Photosynthate remobilization capacity from drought-adapted common bean (Phaseolus vulgaris L.) lines can improve yield potential of interspecific populations within the secondary gene pool

Abstract

Interspecific lines obtained from crosses between common bean (Phaseolus vulgaris L.) and other species from its secondary gene pool have a tendency for excessive vegetative growth and low grain yield. Contrariwise, drought-adapted common bean lines have been observed to produce high yields despite low shoot biomass production. This was attributed to greater remobilization of photosynthates to grain development. The objective of the present study was to investigate whether F2-families derived from crosses between an interspecific line and drought-adapted P. vulgaris lines have improved ability to remobilize greater proportion of photosynthate from shoot biomass to grain yield and subsequently obtain higher yield potential. Seven F2-progenies derived from crosses of an interspecific hybrid line of P. vulgaris × Phaseolus dumosus with seven drought-adapted lines reflecting a range of photosynthate remobilization and partitioning were evaluated under irrigated and rainfed field conditions along with their eight parent lines and one drought-tolerant check at the International Center of Tropical Agriculture (CIAT) at Palmira, Colombia. Although no single parent trait led to higher yield potential in progenies, the mean yield potential of the progenies, as well as mean yield under drought was significantly higher than yields of the interspecific parent, indicating that crosses with drought-adapted bean lines with greater plant efficiency constitute a promising breeding approach for yield improvement of interspecific crosses in both drought stressed and favorable environments

Full text

Journal of Plant Breeding and Crop Science Vol. 4(4), pp. 49-61, 29 February, 2012
Available online at http://www.academicjournals.org/JPBCS
DOI: 10.5897/JPBCS11.087
ISSN 2006-9758 ©2012 Academic Journals
Full Length Research Paper
Photosynthate remobilization capacity from drought-
adapted common bean (Phaseolus vulgaris L.) lines
can improve yield potential of interspecific populations
within the secondary gene pool
Stephanie M. Klaedtke1,2, Cesar Cajiao1, Miguel Grajales1, José Polanía1, Gonzalo Borrero1,
Alberto Guerrero1, Mariela Rivera1, Idupulapati Rao1, Stephen E. Beebe1* and Jens Léon2
1Centro Internacional de Agricultura Tropical (CIAT), A. A. 6713, Cali, Colombia.
2Institute of Crop Science and Resource Conservation, Crop Genetics and Biotechnology Unit, University of Bonn,
Katzenburgweg 5, 53115 Bonn, Germany.
Accepted 27 February, 2012
Interspecific lines obtained from crosses between common bean (Phaseolus vulgaris L.) and other
species from its secondary gene pool have a tendency for excessive vegetative growth and low grain
yield. Contrariwise, drought-adapted common bean lines have been observed to produce high yields
despite low shoot biomass production. This was attributed to greater remobilization of photosynthates
to grain development. The objective of the present study was to investigate whether F2-families derived
from crosses between an interspecific line and drought-adapted P. vulgaris lines have improved ability
to remobilize greater proportion of photosynthate from shoot biomass to grain yield and subsequently
obtain higher yield potential. Seven F2-progenies derived from crosses of an interspecific hybrid line of
P. vulgaris × Phaseolus dumosus with seven drought-adapted lines reflecting a range of
photosynthate remobilization and partitioning were evaluated under irrigated and rainfed field
conditions along with their eight parent lines and one drought-tolerant check at the International
Center of Tropical Agriculture (CIAT) at Palmira, Colombia. Although no single parent trait led to higher
yield potential in progenies, the mean yield potential of the progenies, as well as mean yield under
drought was significantly higher than yields of the interspecific parent, indicating that crosses with
drought-adapted bean lines with greater plant efficiency constitute a promising breeding approach for
yield improvement of interspecific crosses in both drought stressed and favorable environments.
Key words: Drought adaptation, interspecific crosses, dry matter partitioning, Phaseolus, remobilization, yield.
INTRODUCTION
“It is not always easy to distinguish between wild and
cultivated plants in South America, for there are many
intermediate stages between the utilization of plants in
their wild state and their true cultivation”, noted the
ethnologist and anthropologist Claude Lévi-Strauss in
1950 (Smithsonian Institution Bureau of American
Ethnology, 1950). Even today this is true for common
*Corresponding author. E-mail: s.beebe@cgiar.org.
bean (Phaseolus vulgaris L.) and the species from its
secondary gene pool (Harlan and de Wet, 1971).
