Published online August 1, 2005
Identification of Quantitative Trait Loci Conditioning Resistance to Fusarium Root
Rot in Common Bean
Belinda Román-Avilés and James D. Kelly*
ABSTRACT
Fusarium root rot [caused by the soil borne pathogen Fusarium
solani (Mart.) Appel & Wr. f. sp. phaseoli (Burk.) Snyd. & Hans.]
is a major constraint to common bean (Phaseolus vulgaris L.) produc-
Reproduced from Crop Science. Published by Crop Science Society of America. All copyrights reserved.
tion worldwide. The objectives of this study were to transfer Fusarium
root rot resistance from small-seeded Middle American black bean
into highly susceptible large-seeded Andean kidney and cranberry
bean genotypes and identify quantitative trait loci (QTL) associated
with Fusarium root rot resistance in common bean. Two inbred back-
cross line (IBL) populations, developed from crosses between small-
seeded resistant and large-seeded genotypes, were evaluated for reac-
tion to root rot during 2 yr in field and greenhouse experiments.
Significant genetic variation that displayed continuous transgressive
segregation toward root rot susceptibility confirmed the quantitative
nature of resistance. Highly significant treatment-by-environmental
effects were observed. Narrow-sense heritability (h2N) estimates for
resistance ranged from 0.10 to 0.51 for the kidney and from 0.20
to 0.82 for the cranberry IBL populations. Nine QTL significantly
associated with Fusarium root rot resistance in the field and green-
house, explained from 5 to 53% of the total phenotypic variability.
The QTL associated with root rot resistance were located on linkage
groups (LGs) B2 and B5 of the integrated bean map close to previously
identified QTL for resistance on B2. On the basis of a linear regression
model, a combination of five markers associated with QTL on two
different LGs accounted for 73% of the phenotypic variation for root
rot resistance. Data from the current study provides breeders the
opportunity to combine, through marker-assisted backcrossing, large-
effect QTL identified on different LGs to enhance root rot resistance
in Andean germplasm of common bean.
F usarium root rot is a major limiting disease of com-
mon bean (Abawi, 1989). Efforts to control Fu-
sarium root rot in common bean through breeding for
resistance have met with limited success (Boomstra and
Bliss, 1977; Burke and Miller, 1983; Dickson and Boett-
ger, 1977; Tu and Park, 1993; Wallace and Wilkinson,
1965). Complex inheritance combined with genetic in-
compatibility have limited attempts to transfer Fu-
sarium root rot resistance into Andean bean cultivars,
despite extensive information on sources of resistance
in the Middle American gene pool (Beebe et al., 1981;
Wallace and Wilkinson, 1973, 1975). The limited genetic
variability present in Andean germplasm (Beebe et al.,
2001) combined with an emphasis on the selection of
seed and pod quality traits appears to have significantly
reduced the genetic variability in large-seeded beans
(Gepts, 1998) and may have contributed to severe sus-
Dep. of Crop and Soil Sciences, Michigan State Univ., East Lansing,
MI 48824. Received 10 Jan. 2005. *Corresponding author (kellyj@
msu.edu).
Published in Crop Sci. 45:1881–1890 (2005).
Genomics, Molecular Genetics & Biotechnology
doi:10.2135/cropsci2005.0028
© Crop Science Society of America
677 S. Segoe Rd., Madison, WI 53711 USA
1881
ceptibility to F. solani (Schneider et al., 2001). Breeding
systems need to be developed to aid in the transfer of
resistance into temperate adapted large-seeded, deter-
minate Andean cultivars that are based on knowledge of
the genomic location of rot root resistance in tropically
adapted, small-seeded, indeterminate Middle American
bean germplasm.
Since traits such as root rot resistance are genetically
complex and difficult to evaluate, the efficiency of phe-
notypic selection is low resulting in limited progress in
breeding for resistance. Breeders are increasingly using
QTL analysis to quantify and locate quantitative resis-
tance in plant genomes, since the approach can over-
come some of the common limitations encountered by
conventional selection for quantitative traits (Ası́ns,
2002; Beavis, 1998; Kelly and Vallejo, 2005). Indirect
selection for root rot resistance based on markers linked
to the resistance QTL would facilitate improvement of
root rot resistance, as field selection is laborious and
destructive sampling is needed to identify resistance.
Quantitative trait loci analyses of dry bean recombinant
inbred line (RIL) populations have led to the identifica-
tion of QTL contributing to Fusarium root rot resis-
tance. Sixteen QTL for Fusarium root rot resistance
were identified using a F4:5 RIL population derived from
a cross between the susceptible large-seeded red kidney
‘Montcalm’ and the root rot resistant snap bean breed-
ing line FR266 (Schneider et al., 2001). Interval mapping
revealed two QTL for Fusarium root rot resistance using
an F2:6 RIL population derived from a cross between
‘A.C. Compass’, a root rot susceptible navy bean, and
NY2114-12, a highly resistant root rot germplasm (Chowd-
bury et al., 2002). Six QTL for resistance to Fusarium
root rot were identified using a RIL population derived
from a cross between the root rot susceptible snap bean
‘Eagle’ and ‘Puebla 152’, a small black seeded root rot
resistant dry bean (Navarro et al., 2004). Most of these
QTL were located on LGs B2 and B3 of the integrated
bean map (Freyre et al., 1998) close to a region where
defense response genes Pgip, and ChS and pathogenesis
related proteins, PvPR-1 and PvPR-2, have been identi-
fied (Schneider et al., 2001). The co-localization with
genes of known function provides information on the
possible role of QTL, the genetic diversity among resis-
tance sources and emphasizes the need for cyclic breed-
Abbreviations: BJ, BAT93 ⫻ Jalo EEP558 recombinant inbred line
population; CIM, composite interval mapping; cM, centimorgan; DTF,
days to flower; h 2N, narrow-sense heritability; IBL, inbred backcross
line; LG, linkage group; LOD, log of odds; MRF, Montcalm Research
Farm; NSL, Negro San Luı́s; NYSAES, New York State Agriculture
Experimental Station; QTL, quantitative trait loci; RAPD, random
amplified polymorphic DNA; RIL, recombinant inbred line; SMA,
single marker analysis.
