels of broad spectrum
resistance into pinto (and other) market class, which generally have lower levels of physiological resistance than some
of their Andean counterparts such as A 195 and G 122.
In this study, high levels of white mold resistance were
introgressed from P. coccineus PI 439534 into five pinto
bean BL. In comparison with the interspecific BL previously derived from the secondary gene pool (e.g., 92BG-7,
I9365-31, VCW 54, VRW 32), these new BL possess significantly higher levels of resistance. As noted above, neither the secondary gene pool parents nor the early generation populations and families were screened for white mold
response by Miklas et al. (1998) and Singh et al. (2009a,b,
2012). Only the advanced generation BL were screened
in the greenhouse and/or field environments. Also, accessions of the secondary gene pool used by these researchers
might have been variable for white mold response, and
the population size and breeding methods used could have
been inadequate. The greenhouse screening of PI 439534
followed by that of its derived F1, F2, and recurrent backcrosses was performed in Colorado and Idaho (Schwartz
et al., 2006). Subsequent sequential greenhouse screenings between 2007 and 2011 in Idaho using moderately
less aggressive S. sclerotiorum isolates such as CO-S20 and
one inoculation initially would have helped eliminate all
susceptible plants and recombinant genotypes with low
to moderate levels of resistance. Furthermore, a more
severe screening using less aggressive (CO-S20) and more
aggressive (ND710) isolates (McCoy et al., 2012; OttoHanson et al., 2011; Steadman et al., 2006) on the same
plant, multiple inoculations per plant, periodic evaluations
until 35 d post-inoculation, and verification of resistance
at maturity would have allowed survival only of genotypes
with higher levels of resistance. Thus, from approximately
110 BC1F2:3 families and BL only 5 had survived at the end
of the sequential screening process in the spring of 2012.
The screening and selection methods used in this
study are not currently popular in common bean genetics
and breeding studies. White mold resistance is a quantitatively inherited trait controlled by >20 QTL (Chung et
al., 2008; Miklas et al., 2013; Mkwaila et al., 2011; PérezVega et al., 2012; Soule et al., 2011). Despite that, it is
not customary to use the range and frequency of resistant plants within each genotype in the selection process.
Often the mean scores are used to separate resistant, intermediate, and susceptible genotypes. But the range and
percentage of resistant plants could also be useful indicators of the promising genotypes. For example, using these
criteria we were able to identify some resistant plants in
pinto Othello against the isolate NY133. Similarly, we
www.crops.org
crop science, vol. 54, may– june 2014
identified resistant plants in Chase and ICA Bunsi against
isolates CO467 and NY133; and in USPT-WM-1, against
all isolates except ARS12D. The mean responses of the
four genotypes were either intermediate or susceptible to
these isolates. Thus, through a judicious process of pedigree selection, the percentages of resistant plants within
each of these genotypes against these isolates could be
enhanced over time. Breeders interested in higher levels
of resistance and enhanced control of the white mold disease, therefore, may consider the range and frequency of
plants of each score class within each breeding line during
the selection process.
We did not consider plants with intermediate response
to white mold in this study because of our emphasis on
breeding for higher levels of resistance. But in a practical
cultivar development program these could also be of significant value for slowing disease development and reducing fungicide usage. In the midwestern United States,
white mold is a severe production problem in common
bean, and multiple pathogen isolates of different aggressiveness occur (McCoy et al., 2012; Otto-Hanson et al.,
2011). For that region, it may be prudent to use intensive
greenhouse screenings and selection similar to this study for
development of cultivars with high levels of physiological
resistance. Furthermore, for superior high-yielding cultivars, both high levels of physiological resistance and plant
architectural avoidance traits may need to be combined.
Genotypic selection for the latter is currently discouraged,
and 13 physiological resistance QTL were co-located with
13 avoidance trait QTL (Miklas et al., 2013). Thus, it is necessary to combine the above method of greenhouse screening with simultaneous selection for seed yield and avoidance traits under white mold pressure in the field (Ender
et al., 2008; Kelly et al., 2012; Kolkman and Kelly, 2003;
Miklas et al., 2012, 2013; Mkwaila et al., 2011).
It would be unexpected to observe white-mold-susceptible plants for one or more pathogen isolates in each
of the five interspecific pinto bean BL developed in this
study because single-plant selections were made in the
greenhouse under severe disease pressure from the beginning until development of these BL. Singh et al. (2009a)
also reported similar results for white-mold-resistant BL
derived from the secondary gene pool. In our greenhouse
screening for the past 10 yr, we have not found any resistant
Phaseolus species of the secondary gene pool, dry and green
common bean germplasm accession, cultivar, and BL truebreeding or uniform for white mold resistance response to
any isolate(s). Therefore, the resistance response of 100% of
plants of interspecific pinto BL VC13-1 (scores 2 to 4) and
VC13-5 (scores 3 to 4) to isolate ARS12D was very encouraging and the first of its kind. Thus, through a judicious process of prolonged intensive pedigree selection in the greenhouse as practiced in this study, physiological resistance to
other isolates could be enhanced. Also, a comparative study
crop science, vol. 54, may– june 2014 may be worthwhile to determine the usefulness of the five
interspecific pinto bean BL developed in this study over the
existing resistant dry and green bean germplasm accessions,
BL, and cultivars for combating white mold disease in the
United States and elsewhere.
Acknowledgments
This research was supported by the USDA-ARS National
Sclerotinia Initiative Grant No. 58-5442-2-256 “Introgressing
White Mold Resistance from the Secondary Gene Pool of
Common Bean” from 2003 to 2008. The authors also acknowledge complementary support from the Idaho and Colorado
Agricultural Experiment Stations.
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