Cultivated P. vulgaris seems to have inherited survival
mechanisms from its wild ancestor expressed as
excessive viney growth and a lack of clear transition
between the vegetative and reproductive growth stages,
leading to a suppression of reproductive growth under a
range of environments and a poor response to favorable
conditions (Kelly et al., 1999; Beebe et al., 2008, 2009;
Butare et al., 2011). Analogous growth habits, with low
harvest indices (HI) and suboptimal yields are also

50 J. Plant Breed. Crop Sci.
adopted by species within common bean‟s secondary
gene pool such as wild and cultivated forms of Phaseolus
coccineus L. and Phaseolus dumosus Macfady and wild
Phaseolus costaricensis Freytag and Debouck (Debouck,
1999; Singh, 2001). Nevertheless, common bean is the
world‟s most important grain legume for direct human
consumption (Broughton et al., 2003), with 20.3 million
tons of dry bean harvested from 27.9 million ha
worldwide in 2008 (FAOSTAT, 2010). Almost 80% of dry
bean (P. vulgaris) is produced by small landholders in the
developing countries of tropical Latin America and Africa
(Rao, 2001), particularly in eastern and southern Africa
and Central America. In these regions, beans constitute
an important source of plant protein and micronutrients in
human diets (Broughton et al., 2003).
Common bean is often grown on marginal lands under
unfavorable environmental conditions (Rao, 2001;
Broughton et al., 2003) with minimal soil and crop
management inputs (Rao, 2001; Beebe et al., 2008, 2009).
Low soil fertility due to phosphorus (P) deficiency or
aluminum (Al) toxicity (Beebe et al., 2009) and high risk
of intermittent or terminal drought (White and Izquierdo,
1991; Muñoz-Perea et al., 2006) are among the most
common abiotic stresses. These production constraints
explain why average yields in many countries of Africa
and Latin America did not exceed 700 kg/ha in 2008
(FAOSTAT, 2010), although experimental dry bean yield
potential exceeds 3000 kg/ha (Beebe et al., 2006).
Regarding breeding efforts to improve grain yields, it has
been estimated that up to 90% of genetic variability in
common bean and its sister species remains un- or
underutilized (Singh, 2001). Therefore, species in the
secondary gene pool are considered easily accessible
potential sources not only for tolerance to abiotic
stresses, but also for agronomic and nutritional traits:
Year-long bean (P. dumosus) and scarlet runner bean (P.
coccineus) have been identified as sources of resistance
to important fungal pathogens (Singh, 2001) and high
iron (Fe) and zinc (Zn) content in grain in common bean
(Beebe et al., 2006; CIAT, 2008). Scarlet runner bean
also features resistances to viral and bacterial pathogens
(Singh, 2001) and to damage caused by the bean fly
(Ophiomyia phaseoli Tryon) (Kornegay and Cardona,
1991), as well as tolerance to low temperatures (Singh,
2001) and Al toxicity in soils (Beebe et al., 2009). P.
costaricensis holds yet unutilized potential for common
bean breeding (Singh et al., 1997). In fact, breeding
programs have mainly concentrated on P. coccineus
cultigens for gene introgression and the development of
advanced lines with acceptable yield from interspecific
hybrids with the secondary gene pool, particularly with
wild forms has been limited (Debouck, 1999; Singh, 2001).
Difficulties to capitalize on variability in these sister
species are attributable to excessive vegetative growth
and poor partitioning of dry matter to grain which are
inherent to all of them. However, efficient development
patterns with a clear transition to reproductive growth
allowing for higher grain yields under both drought and
favorable environments have been observed in drought-
adapted bean lines (Beebe et al., 2008). This was
associated with greater plant efficiency and remobili-
zation of photosynthates to grain (Rao, 2001; Beebe et
al., 2006, 2008; Rao et al., 2007, 2009). However, such
remobilization capacity is needed in interspecific lines
within the secondary gene pool to capitalize on their
excessive vegetative growth under favorable conditions.
Therefore, the present study was conducted to assess
whether the photosynthate remobilization and the
subsequent yield potential, of an interspecific advanced
bean line resulting from a cross between P. vulgaris and
P. dumosus can be improved by crossing it with drought-
adapted bean lines possessing higher photosynthate
remobilization capacity. An expected outcome of this
study is to draw initial conclusions for the implementation
of respective crosses in breeding programs aiming for the
introgression of desirable traits from the secondary gene
pool into P. vulgaris.
MATERIALS AND METHODS
Experimental site and meteorological conditions
The experiment was conducted during the dry season from June to
September 2009 at the main experimental station of the
International Center for Tropical Agriculture (CIAT) in Palmira,
Colombia, located at latitude 3° 29‟ N, longitude 76° 21‟ W and an
altitude of 965 m. The site has an average relative humidity of 74%,
896 mm of annual rainfall and an annual potential evaporation of
1834 mm. The soil is fine-silty, mixed, isohyperthermic Aquic
Hapludoll, having no major fertility problems (pH = 7.7). The trials
were managed according to standard practices to assure normal
growth of the crop (Beebe et al., 2010). During the crop growing
season, the mean maximum and minimum air temperatures were of
29.9 and 19.3°C in June, 32.2 and 19.1°C in July, 32.1 and 19.7°C
in August and 33.1 and 19.5°C in September, respectively. The
total potential pan evaporation of 574 mm during crop growth
exceeded total rainfall, amounting to 86 mm. With 21 mm of rainfall
in June, 8 mm in July, 29 mm in August and 28 mm in July, the
rainfall distribution pattern corresponded to terminal drought stress
conditions (Ludlow and Muchow, 1990).