 1882 CROP SCIENCE, VOL. 45, SEPTEMBER–OCTOBER 2005
ing systems to combine QTL located in diverse geno-
mic regions.
Balanced populations such as RIL, F2, and doubled
haploid populations in which both parental alleles are
present in high frequencies have been used most often
in QTL studies (Butruille et al., 1999). The estimation
of the number of QTL and the relative position and
contribution of each QTL to the expression of a trait
of interest is determined more efficiently in balanced
Reproduced from Crop Science. Published by Crop Science Society of America. All copyrights reserved.
populations. An alternative to the balanced population
is the advanced backcross population where the alleles
of one parent are present at a much lower frequency
(Tanksley and Nelson, 1996). Unbalanced populations
have been used in QTL mapping to determine the num-
ber of genes controlling a quantitative trait and to intro-
gress desirable QTL from unadapted to better adapted
germplasm, (Chetelat and Meglic, 2000; Doganlar et al.,
2002; Fulton et al., 2000; Tanksley and Nelson, 1996).
When using unbalanced populations for mapping and
identifying QTL, there is a loss of resolution and effi-
ciency due to the unequal allele frequency inherited in
IBL populations (Butruille et al., 1999; Tanksley and
Nelson, 1996). However, IBLs or backcross RILs still
provide linkage information to enhance genetic maps
(Doganlar et al., 2002) and unbalanced populations have
the advantage of being more genetically and phenotypi-
cally similar to the recurrent parent. The advantage of
using such populations is the recovery of genetic materi-
als that resemble the recurrent parent but with the addi-
tion of desirable alleles from the donor parent (Bliss,
1993). In crosses between Middle American and An-
dean gene pools, unbalanced populations are more use-
ful to reduce the frequency of phenotypically inferior
genetic material that results from wide crosses between
bean gene pools.
The objectives of this study were to (i) use IBL popu-
lations to introgress Fusarium root rot resistance into
the large-seeded Andean kidney and cranberry beans
using a small-seeded black bean from the Middle Ameri-
can gene pool as the source of resistance; and (ii) iden-
tify significant QTL-marker associations which could be
used to facilitate indirect selection for Fusarium root
rot resistance in common bean.
MATERIALS AND METHODS
Plant Material and Population Development
Two IBL populations, one with 91 IBL individuals from a
cross of ‘Red Hawk’*2/‘Negro San Luı́s’ (NSL) and the other
with 78 IBL individuals from a cross of C97407*2/NSL were
developed using the inbred backcross procedure similar to the
method described by Bliss (1993) in common bean. For this
study, two backcrosses were made to the recurrent parents
Red Hawk and C97407 of Andean origin (Race Nueva Gra-
nada) using NSL as the source of resistance. Red Hawk is a
full season, large-seeded (60 g 100 seed⫺1), dark red kidney
bean cultivar with excellent processing quality (Kelly et al.,
1998). Red Hawk exhibits the type I upright determinate bush
growth habit, is resistant to Bean Common Mosaic Virus, rust
[Uromyces appendiculatus (Pers.:Pers.) Unger], and anthrac-
nose [Colletotrichum lindemuthianum Sacc. & Magnus) Lams.-
Scrib.], but is highly susceptible to Michigan isolates of root
rot caused by F. solani. C97407 is a large-seeded (50 g 100
seed⫺1) cranberry bean breeding line (‘Taylor Horticultural’*/
‘Cardinal’) that also exhibits the type I growth habit and is
susceptible to Fusarium root rot. The small-seeded (25 g 100
seed⫺1) black bean cultivar NSL, from the Middle American
gene pool (Race Durango), was used as the donor parent for
root rot resistance in the intergene pool crosses. Negro San
Luı́s is a late-maturing photoperiod-sensitive cultivar, widely
grown in the semiarid highlands of Central Mexico, that has
an indeterminate prostrate type III growth habit and exhibits
high levels of root rot resistance and drought tolerance.
Both BC2 generation populations were advanced by single
seed descent to the BC2F4:5 generation. No selection was ap-
plied in any generation other than to maintain diversity based
on pedigree, and BC1 plants were chosen randomly for addi-
tional backcrossing. Nevertheless, some parental lines were
lost in subsequent generations due to lethality and photope-
riod sensitivity problems. Both IBL populations were treated
independently and were considered as two separate experi-
ments to reduce error variance.
Field Trials
Resistance of the IBL populations, parents and additional
checks of known root rot reaction were evaluated for Fusarium
root rot resistance at maturity in 2002 and during flowering in
2003. Four field experiments were conducted at the Montcalm
Research Farm (MRF) located near Entrican, MI (43⬚20⬘ N;
85⬚01⬘ W), in an alfisol soil, series name Montcalm/McBride
loamy sand, which is naturally infected with F. solani. A fifth
experiment was conducted at the New York State Agricultural
Experiment Station (NYSAES) in Ontario County near Ge-
neva, NY, where the soil type was a fairly rocky lime silt loam,
with a history of bean production and root rot diseases. This
field has been in continuous bean production for over 10 yr and
is heavily infested with several root rot pathogens including
Fusarium, Pythium, Rhizoctonia, and Thielaviopsis.
The NYSAES experiment was arranged in a 100 entry ran-
domized block design (91 IBLs from kidney IBL population
plus nine checks) with three replications and was planted on
10 to 16 June 2003. Samples were dug and rated for root rot
on 22 July and 18 Aug. 2003 (G.S. Abawi, personal communi-
cation).
The kidney and cranberry IBL populations were evaluated
separately in two experiments planted at MRF on 20 June
2002. The kidney IBL experiment was arranged in a 10 by 10
square lattice design (91 IBL from the kidney IBL population
plus nine checks) and the cranberry IBL experiment was ar-
ranged in a 9 by 9 square lattice design (78 IBL from the
cranberry IBL population plus three checks) with three repli-
cations. Each experimental unit consisted of 20 plants per row
(row length 5.0 m, row width 50 cm, in-row plant spacing
20 cm). The third and fourth experiments were planted at
MRF on 17 June 2003, similar to the design of the previous
two experiments. The kidney population experiment was ar-
ranged in a 10 by 10 square lattice design similar to the 2002
field experiment, and the cranberry experiment was arranged
in an 8 by 9 rectangular lattice design (64 IBL of the cranberry
IBL population plus eight checks) with three replications. The
number of IBLs for the cranberry experiment was reduced in
the 2003 season due to loss of IBLs caused by a heavy infection
with common bacterial blight (Xanthomonas axonopodis pv.
phaseoli) in 2002. Each experimental unit in the 2003 trials
consisted of 80 plants per row (row length 5.0 m, row width
50 cm, in-row plant spacing 7.6 cm). Standard agronomic prac-
tices for tillage, fertilization, insect, and weed control were
applied to ensure adequate plant growth and development.
 ROMÁN-AVILÉS & KELLY: QTL CONDITIONING RESISTANCE TO FUSARIUM
All plots received supplemental irrigation. Plots were irrigated
twice for a total of 41 mm in 2002 and were irrigated three
times in 2003 for a total of 48 mm of supplemental water.
Three random plants from each row in all three replications
were carefully removed from soil and rated for Fusarium root
rot symptoms at maturity during 2002 and at flowering during
2003. Care was taken that the plants at both ends of the rows
were not sampled to avoid error. The root rot screening in
2002 was conducted at the end of the season, as there was
insufficient seed to plant larger plots suitable for destructive
Reproduced from Crop Science. Published by Crop Science Society of America. All copyrights reserved.
sampling earlier in the season and there existed the need to
save sufficient seed for more extensive testing in 2003. Disease
reaction was scored using the root rating scale of 1 to 7 (Schnei-
der and Kelly, 2000), where 1 ⫽ healthy root system with no
discoloration of root or hypocotyl tissue and no reduction in
root mass, and 7 ⫽ pithy or hollow hypocotyl with much
extended lesions, root mass is severely reduced, and is func-
tionally dead. The MRF data was collected by BRA during
the 2002 and 2003 field and greenhouse trials, and the data
was collected by G. S. Abawi, Cornell University for the NY-
SAES experiment.
Greenhouse Trials
Both IBL populations and additional checks of known dis-
ease reaction were evaluated for root rot reaction in the green-
house using a perlite-based protocol (Schneider and Kelly,
2000). Seventy-two-well greenhouse flats were filled with per-
lite and a single seed was germinated in each well, using no
fewer than three seedlings per line per replication for each
individual IBL population. A randomized complete block de-
sign with three replications was used, and each experiment
was evaluated twice. The perlite was saturated with nutrient
solution at planting and at weekly intervals. When plants were
10 d old, they were inoculated with 10 mL of 2 ⫻ 105 spore
suspension of F. solani. The inoculum was applied over the
base of the hypocotyl using a 4-L polyethylene hand sprayer.
The inoculum was prepared by scraping PDA plates of F.
solani into distilled water; quantification was conducted using
a hemocytometer, and the concentration was adjusted to of 2 ⫻
105 spores mL⫺1. The Hawks 2b isolate of F. solani collected by
Schneider and Kelly (2000) in Presque Isle County, Michigan,
was used for all inoculations. Two weeks after inoculation,
seedlings were removed from the flats, and the roots were
cleaned of excess perlite and rated using the scale described
previously. The fungus was cultured continuously, and the
pathogenicity of the culture was maintained by reisolating the
fungus from infected susceptible Red Hawk plants following
the procedure of Schneider and Kelly (2000).
Statistical Procedures
All experiments conducted in the greenhouse and field were
analyzed as a one-way ANOVA using PROC GLM and PROC
MIXED (SAS Institute, 1995). Root rot ratings collected from
greenhouse and field evaluations were averaged to give a
plot mean that was subsequently used for ANOVAs. Pearson
correlations were conducted among agronomic traits and root
rot scores using SAS PROC CORR. Agronomic data were
collected for days to flower (DTF), days to maturity, growth
habit, root vigor, seed yield, and seed weight. The h 2N estimates
for root rot scores in 2002 and 2003 were based on variance
component estimates calculated on an entry mean basis (Hal-
lauer and Miranda, 1981). Pearson rank correlation coeffi-
cients were calculated by PROC CORR to compare means
of root rot ratings for IBLs between greenhouse and field
evaluations (SAS Institute, 1995).
1883
Selective Mapping
The combined selective mapping strategy used to identify
random amplified polymorphic DNA (RAPD) markers linked
to the genomic regions conditioning resistance to Fusarium
root rot consisted of bulked segregant analysis (Michelmore
et al., 1991) and selective genotyping (Lander and Botstein,
1989). The identification of markers followed a five-step pro-
cess for combined selective mapping described by Miklas et
al. (1996). The homozygosity of the selected BC2F4:5 IBLs, to
be used in the bulks, was determined by inoculating both
populations under greenhouse conditions. On the basis of
these inoculations, a contrasting pair of resistant and suscepti-
ble DNA bulks was developed for each population. Each bulk
represented a pool of DNA from the eight most resistant
or eight most susceptible IBLs. Inoculation conditions and
symptom evaluation was performed as previously described.
Before inoculation with F. solani, tissue from BC2F4:5 IBL
populations and parent genotypes was collected for DNA
extraction from greenhouse grown plants, lyophilized, and
ground. DNA was extracted using the miniprep procedure
described by Afanador et al. (1993), with slight modifications.
The RAPD fragments greater in size than 700 bp were ampli-
fied using Invitrogen brand Taq DNA polymerase (Life Tech-
nologies, Rockville, MD), and those bands smaller in size than
700 bp were amplified by AmpliTaq DNA polymerase, Stoffel
Fragment (PerkinElmer, Norwalk, CT). The extracted DNA
was standardized to uniform concentration (10 ng ␮L⫺1) using
DNA fluorometer (Hoefer Pharmacia Biotech, San Francisco,
CA). DNA was amplified using a PerkinElmer Cetus DNA
Thermal Cycler 480 (PerkinElmer, Cetus, Norwalk, CT). Ap-
proximately 20 ␮L of amplified DNA from each sample was
run on a 1.4% agarose gel containing 0.5 ␮g mL⫺1 of ethidium
bromide, 40 mM Tris-acetate, and 1 mM EDTA. DNA was
viewed under ultraviolet light and photographed for perma-
nent record, and polymorphisms were recorded as either pres-
ence or absence of bands.