Plant material
The interspecific [P. vulgaris × (P. vulgaris × P. dumosus)]
advanced inbred line MIB 755 was crossed with seven other
advanced inbred CIAT bean lines. MIB 755 was selected for high
Fe content in the grain from a backcross of an interspecific hybrid of
a Carioca-type common bean line (FEB 226) with a P. dumosus
accession, with FEB 226 as recurrent parent. Despite its valuable
Fe content, it lacks wide acceptance with farmers due to its viney
growth and low grain yields (S. Beebe, unpublished results),
according to the growth pattern described earlier. MIB 755 was a
suitable elite line to study the typical, viney growth pattern of
interspecific bean lines with the secondary gene pool and to use as
a common parent in further crosses for the study. The seven parent
lines crossed with MIB 755 resulted from breeding programs aiming
to produce drought-adapted beans from germplasm originating
from the Mesoamerican gene pool (Kwak and Gepts, 2009), but were
nevertheless chosen to test a range of productivity and
photosynthate remobilization capacity under rainfed conditions
based on earlier experience at CIAT. The only advanced line which

Klaedtke et al. 51
Table 1. Description of bean lines used as parents or as drought-resistant check.
Advanced line
Market class
Inter-specific
Breeding objectives
MIB 755
Carioca-type
Yes
High mineral content, particularly iron.
ALB 49
Red
Yes
Tolerance to Al toxicity, some drought tolerance.
SEN 46
Black
No
Drought adaptation.
SEN 74
Black
No
Drought adaptation.
SER 155
Red
No
Drought adaptation.
SER 16
Red
No
Drought adaptation.
SMR 4
Red
No
High iron content and drought tolerance.
SXB 743
Red
No
Drought resistance.
SER 118
Red
No
Drought resistance, associated with greater ability for remobilizing photosynthates.
had not resulted directly from a drought-breeding program was ALB
49, which was selected from a backcross of a scarlet runner bean
(P. coccineus) accession with SER 16, a drought-adapted line, also
used in the present study. A brief description of the advanced lines
used in crosses or as check (SER 118) is given in Table 1. In the
crosses with SEN 46, SER 16 and SXB 74, MIB 755 was employed
as female parent. In the crosses with ALB 49, SEN 74, SER 155
and SMR 4, MIB 755 was employed as male parent. Seven F1-
progenies resulted from these crosses. One F2-population was
derived from each F1-progeny by self-fertilization, resulting in seven
genetically segregating F2-progeny populations. These F2-
populations, the eight parent lines and one drought-resistant check
(SER 118) were included in the field trial, resulting in a total of 16
genotypes. All of these had indeterminate bush-type growth habits
with little climbing ability [(categories IIa to IIIa according to the
classification as described in van Schoonhoven and Pastor-
Corrales (1987)].
The CIAT advanced line SER 118 was used as drought-resistant
check having better dry matter partitioning ability to produce grain.
Later, the t erm „genotype‟ is used for the genetic materials included
in this study, be they homozygous advanced lines or F2-progenies.
For statistical analysis, genotype categories were formed. The term
„drought-adapted parents„ further on designates the seven
advanced lines which represent a range of drought adaptation and
all were crossed with MIB 755 while ‟progenies‟ designate the F2-
populations resulting from these crosses.
Experimental design
Two field experiments were planted as 4 × 4 lattice designs with
three replications. The 16 genotypes were sown in six-row plots
with 60 cm between rows, using rows of 3.72 m long with a plant to
plant spacing of 7 cm within the row. The progeny of the cross
between MIB 755 and ALB 49 was an exception, as only four rows
of 1.86 m long were sown in each replication because of insufficient
seed that was harvested from the difficult cross between two
interspecific bean lines. The field with irrigated treatment received
eight gravity irrigations of 35 mm of water each during plant growth
to create favorable growth conditions. The field with drought
treatment was irrigated only twice for the establishment of the crop
and then left rainfed to create water-deficit conditions. In the
irrigated environment, two supplementary sowing dates were
needed to fill rows which dropped out because of technical
incidents. The second sowing date had six days of delay compared
to the first date. Rows sown on the third date were not used for
sampling.
All samples for estimation of yields were taken from rows sown
on the first sowing date, while samples for physiological
measurements were taken from rows sown on the first or second
sowing date, when the plants reached the desired developmental
stage.
Yield measurements and phenological assessment
In the irrigated plots, grain was harvested from two rows (from an
average of 73.6 plants) after discarding end plants. In the rainfed
plots, grain was harvested from four rows (from an average of 174.2
plants) to compensate for spatial effects on plant growth. For the
progeny of the MIB 755 × ALB 49 cross, grain from only two rows
was harvested in both the irrigated and rainfed plots. Mean yields
per hectare were corrected for 14% moisture in grain. The drought
intensity index (DII) was calculated according to Fischer and Maurer
(1978). Days to flowering (DF) and days to physiological maturity
(DPM) were determined for each plot. DF is defined as the number
of days after planting until 50% of the plants have at least one open
flower. DPM is the number of days after planting until 50% of plants
have at least one pod losing its green pigmentation.