The three parents were screened with a total of 2500 RAPD
primers. The DNA bulks were tested with only those primers
shown to generate polymorphisms between the parents.
Among the 2500 RAPD primers, only 14% or 350 were poly-
morphic either between parents of the kidney and cranberry
populations. The RAPD markers that co-segregated with the
disease reaction in at least 90% of the individuals compris-
ing the DNA bulks were subsequently assayed across the en-
tire IBL populations. Additional polymorphic markers, pre-
viously identified as associated to Fusarium root rot resistance
(Schneider et al., 2001), were also included in the analysis to
enhance genome coverage (Shen et al., 2003) and determine
if different resistant sources possessed the same QTL as were
detected in the IBL populations.
Genetic Linkage Map and QTL Analysis
None of the genetic mapping software commonly used in
QTL mapping would perform the multipoint analysis and
mapping of the IBL populations. However, mapping programs
such as MAPMAKER and JoinMap accept two point informa-
tion to build genetic maps and provide an estimate of recombi-
nation frequency and corresponding log of odds (LOD) scores.
The mapping program JoinMap was chosen to construct par-
tial LGs based on a minimum LOD score of 4 (Stam, 1993;
van Ooijen and Voorrips, 2001). The addition of previously
identified markers linked to root rot resistance in F4 derived
RILs served as an anchor point not only for the partial LG
construction but also for co-integration with the integrated
bean linkage map (Freyre et al., 1998). All segregating RAPD
 1884 CROP SCIENCE, VOL. 45, SEPTEMBER–OCTOBER 2005

markers from each resulting partial LG were analyzed in a
multiple regression analysis using SAS PROC GLM (SAS
Institute, 1995), and significance was set at P ⬍ 0.05. WinQTL-
Cartographer v2.0 software package was used to map QTL
using composite interval mapping (CIM; Basten et al., 2003),
and single marker analysis (SMA) was used to confirm the
QTL identified by CIM. Permutation analysis was performed
(1000 permutations) for individual traits to identify a signifi-
cance threshold of the test statistic for individual QTL (Doerge
et al., 1997; Edwards et al., 1987; McMullen et al., 2001).
Reproduced from Crop Science. Published by Crop Science Society of America. All copyrights reserved.
cant for both the kidney (F value ⫽ 4.36; P ⬍ 0.001) and
cranberry (F value ⫽ 4.21; P ⬍ 0.001) IBL populations.
Highly significant treatment-by-environment interac-
tions (F value ⫽ 1.90, P ⬍ 0.001) were observed for
the combined ANOVA across two environments in the
cranberry IBL population. Significant interactions for
combined field trials across three field environments
(2002 and 2003 at MRF and 2003 at NYSAES) were
observed (F value ⫽ 1.59, P ⬍ 0.001) for the kidney

MAPMAKER/EXP 3.0 (Lincoln et al., 1987) was used to
anchor the LGs identified in this study to the integrated bean
map by screening the BAT93 ⫻ Jalo EEP558 RIL population
(hereafter referred to as BJ) with those markers that were
polymorphic between the BAT93 and JaloEEP558 parents.
To detect significant loci and epistatic interactions as de-
scribed by McMullen et al. (2001), RAPD marker data for
each IBL was tested for significant associations between root
rot resistance and marker genotype by QTL-cartographer
SMA and CIM. Marker-QTL associations were determined
by F tests with significance at P ⬍ 0.05. The presence of a QTL
was declared significant whenever its LOD score exceeded
the calculated threshold level determined by the permutation
analysis. The estimated position of the QTL was the point
where the maximum LOD score was found in the region
under consideration.
RESULTS AND DISCUSSION
Field and Greenhouse
Significant genetic variation among IBLs was ob-
served for root rot ratings in the four greenhouse experi-
ments and in all field tests of the kidney and cranberry
IBL populations except in the NYSAES test (Table 1).
The limited variation observed at the NYSAES location
may have resulted from confounding effects of other
root rotting organisms. Genetic variation for combined
field trials during 2 yr (2002 and 2003) was highly signifi-
IBL population. Continuous variation in root rot ratings
was observed for both populations, but there was a
broader range of root rot scores in the cranberry IBL
population (Fig. 1). Transgressive segregation toward
susceptibility was observed in both populations, which
is not unexpected given the population structure and
the use of susceptible genotypes as recurrent parents in
the development of the IBL populations. In general, the
mean root rot scores for the kidney IBL population
were higher than the mean root rot score for the cran-
berry IBL population, suggesting the presence of a mod-
erate level of resistance in C97407 parent (Table 1).
Under severe disease pressure, root rot resistance can
vary as it is evident by the range in root rot ratings
(2.4 to 3.7) for the resistant check, FR266, but a less
significant increase in root rot rating (1.1 to 2.5) was
observed for the resistant parent NSL (Table 1). The
susceptible genotypes (Red Hawk, Montcalm, and
C97407) had significantly higher scores (4.1–6.5), than
the values observed for the resistant parent at all loca-
tions. A similar pattern was observed by Schneider et
al. (2001) when evaluating root rot resistance in Mont-
calm ⫻ FR266 population, where the resistant parent
FR266 ranged from 2.0 to 4.5, and the susceptible parent
Montcalm scored 1 to 2 points more than FR266 in all
experiments. Even though environment can play a ma-

Table 1. Narrow-sense heritability (h 2N), parental mean, mean and range of root rot disease evaluations for 91 BC2F4:5 kidney and 78
BC2F4:5 cranberry inbred backcross lines (IBLs) evaluated for resistance to Fusarium root rot under greenhouse and field environments
in 2002 and 2003.
Mean disease score†
2002 2003
Genotypes GH MRF GH MRF NYSAES
Kidney IBL population
NSL‡ 1.5a§ 1.5a 1.3a 1.1a 1.8a
‘Red Hawk’ 5.8b 5.2b 5.4b 5.6b 4.5b
Lowest IBL 3.6 4.1 3.6 3.0 2.9
Highest IBL 7.0 7.0 7.0 6.9 6.0
Mean (91) 6.7 6.3 5.4 5.3 5.8
h 2N ⫾ SE¶ 0.51 ⫾ 0.20 0.20 ⫾ 0.28 0.44 ⫾ 0.22 0.10 ⫾ 0.31 0.16 ⫾ 0.30
Cranberry IBL population
NSL 1.5a 1.0a 2.5a 1.1a –
C97407 6.5b 4.3b 5.7b 4.1b –
Lowest IBL 2.5 2.6 3.2 2.8 –
Highest IBL 6.8 7.0 7.0 6.8 –
Mean (78) 4.5 5.9 5.1 4.9 –
h 2N ⫾ SE¶ 0.51 ⫾ 0.24 0.82 ⫾ 0.17 0.35 ⫾ 0.28 0.30 ⫾ 0.29 –
FR266 (check) 3.1a 3.7a 3.1a 2.4a 3.5a
‘Montcalm’ (check) 6.2b 6.3b 6.2b 5.8b 6.4b
† Disease score was visually rated on a scale of 1 to 7, with 7 being severely diseased and 1 being no disease (Schneider and Kelly, 2000). Parents, checks,
and IBLs from the kidney and cranberry populations were evaluated in the greenhouse (GH) and in the Montcalm Research Farm (MRF) in 2002 and
2003, and only the kidney IBL population was evaluated at the New York State Agriculture Experimental Station (NYSAES) during 2003.
‡ NSL ⫽ Negro San Luı́s.
§ Parental means in a row followed by the same letters were not significantly different at the 0.05 probability level.
¶ Refers to h 2N ⫾ standard error for the IBL population.
 ROMÁN-AVILÉS & KELLY: QTL CONDITIONING RESISTANCE TO FUSARIUM
jor role in disease development and severity observed
at individual locations, our data support the conclusion
that resistant genotypes exhibited a consistent and sub-
stantial reduction in root rot incidence, which would be
reflected by the genetic differences among individual
IBLs.
Pearson correlations were calculated for root rot rat-
ings among the kidney and cranberry IBL evaluated in
the field and greenhouse trials. Greenhouse evaluations
Reproduced from Crop Science. Published by Crop Science Society of America. All copyrights reserved.
for root rot resistance in the kidney IBL population
were positively and significantly correlated with the field
evaluations in 2002 (r ⫽ 0.40; P ⬍ 0.001) and 2003 (r ⫽
0.36; P ⬍ 0.001). A significant but small correlation
among root rot scores was also observed for the kidney
IBL population evaluated at MRF and NYSAES (r ⫽
0.14; P ⬍ 0.01) in 2003. Greenhouse root rot evaluations
for the cranberry IBL population was also positively
and significantly correlated with field evaluations during
2002 (r ⫽ 0.21; P ⬍ 0.01). Negative but significant corre-
lations were observed between DTF and root rot ratings
for the kidney population at MRF during 2002 (r ⫽
⫺0.19; P ⬍ 0.001) and 2003 (r ⫽ ⫺0.11; P ⬍ 0.05). A
negative correlation between root rot ratings with DTF
is expected in genotypes with a determinate growth
habit. Vegetative and root growth of determinate geno-
types ceases at flowering, and the plant partitions all
resources to seed development, which results in less
resources available for host defense response. Further-
more, root death can antagonize damage caused by the
pathogen through the release of nitrogenous compounds
that can stimulate pathogen growth (Toussoun, 1970).
Similar negative correlations between DTF and green-
house and field root rot evaluations were also observed
by Schneider et al. (2001). Bean plants appear to be
Fig. 1. Distribution frequency for Fusarium root rot ratings for a kidney and cranberry bean (Phaseolus vulgaris L.) inbred backcross line (IBL)
populations evaluated at Montcalm Research Farm in 2002 and 2003. NSL ⫽ Negro San Luı́s resistant parent.
1885
more affected by root rot during flowering and later
stages of development when the plant is undergoing
reproductive growth and is more susceptible to abiotic
and biotic stresses.
The h 2N estimates of root rot rating for the greenhouse
trials were intermediate for the kidney (h 2N ⫽ 0.44–0.51)
and cranberry (h 2N ⫽ 0.35–0.51) IBL populations (Table
1). Heritability estimates for field root rot ratings in the
kidney IBL population were low (0.1–0.2) and ranged
from intermediate to high (0.3–0.82) in the cranberry
IBL population. Similar intermediate to high h 2N esti-
mates (0.48–0.71) for root rot ratings were reported in
RIL populations of Montcalm ⫻ FR266 and ‘Isles’ ⫻
FR266 (Schneider et al., 2001). Estimates obtained in
the current and previous studies suggest that the inheri-
tance pattern for root rot was influenced by the testing
procedures employed, age of plants evaluated, and the
parents involved (Boomstra and Bliss, 1977; Hall and
Phillips, 2004; Hassan et al., 1971). High heritability
estimates (77.9% for ‘Redkote’ ⫻ 2114-12 and 79.7%
for Redkote ⫻ N203) were obtained when evaluating
13-wk-old field-grown bean plants for root rot as com-
pared with lower and dissimilar heritability estimates
(33.6 and 10.0%) calculated for 5-wk-old plants (Hassan
et al., 1971). The difficulty in classifying plants for de-
grees of resistance late in the season may have resulted
in greater root rot ratings for 2002 as compared with
the 2003 trials (Table 1). Rating for root rot at maturity
after disease has invaded the decaying root system is
challenging. Late season evaluations were a necessity
in 2002 due to the need to save sufficient seed for further
testing. Late season evaluations are preferred by breed-
ers needing to advance resistant germplasm selected
from segregating populations. Destructive evaluations
 1886 CROP SCIENCE, VOL. 45, SEPTEMBER–OCTOBER 2005

conducted earlier in the season during anthesis should
result in more effective differentiating of root rot resis-
tance, but can only be used with advanced homozygous
lines. The range in heritability estimates for root rot
resistance obtained in the greenhouse and field studies
indicate the quantitative nature of root rot resistance
in beans. Improvement of resistance to Fusarium root
rot should be possible, provided there is adequate con-
trol of the environmental conditions under which the
Reproduced from Crop Science. Published by Crop Science Society of America. All copyrights reserved.