Assessment of leaf chlorophyll content, dry matter partitioning
and seed P concentration
Foliar greenness was measured from each leaflet of the youngest
fully expanded leaf of six plants in all plots by using a SPAD (soil
plant analysis development) chlorophyll meter (SPAD-502
Chlorophyll Meter, Minolta Camera Co., Ltd., Japan) at mid-pod
filling (MPF) (growth stage code 75 according to the BBCH scale for
beans) under irrigated and rainfed conditions. Dry matter
partitioning was assessed at MPF growth stage and also at harvest.
Plants growing in 1 m of row, chosen to be representative of the
growth on the respective plot were cut at the base. These samples
correspond to an area of 0.6 m2 and averaged 15 plants. Plants
were counted and separated into plant organs which were then
oven-dried for at least two days at 60°C and weighed. At MPF, dry
weights (DW) of leaves, stems and pods and reproductive
structures were determined. Leaf area was measured using a leaf
area meter (model LI-3000, LI-COR, NE, USA) and the leaf area
index (LAI) was calculated. At harvest, DW of stems, pod walls and
seeds, as well as the number of seeds were quantified. Pod
partitioning index (PPI), pod harvest index (PHI) and stem biomass
reduction (SBR) were calculated as defined previously (CIAT, 2009;
Beebe et al., 2010):
PPI (%) =

52 J. Plant Breed. Crop Sci.
PHI (%) =
SBR (%) =
Economic growth rate (EGR), that is, grain yield formed per day of
active plant growth up to physiological maturity was calculated
according to Ramirez-Vallejo and Kelly (1998). Whereas, PHI and
EGR were calculated for each genotype and replication and thus
underwent an ANOVA, PPI and SBR were calculated from means
of genotypes in the respective environment. Total seed P
concentrations were determined according to the procedures
described by Walinga et al. (1989).
Statistical analysis
One plot of ALB 49 was very heavily affected by Macrophomina
phaseolina and therefore was excluded from statistical analyses to
avoid inclusion of an unplanned diverging factor in the crop
environment caused by spatial differences in soil inoculum. Due to
missing data, the ANOVA could not be calculated for the planned
lattice design and was run as for a design of complete randomized
blocks, as suggested by Thomas (2006), by SAS generalized linear
model procedure (SAS Proc GLM), (SAS Insitute, 2004). Combined
analyses of drought and irrigated conditions were conducted with
replication, moisture treatment, genotype and genotype*moisture
treatment interaction as fixed factors. Separate analyses for
drought and irrigated conditions were conducted with replications,
genotypes, and a classification into the four genotype categories
„common parent‟ (that is, MIB 755), „drought-adapted parents‟ (that
is, ALB 49, SEN 46, SEN 74, SER 155, SER 16, SMR 4 and SXB
743), „progenies‟ (that is, the F2-populations resulting from the
crosses between the drought-adapted parents and the common
parent MIB 755) and „check‟ (that is, SER 118) on one hand and
genotypes among „drought-adapted parents‟ and among progenies
on the other as factors. Least square means were generated and
pairwise differences analyzed by Tukey's range test, in the case of
equal sample sizes, or Tukey-Kramer method, for variables with
missing data. Honestly significant differences (HSD) were
computed for a level of probability of 5%. Differences between
genotype categories were estimated and tested using orthogonal
contrasts in the generalized linear model procedure. Pearson‟s
product-moment correlation coefficients and respective significance
levels were calculated using SAS Correlation procedure (SAS Proc
CORR). Traits of F2-prognies were regressed on traits of drought-
adapted parents using the SAS regression procedure (SAS Proc
REG).
In the following, values marked with *, ** or *** are statistically
significant at probability levels of 5, 1 and 0.1%, respectively.
RESULTS
Grain yields ranged between 1372 and 3364 kg/ha under
irrigated conditions and between 130 and 1928 kg/ha
under terminal drought (Table 2). The DII, reflecting
average yield reduction under drought, amounted to 0.57.
The drought-adapted parent SER 16 yielded highest in
both environments, out-yielding the drought-resistant
check. The interspecific lines MIB 755 and ALB 49 had
lowest yields. Although genotype-by-treatment interaction
for yield was non-significant (Table 3), the ranking of
genotypes according to yields differed between the two
environments when taking all genotypes into account and
when considering drought-adapted parents and progenies
separately. Nevertheless, yields under well-watered and
drought conditions were positively correlated. No geno-
type yielding more than the treatment mean under drought
stress yielded less than the mean under irrigation.
Although significant yield differences were found among
drought-adapted parents in both environments, none
were found among the progeny populations (Table 3).