tance on B5, comes from the detection of QTL in both
populations grown in different environments. Two QTL
identified in the kidney IBL population explained
19.0% (G6.2000–G17.900) in 2003 and 30.0% (G17.900–
AL20.350) of the phenotypic variation for root rot resis-
tance in 2002 trials in MRF. Both of these QTL have
a common flanking marker (G17.900), suggesting that
they may share a common genomic region of LG 7
(B5; Fig. 2). Additional support for QTL for root rot

disease is evaluated. resistance in this region of B5 comes from the kidney

IBL population grown in 2002. The third QTL was de-
QTL Analysis tected in the same general region spanning ≈13.0 cM
A linkage map was constructed using JoinMap (Stam, between G6.2000 and AL20.350 on B5 that explained
1993) by placing 33 out of 350 polymorphic RAPD 29% of the phenotypic variability in MRF02 (Table 2).
markers on 10 partial LGs for a total length of 183 This QTL also shares a common marker (G6.2000) with
centimorgans (cM). The limited coverage represents ap- the QTL (G6.2000–G17.900 interval), described above.
proximately 15% of the estimated total length (1200 In previous work with different resistance sources, a
cM) of the bean genome (Kelly et al., 2003) and is QTL for root rot resistance linked to the common
the direct result of the narrow genetic base of the IBL G17.900 marker was reported, but that QTL was not
populations investigated. The partial LGs were an- mapped (Schneider et al., 2001). The QTL in the current
chored to the integrated bean map by genotyping the study displayed highly significant large effects (R2 ⫽ 29
BJ RIL population with markers identified as linked to and 30%) and were supported by LOD values ⬎ 8.0,
QTL for root rot resistance that were previously mapped significantly above the threshold value (LOD ⫽ 7.57).
to the consensus map (Freyre et al., 1998). Three LGs Additional QTL (AL20.700–G6.2000) that explained
(LG 1, 7, and 9) possessing QTL associated with root 33% of the variation for root rot resistance in MRF03,
rot resistance co-integrated with LGs B2 and B5 of the but explained only 1.2% of the phenotypic variation in
integrated map (Table 2), but LG5 and LG8 remained the MRF02, were anchored to B5 with AL20.700 marker
unassigned. In the current study, QTL analysis was con- in the kidney IBL population (Fig. 2). The QTL with
ducted for each year of the study separately due to the small effect (1.2%) was not significant (P ⬍ 0.0526)
the high genotype-by-environment interaction obtained but was highly significant in 2003 (P ⬍ 0.001; Table 2).
when combining data for the 2002 and 2003 field trials. Quantitative trait loci were also identified in the same
Coefficient of determination (R2) values, which reflect genomic region spanning a distance of ≈25 cM on LG 1
the amount of variation explained by a given QTL, (B5) between AL20.850 and G8.1400 in the cranberry
ranged from 5.0 to 53.3% for root rot resistance detected IBL population (Fig. 2). The large-effect QTL that ex-
in different environments (Table 2). Support for the plained 53.3% of the phenotypic variability for root rot
presence of putative QTL, associated with root rot resis- resistance in MRF02 was supported with a significant
Table 2. Linkage group, marker interval, parent donating the allele, position, and environment where the quantitative trait loci (QTL)
were identified, R2 values, and LOD score for QTL significantly associated with root rot resistance in the Red Hawk*2/NSL and
C97407*2/NSL inbred backcross line (IBL) populations.
Linkage Marker interval Parent Position of
group† (population)‡ donating allele‡ QTL§ Environment¶ R 2# LOD
cM %
7 (B5) G6.2000–G17.900 (K) NSL 9.0 MRF03 19.0*** 4.02
7†† G17.900–AL20.350 (K) NSL 11.0 MRF02 30.0** 8.31
7 G6.2000–AL20.350 (K) NSL 6.0 MRF02 29.0* 8.40
7 AL20.700–G6.2000 (K) NSL 0.1 MRF03 33.0*** 7.81
7 NSL 2.0 MRF02 1.2 (P ⬍ 0.053) 7.57
7 AL20.850–AJ4.3000 (K) NSL 21.0 NYSAES03 27.0** 6.70
7 NSL 21.0 GH2 9.8* 7.89
1 (B5) AL20.850–G8.1400 (C) NSL 28.0 MRF02 53.3‡‡ 15.72
1†† O12.800–AL20.850 (C) NSL 12.0 MRF02 7.3*** 6.98
9 (B2) AJ4.350–X3.3054 (K) RH 20.0 NYSAES03 15.0‡‡ 10.50
5 S19.1000–S19.1100 (C) C97407 10.0 GH1 10.7*** 2.35
C97407 6.0 GH2 33.6*** 4.02
8 AN19.1300–H4.1200 (K) NSL 7.1 GH2 39.0*** 9.95
* Significant at the 0.05 probability level.
** Significant at the 0.01 probability level.
*** Significant at the 0.001 probability level.
† Linkage groups detected in current study. Parentheses corresponds to location of marker on the integrated map (Freyre et al., 1998).
‡ C ⫽ Cranberry IBL population, K ⫽ Kidney IBL, NSL ⫽ Negro San Luı́s, RH ⫽ Red Hawk.
§ Position of the QTL peak to the right of the left side marker based on results of Composite Interval Mapping.
¶ MRF02 and MRF03 refer to Montcalm Research Farm experiments during the summer 2002 and 2003, respectively; GH1 and GH2 refer to greenhouse
evaluations one and two respectively, and NYSAES refers to New York State Agriculture Experimental Station.
# Significance was based on single marker analysis data.
†† Markers, underlined, previously identified by Schneider et al. (2001) as linked to QTL associated with root rot resistance.
‡‡ Significant at the 0.0001 probability level.
 ROMÁN-AVILÉS & KELLY: QTL CONDITIONING RESISTANCE TO FUSARIUM 1887

LOD score ⬎ 15 (LOD threshold value ⫽ 3.58; Table 2).
The QTL in the cranberry IBL population on B5 shared
a common flanking marker (AL20.850) with the QTL de-
tected in the kidney IBL population, and the AL20.850
marker also served as an anchor to the integrated bean
map. Most of the QTL on B5 could be considered major
QTL due to their large effect supported by the high LOD
values, relative to the QTL peak and threshold values
determined by the permutation analyses (Table 2). Large-
Reproduced from Crop Science. Published by Crop Science Society of America. All copyrights reserved.
trials, respectively (Fig. 2). Support for additional QTL
in this region of B5 comes from another QTL (R2 ⫽ 7.3,
P ⬍ 0.001) detected in cranberry population in MRF02
between AL20.850 and O12.800 markers (Table 2).
Marker O12.800 was previously identified by Schneider
et al. (2001) as linked to QTL for resistance to root rot,
but the marker was not assigned to a LG. Although a
QTL was not identified between O12.800 and G8.1400
in the kidney IBL population, the same RAPD markers

effect QTL (those QTL that explained 30% or more of
the phenotypic variability) associated with resistance to
root rot are useful starting points for marker-assisted selec-
tion. A large-effect QTL might also be due to a series of
linked QTL, each of small effect (Flint and Mott, 2001).
The regions where QTL are localized can be quite large
as in the current study, and such regions may contain a
number of minor QTL that can only be confirmed with
additional fine mapping.
Additional QTL were detected on a different region
of B5 based on data from the kidney IBL population
evaluated in trials in NY and in the greenhouse. These
QTL, detected between AL20.850 and AJ4.3000 mark-
ers, explained 27 and 9.8% of the phenotypic variation
for root rot resistance in the NYSAES and greenhouse
displayed the expected size polymorphic fragments be-
tween Red Hawk and NSL and segregated in the IBL
population, but these markers remained unassigned
when creating the partial LGs for the kidney IBL popu-
lation. Despite some inconsistencies between popula-
tions and location effects, the QTL analysis has clearly
identified B5 as an important LG for the root rot resis-
tance in common bean. Previously unassigned markers
linked to resistance QTL for root rot were also mapped
to B5. Other resistance factors previously mapped to
B5 (Kelly et al., 2003) include QTL for resistance to
common bacterial and halo blight (Pseudomonas syrin-
gae pv. phaseolicola) and the lipoxygenase gene, Lox-1,
required during development of bean plants under desic-
cation stress (Porta et al., 1999). Despite the obvious con-

Fig. 2. Locations of random amplified polymorphic DNA markers and selectively mapped quantitative trait loci conditioning resistance to
Fusarium root rot in the C97407*2/Negro San Luı́s (NSL) and Red Hawk*2/NSL inbred backcross line (IBL) populations. The partial linkage
groups LG 1 (cranberry IBL population) and LG 7 (kidney IBL population) (Table 2) were cointegrated with LG B5 of the bean consensus
map (Freyre et al., 1998), and common markers in different linkage groups are joined by dashed lines. The graphical presentation was created
with MapChart v. 2.0 (Voorrips, 2002).
 1888 CROP SCIENCE, VOL. 45, SEPTEMBER–OCTOBER 2005
nection between root health and water stress, the potential
role of lipoxygenases in root rot resistance is speculative
in the absence of direct evidence for co-localization of
the Lox-1 gene and QTL for root rot resistance.
The second LG, where major-effect QTL for root rot
resistance were detected, was B2. A QTL associated
with the AJ4.350–X3.3054 markers explained a signifi-
cant portion (R2 ⫽ 15.0, P ⬍ 0.001) of variation for root
rot resistance in the kidney IBL population in NY-
Reproduced from Crop Science. Published by Crop Science Society of America. All copyrights reserved.
SAES03 (Table 2). The AJ4.350 marker on LG 9 was
anchored to B2 in the vicinity of the chalcone synthase
locus, ChS (Ryder et al., 1987; Mohr et al., 1998), polyga-
lacturonase-inhibiting protein, Pgip (Toubart et al.,
1992; De Lorenzo et al., 2002), and the pathogenesis
related protein, PvPR-2 (Walter et al., 1990). Plant de-
fense response is a complex mechanism that is triggered
by pathogen attack. In beans, several defense response
genes co-localize with resistance QTL suggesting a func-
tional relationship between the QTL and the defense
response genes (Geffroy et al., 2000). Other QTL for
resistance to root rot and white mold have been pre-
viously mapped to regions close to ChS, Pgip, and the
PVPR-2 on B2, suggesting that physiological resistance
to Fusarium root rot and white mold [Sclerotinia scleroti-
orum (Lib.) de Bary] is associated with a generalized
host defense response (Schneider et al., 2001; Kelly and
Vallejo, 2005). A study of the biochemical response of
soybean to F. solani f. sp. glycine infection showed that
soybean roots inoculated in soil induced phenylalanine
ammonia-lysase (Lozovaya et al., 2004). Phenylalanine
ammonia-lysase is the first enzyme in the phenylpropa-
noid biosynthetic pathway that produces the phyto-
alexin glyceollin, and lignin, indicating that these de-
fense response compounds may be involved in the
partial resistance response to Fusarium. In addition, a
QTL (V6.1500–P10.1600) that explained only 1.8% of
the phenotypic variation for root vigor was detected in
the cranberry IBL population. The small effect QTL
was significant as it was supported by a maximum LOD
value of 7.78 (LOD threshold value ⫽ 6.5). Root vigor
was significantly and positively correlated with root rot
scores for the cranberry IBL (r ⫽ 0.24; P ⬍ 0.001)
population in MRF03. The QTL was located in the
vicinity of the locus for the pathogenicity related protein
PvPR-2 protein on B2. All the markers anchored to B2
of the integrated map were located close to marker
(P10.1660) previously identified by Schneider et al.
(2001) as associated with root rot resistance in common
bean. The detection of the same QTL in different root
rot resistance sources would suggest a more common
generalized resistance response than the specific special-
ized response conditioned by major resistance genes.