The mean yield of progenies was, however, significantly
higher than that of the common interspecific parent
(Table 2). Significant differences were also found
concerning the time to flower and maturity. Progeny
populations flowered significantly earlier than the common
interspecific parent, but not as early as the mean value of
drought-adapted parents. Drought-adapted parents and
the drought-tolerant check matured earlier than the
interspecific parent and the progeny populations. On
average, the F2-populations matured significantly earlier
than their common interspecific parent under irrigated
conditions (Table 2). DF (Table 4) and DPM (Figure 1)
related negatively with yields regardless of moisture
treatments. The resulting EGR was highest for the
drought-resistant check and the mean of drought-adapted
parents in both environments. The mean EGR of progeny
populations was significantly higher than that of the
interspecific parent (Table 2). At MPF, no significant
differences in shoot biomass were found between geno-
types under irrigated conditions. Under drought, drought-
adapted parents and progeny populations produced
significantly more shoot biomass than the interspecific
MIB 755 and the check genotype (Table 2).
Regarding the values on dry matter distribution among
plant structures, the DW of vegetative plant organs at
MPF, that is, stems and leaves, did not significantly
correlate with grain yield in either of the two
environments, whereas the DW of pods did (rirrigation =
0.7**; rdrought = 0.83***). The following results were found
for LAI and SPAD chlorophyll meter readings (SCMR). As
for total shoot biomass DW, mean LAI at MPF was
significantly higher under irrigated conditions (3.38) than
under drought (2.35). In both environments, the progeny
populations produced the highest mean LAI values of
3.81 for irrigated and 2.54 for drought, differing
significantly from the mean value of 3.02 for drought-
adapted parents under irrigated conditions and from MIB
755 (1.74) and the check (2.01) under drought stress.
Mean SCMR at MPF were significantly higher under
drought (44.5) than under irrigation (42.5). Genotype ×
treatment interaction was significant. Under irrigation and
drought treatments, the mean SCMR of progenies (43.9
and 45.4, respectively) were significantly higher than for
drought adapted parents (41.4 and 44.0, respectively).
MIB 755 scored 44.1 and 43.6 under irrigation and
drought, respectively. Significant differences were found

Klaedtke et al. 53
Table 2. Least square means of yield (kg/ha), DF (d), DPM (d), EGR (kg/ha/d) shoot biomass DW at MPF (kg/ha), stem DW at harvest (kg/ha), PHI (%) and seed P concentration (%) and
respective honestly significant difference (HSD0.05) values under irrigated conditions (ir) and terminal drought stress conditions (td) for individual genotypes and the genotype categories
„drought-adapted parents‟ and „F2-progenies‟.
Yield
DF
DPM
EGR
Shoot DWMPF
Stem DWharvest
PHI
Seed P conc.
ir
td
ir
td
ir
td
ir
td
ir
td
ir
td
ir
td
ir
td
MIB 755
1382
c
130
c
39.0
a
36.7
a
78.0
a
65.7
a
17.7
d
2.0
c
4169
a
1719
b
1673
a
997
b
59.6
c
35.6
c
0.638
a
0.628
a
Drought.adapted parents
SER 16
3364
1928
32.0
32.7
64.3
61.3
52.3
31.4
4214
2714
908
435
80.7
79.3
0.461
0.394
SXB 743
3004
1882
34.0
33.7
68.0
62.7
44.2
30.0
5430
3488
1171
732
79.1
79.1
0.559
0.412
SEN 46
3175
1745
35.3
35.0
69.7
62.7
45.6
27.8
4310
3615
923
643
82.4
78.0
0.469
0.386
SEN 74
2732
1380
38.0
36.3
67.3
65.7
40.6
21.0
4322
2468
1502
825
79.1
77.8
0.533
0.429
SMR 4
2905
1332
38.3
36.0
70.0
64.3
41.5
20.7
3467
3165
1503
784
74.7
71.3
0.586
0.487
SER 155
2881
1299
32.0
33.0
62.3
58.0
46.2
22.4
4004
2944
709
657
79.9
76.9
0.519
0.432
ALB 49
1372
557
39.0
35.9
76.7
69.4
17.9
8.1
2837
2035
1096
1094
73.1
65.2
0.551
0.549
Mean
2776
b
1446
a
35.5
c
34.6
c
68.3
c
63.1
b
43.9
b
23.1
a
4083
a
2918
a
1116
b
739
b
78.4
a
75.9
a
0.526
c
0.441
bc
F2-Progenies from cross:
MIB 755 x SER 16
2900
1210
34.7
34.7
73.0
65.0
39.7
18.6
4735
2600
1130
955
73.5
67.6
0.603
0.406
MIB 755 x SXB 743
2777
1098
35.7
35.0
74.7
64.7
37.3
17.0
4881
3109
1603
867
73.9
69.5
0.591
0.470
MIB 755 x SEN 46
2665
1055
35.7
35.0
72.7
66.3
36.7
16.0
4844
2847
1388
1336
68.3
66.7
0.607
0.421
SEN 74 x MIB 755
2704
1052
38.3
36.7
73.0
67.0
37.1
15.7
4727
2906
1744
1211
75.5
66.8
0.563
0.484
SMR 4 x MIB 755
2449
860
37.3
36.0
76.0
66.0
32.2
13.0
3992
2838
1361
1011
71.1
62.8
0.583
0.516
SER 155 x MIB 755
3067
848
34.3
34.3
72.0
63.7
42.6
13.3
4928
2606
1608
847
76.0
61.8
0.529
0.498
ALB 49 x MIB 755
2686
936
41.3
36.3
79.0
65.7
34.0
14.2
3736
2143
1157
1144
72.0
63.3
0.518
0.456
Mean
2750
b
1008
b
36.8
b
35.4
b
74.3
b
65.5
a
37.1
c
15.4
b
4549
a
2721
a
1427
a
1053
a
72.9
b
65.5
b
0.571
b
0.464
b
SER 118 (check)
3361
a
1508
a
36.0
bc
35.3
b
67.7
c
63.0
b
49.7
a
23.9
a
3800
a
2263
b
974
b
640
b
81.0
a
81.2
a
0.471
c
0.395
c
Treatment mean ***
2714
1176
36.3
35.2
71.5
64.4
38.4
18.4
4275
2716
1278
886
75.0
68.9
0.549
0.460
HSD0.05 genotypes
1283
596
4.3
1.6
2.3
3.7
17.5
9.3
ns
1119
894
479
6.4
15.9
0.136
0.137
a, b, c, d Means within one column marked with different letters have statistically significant differences at a probability level of 5% . ***Differences between treatment means were statistically significant at a
probability level of 0.1% for all traits shown. Conc.: concentrations. ns: result was not statistically significant.
among drought-adapted parents and progenies
regardless of irrigated or drought stress treat-
ments. Under irrigation, SCMR readings at MPF
correlated negatively with grain yield (r = -0.65**)
and EGR (r = -0.77***). Among the plant
structures weighed at harvest, stem DW under
drought correlated negatively with grain yields
under drought (r = -0.67**) and irrigation (r = -0.56*).
The PHI of the common interspecific parent was
significantly lower than that of any other genotype
category, whereas the progeny mean was below
that of the drought-adapted parents and drought-
resistant check (Table 2).
Note that the common interspecific parent MIB
755 showed by far the lowest PPI (Figure 2) and
increased its shoot biomass DW between MPF
and harvest under drought, as reflected by a
negative SBR value (Figure 3). Under drought
conditions, positive correlations of SBR with PHI (r
= 0.65**) and PPI (r = 0.5*) were found while
correlations with seed P concentration (r = -0.58*)
and stem DW at harvest (r = -0.76***) were
negative. In the irrigated environment, SBR cor-
related positively with shoot biomass DW at MPF
(r = 0.56*) but negatively with PPI (r = -0.58*). The
mean P concentration in seeds at harvest was
significantly lower for the progeny populations

54 J. Plant Breed. Crop Sci.
Table 3. Degrees of freedom (DFr) and type I sums of squares of main effects for yield (kg/ha) and
days to physiological maturity (d) in the combined ANOVA of traits observed on 9 advanced bean
lines and 7 F2-progenies grown under irrigation and drought stress in Palmira, Colombia.
Source
DFr
Sum of squares (Type I)
Yield
DPM
Treatment
1
54960192.6*
1224.4*
Genotype
15
22613051.3*
1092.7*
Genotype category
3
11518819.7*
498.5*
Among drought-adapted parents
6
10518011.8*
519.6*
Among progenies
6
576219.9
74.6*
Genotype x treatment interaction
15
2096739.6
228.4*
Replication (within treatment)
4
702884.1
5.5
Error
59
5566988.8
56.0
* Statistically significant at a probability level of 5%.
Table 4. Correlation coefficients (r) between grain yield, DPM and P concentration in seeds and yield
components and biomass and partitioning traits observed on 9 advanced bean lines and 7 F2-progenies
grown under irrigation (ir) and terminal drought stress (td) in Palmira, Colombia.
Variable
Grain yield (kg/ha)
DPM (d)
Seed P conc. (%)
DF (d)
ir
-0.58
*
0.78
***
0.32
td
-0.60
*
0.75
***
0.56
*
Seed P conc. (%)
ir
-0.58
*
0.56
*
.
td
-0.89
***
0.51
*
.
Stem DWharvest (kg/ha)
ir
-0.32
0.51
*
0.64
**
td
-0.67
**
0.78
***
0.44
PPI (%)
ir
0.48
-0.39
-0.51
*
td
0.80
***
-0.46
-0.86
***
PHI (%)
ir
0.75
***
-0.76
***
-0.81
***
td
0.90
***
-0.47
-0.87
***
SBR (%)
ir
0.25
-0.10
-0.08
td
0.77
***
-0.63
**
-0.58
*
*, **, *** Statistical significance at a probability level of 5, 1 and 0.1%, respectively. conc.: concentration.
than for MIB 755 (Table 2). Yields were negatively
correlated with seed P concentration, as were partitioning
indices, regardless of irrigated or drought stress treat-
ments (Table 4). SBR correlated negatively with seed P
only under drought. Under irrigation, stem DW at harvest
correlated with seed P concentration. The partitioning
indices related more strongly with grain yield under
drought. PHI was among the traits most strongly related
with grain yields regardless of irrigated or drought stress
treatments. The relation of partitioning indices PPI and
PHI obtained under drought with grain yields produced
under irrigation is illustrated in Figure 2. Whereas, SBR
correlated with grain yield and early maturity under
drought, it did not under irrigation (Figure 3). The
regression analysis of grain yields and DPM of the F2
progenies under irrigated conditions on traits expressed
by their respective drought-adapted parent line under
drought and irrigated conditions revealed more parent
traits with an effect on the time to maturity than on yield
of progenies.