The remaining QTL identified on LGs 5 and 8 could
not be assigned to specific LGs on the bean consensus
map due to the limited number of polymorphic markers
common to the BJ RIL mapping population and the
IBL populations evaluated in this study. In the cranberry
IBL population, a QTL explaining 10.7% of the pheno-
typic variability for root rot resistance in the first green-
house study and 33.6% of phenotypic variability in a
second greenhouse study was detected in the same re-
gion of LG 5 (Table 2). The QTL spanned a distance
of ≈11 cM between S19.1000 and S19.1100, but interest-
ingly, C97407, not the NSL parent, contributed the fa-
vorable allele for this QTL. Lower root rot scores were
also observed for C97409 parent (4.1–4.3) compared
with Red Hawk parent (5.2–5.6) in the field, suggesting
the presence of moderate levels of resistance in the
cranberry parent (Table 1). Quantitative trait loci de-
tected under greenhouse conditions in the susceptible
parent C97407 must be expressed at an early stage of
bean development as root rot evaluations were delayed
to anthesis in the field environment. In the kidney IBL
population, a QTL was identified between AN19.1300–
H4.1200 markers that explained 39.0% of the pheno-
typic variability for root rot resistance in the second
greenhouse evaluation (Table 2). Despite the lack of
information on the location of these greenhouse associ-
ated resistance QTL, they can still be used in marker-
aided breeding for root rot resistance. The lack of associ-
ation between QTL identified in field or greenhouse
experiments could result from masking of the genetic
variation for physiological resistance present in the field
by environmental factors and/or the interaction with
other known root rot pathogens as in the NYSAES field
environment. The quantification of root rot diseases is
made more difficult by the presence of other soil borne
pathogens and the large environmental variation in tem-
perature and moisture that affect growth of F. solani in
the field. In the current and previous studies of root rot
in common bean, markers significantly associated with
field root rot ratings were not significantly associated
with greenhouse root rot ratings and vice versa, with
the exception of AL20.850 marker on B5, which was
significantly associated with greenhouse and field trials
(Fig. 2). Detecting similar QTL associated with root rot
resistance over years and/or locations is challenging.
Alternatively, breeders can use QTL associated with
root rot resistance on different LGs to select and in-
termate progeny possessing complementary QTL for
resistance. Multiple regression analyses using combina-
tions of significant markers linked to QTL for root rot
resistance and their interactions revealed that epistatic
interactions were not significant. Up to 7.6 and 73.8%
of phenotypic variation for greenhouse and field ratings,
respectively, was explained by a set of QTL flanking
markers that included AL20.850 (B5), G17.900 (B5),
AJ4.350 (B2), O12.800 (B5), and V6.1500 (B2). In previ-
ous studies, 50% of the total phenotypic variation for
root rot resistance was explained by two QTL (Chowd-
bury et al., 2002), whereas a subset of four markers
accounted for only 29% of the phenotypic variation for
root rot resistance (Schneider et al., 2001). In the current
study, five marker-QTL associations were identified
that accounted for up to 73% of the phenotypic variation
for root rot resistance in the field. These markers in-
cluded G17.900, O12.800, AL20.850 on B5, and AJ4.350
and V6.1500 on B2. G17.900 and O12.800 markers were
linked to QTL previously identified by Schneider et al.
(2001), but were unassigned. On the basis of linkage to
other markers mapped to B5 on the bean integrated
map, G17.900 and O12.800 markers must reside on B5
 ROMÁN-AVILÉS & KELLY: QTL CONDITIONING RESISTANCE TO FUSARIUM
but appear to be associated with different QTL on that
LG (Fig. 2). To enhance root rot resistance, the QTL
linked to AL20.850 and AL20.500 on B5 could be com-
bined with other QTL linked to the O12.800 marker on
B5. AL20.850 was linked to the large-effect QTL (R2 ⫽
27 and 53.3%) in both the kidney and cranberry IBL
populations as well as in one greenhouse trial (R2 ⫽
9.8%). The QTL linked to AL20.500 in the cranberry
IBL population was also polymorphic in the kidney IBL
Reproduced from Crop Science. Published by Crop Science Society of America. All copyrights reserved.
population. Although the later QTL were not identified
in both populations, the markers linked to this QTL
associated with resistance can be utilized to enhance
conventional breeding approaches by providing infor-
mation that breeders can use to make educated choices
of which putatively linked resistance loci, with large-
effect QTL to combine in future bean cultivars.
CONCLUSIONS
One objective of the current study was to develop
large-seeded kidney and cranberry genotypes with en-
hanced levels of resistance to Fusarium root rot. Several
IBLs resembling the recurrent parents in seed and agro-
nomic traits were identified with root rot resistance su-
perior to both Andean parents. The development of
IBL populations was an effective breeding method to
generate lines similar to the recurrent parents in critical
seed and agronomic traits while retaining sufficient ge-
netic variability for improvement of root rot resistance
present in the donor parent. Given the quantitative na-
ture of the resistance, none of the IBLs achieved the
high level of resistance present in the NSL parent. How-
ever, QTL that explained up to 53% of the phenotypic
variability for resistance to root rot were identified in
individual IBLs. The limited coverage (15%) of the bean
genome did not prevent the confirmation of QTL for
resistance on B2, nor the identification of new QTL on
B5, but two LGs remain unassigned, and previously
reported QTL on other LGs could not be confirmed.
The opportunity now exists to combine different resis-
tance QTL into a single genotype that would exhibit
higher levels of resistance than individual genotypes
alone. For example, genotypes possessing the G17.900
marker on B2 could be combined with other genotypes
possessing the O12.800, AL20.850, and AL20.500 markers
associated with QTL controlling Fusarium root rot resis-
tance on B5. Interestingly, the QTL between G17.900
and AL20.350 that explained up to 30% of the pheno-
typic variation for Fusarium root rot was linked to the
previously unassigned G17.900 marker associated with
root rot resistance (Schneider et al., 2001). The detection
of QTL in the same genomic regions as previously re-
ported QTL for root rot resistance would suggest that
different resistance sources possess similar defense re-
sponse genes or resistance mechanisms. This is not un-
expected, given that previously utilized resistance sources
were small-seeded Middle American black bean geno-
types from Mexico. Data and germplasm from the cur-
rent study should provide breeders the opportunity to
enhance root rot resistance in common bean by combin-
1889
ing large-effect QTL (R2 ⬎ 30) identified on different
LGs through marker-assisted backcrossing.
ACKNOWLEDGMENTS
The authors wish to recognize the contribution of George
Abawi in evaluating the genetic populations in Geneva, NY
and providing data on root rot reaction.
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