Regarding parent traits expressed under drought
stress, DF and LAI at MPF were related negatively with
progeny yield under irrigation (Table 5).
DISCUSSION
Significant differences between irrigated and drought

Klaedtke et al. 55
Figure 1. Days to physiological maturity (DPM) in days vs. grain yield (kg/ha) of nine advanced bean lines and seven F2-progenies
grown under A) irrigated conditions and B) under terminal drought stress in Palmira, Colombia. * indicates statistical significance at a
probability level of 5%.
Figure 2. Pod partitioning and pod harvest indices (%) of nine advanced bean lines and seven F2-progenies
under terminal drought stress vs. their grain yield (kg/ha) under irrigated conditions in Palmira, Colombia. ***
indicates statistical significance at a probability level of 0.1%.
stress treatments of overall means for grain yield,
phenological traits and total shoot biomass DW indicate
severe drought stress conditions in the rainfed crop. It
has been argued that DII values above 0.50 allow for
identification of high levels of drought resistance,
whereas genetic differences in germplasm may not result
in significant differences under very severe terminal
drought stress (Singh, 2007). Hence, the observed DII of
0.57 should permit the determination of genetic
differences of genotypes under severe terminal drought
in the rainfed environment. Grain yields obtained in the
favorable irrigated environment are considered as
reflecting yield potential of the respective genotype
(Beebe et al., 2008).

56 J. Plant Breed. Crop Sci.
Figure 3. Stem biomass reduction (%) vs. grain yield (kg/ha) of nine advanced bean lines and seven F2-progenies grown
under irrigated conditions and under terminal drought stress in Palmira, Colombia. *** indicates statistical significance at a
probability level of 0.1%; ns indicates that a result was not statistically significant.
Table 5. Regression coefficients (b1) and coefficients of determination (R2) of yield and DPM
of 7 F2-families irrigated conditions on selected traits expressed by the respective drought-
adapted parents.
Progenies, irrigated
Yield (kg/ha)
DPM (d)
b1
R2
b1
R2
Parent traits under drought
Yield (kg/ha)
0.080
0.04
-0.004
0.49
EGR (kg/ha/d)
6.919
0.08
-0.230
0.54
DF (d)
-102.624
*
0.65
0.826
0.26
DPM (d)
-35.912
0.43
0.560
*
0.66
LAI at MPF
-377.911
*
0.74
1.110
0.04
Stem DWharvest (kg/ha)
-0.427
0.19
0.010
*
0.63
PHI (%)
16.498
0.20
-0.423
**
0.81
SBR (%)
0.061
0.00
-0.083
*
0.64
Seed P conc.
-1305.904
0.15
37.837
**
0.79
Parent traits under irrigation
Yield (kg/ha)
0.057
0.04
-0.003
*
0.67
EGR (kg/ha/d)
6.088
0.12
-0.194
*
0.75
DF (d)
-53.565
*
0.67
0.569
0.47
DPM (d)
-28.435
0.45
0.472
**
0.78
SCMR at MPF
-53.361
0.42
0.800
*
0.59
Stem DWharvest (kg/ha)
-0.502
*
0.61
0.003
0.13
PHI (%)
29.303
0.25
-0.678
**
0.84
*, ** Statistical significance at a probability level of 5 and 1%, respectively. conc.: concentration.

The common interspecific parent
The common interspecific parent, MIB 755, presented
growth patterns differing markedly from the drought-
adapted common bean lines used in the trial. Low
photosynthate partitioning and subsequent remobilization
capacity, as reflected by low PPI and PHI under drought,
led to low grain yield under irrigation despite similar shoot
biomass production. High SCMR at MPF, reflecting high
chlorophyll content in leaves, also indicate excessive
vegetative growth and delayed senescence of leaves
inhibiting a clear transition to reproductive growth and
development. Consequently, maturity was reached more
than 10 days after the check and EGR was extremely
low. In fact, this poor response of MIB 755 to favorable
growth conditions led its mean grain yield to be
significantly lower than yields of the drought-resistant
check and all drought-adapted parents with the exception
of ALB 49, an interspecific line with P. coccineus.
Congruent growth tendencies were observed under
drought. Although total shoot biomass production was
lowest of all, it did not differ significantly from the drought
tolerant check. However, the mean yield of MIB 755
demonstrates a crop failure, whereas the check was
among the highest-yielding lines. Apart from extremely
poor dry matter partitioning towards grain yield, this is
explained by a negative SBR value. Even after the onset
of pod-filling, the MIB 755 crop continued storing of
photosynthates in stems instead of remobilizing them to
pods and seeds.
In conclusion, overlapping vegetative and reproductive
phases inherited from P. dumosus seem to hamper
drought-adaptation and also resulted in poor response to
favorable conditions as recorded in MIB 755.
Yields, phenology and economic growth rate
Acceleration of flowering and maturity have been
identified as important traits in adaptation of common
bean to terminal drought (White and Singh, 1991a;
Rosales-Serna et al., 2004), but early maturity has
generally been associated with lower yield potential in
favorable environments (White and Singh, 1991b).
Nevertheless, the correlation between irrigated grain yield
and DPM was significant and negative. Congruent
relationships were also found in interspecific RIL from
crosses of P. vulgaris with P.coccineus, leading to the
conclusion that traits inherited from P. coccineus may
have dominated and subsequently led to late maturity,
excessive vigor and inefficient partitioning of photo-
synthates to grain (Beebe et al., 2009), as observed in
the interspecific lines (ALB 49 and common parent MIB
755) and progeny populations when compared with the
drought-adapted common bean lines and the check. Two
reasons thus explain the negative correlation of DPM and
yield potential: Firstly, by simultaneous selection for grain
Klaedtke et al. 57
yield and early maturity (Wallace et al., 1993; Kelly et al.,
1999) under drought, breeders might have indirectly
selected for higher EGR in the drought-adapted lines.
Secondly, the inclusion of interspecific lines and
populations means that longer maturity in those
genotypes was attributed to excessive vegetative growth
and hence low EGR.
Photosynthate partitioning and remobilization
In both the drought and favorable environment, grain
yields correlated with pod DW, but not with DW of
vegetative plant structures, indicating that yields were
generally limited more by the capacity to partition dry
matter to reproductive growth than by lack of dry matter
accumulation. In view of the stronger reliance of grain
filling upon the remobilization of photosynthates within
the plant (Egli and Leggett, 1976), the variation of
photosynthate remobilization and partitioning capacity
may be expressed more clearly under drought. In
addition, the utilization of total shoot biomass at MPF for
the calculation of PPI can lead to an underestimation of
the maximal shoot biomass and overestimation of PPI for
some genotypes: the total shoot biomass DW of bush-
type bean crops commonly peak at the onset of rapid pod
growth, but some genotypes obtain their maximum
canopy DW near maturity (White and Izquierdo, 1991),
particularly under irrigation (Rosales-Serna et al., 2005).
For the interpretation of results, partitioning indices
obtained under terminal drought were thus assumed to
reflect the true potential of genotypes for photosynthate
partitioning to seed, particularly in the case of PPI. The
positive correlation of partitioning indices PHI and PPI
with yield under drought highlight the importance of both
steps of dry matter partitioning for yield production, that is
i) from vegetative biomass to pods, indicated by the PPI,
and ii) from pod wall to grain, indicated by the PHI. The
remobilization of photosynthates stored first in stems,
then in pod walls, to seeds has also been found to be
important for drought tolerance in Lupinus albus and
Lupinus mutabilis (Carvalho et al., 2004, 2005).
In the irrigated treatment, yield only directly correlated
with PHI. This does not contradict the importance of the
partitioning of photosynthates to pods, but indicates
yields were limited by poor allocation of dry matter to
seeds within pods rather than by pod formation. Beebe et
al. (2009) have found significant variability among bean
genotypes for mobilization of photosynthates from pod
walls to seeds and termed the failure to fulfill this very last
step of grain production as “lazy pod syndrome”. Of all
traits, PHI showed strongest correlations with yield
regardless of the irrigated or drought treatment.
Confirming its poor photosynthate remobilization
capacity, the PHI of MIB 755 was significantly below that
of any other genotype examined. Yield, partitioning
indices and EGR were negatively correlated with grain P

58 J. Plant Breed. Crop Sci.
concentration, suggesting that some genotypes utilize
acquired P more efficiently for grain production (Rao et
al., 2007). Yields related more strongly with low seed P
concentrations under drought than under irrigation. The
strong correlation of SBR values observed under drought
conditions with yields obtained under drought and
irrigated conditions indeed corroborates the importance
of the capacity to efficiently remobilize stem reserves to
pods for improving yield potential under favorable,
irrigated conditions as well as under drought conditions.
However, the physiological processes linked to this
remobilization seem to differ between plants grown under
drought stress and under favorable conditions. SBR
under irrigation and drought were in fact unrelated,
indicating that differences in stem reserve remobilization,
unlike other traits conducive to efficient reproductive
growth and earliness, were environmentally induced.
Under drought, SBR correlated negatively with seed P
concentration and stem DW at harvest and positively with
PHI and PPI. This indicates that superior performers
remobilize greater amounts of photosynthates from stems
to seed per unit amount of P mobilized to seed (CIAT,
2005, 2006). In contrast, under favorable conditions, SBR
correlated positively with shoot biomass DW at MPF and
negatively with PPI, suggesting that genotypes having
accumulated much dry matter in canopy, remobilized
more photosynthates from stems, but did not mobilize
them to pods. Such genotypes may have remobilized
photosynthates to leaves to favor vegetative growth
instead of making a clear transition to reproductive
growth. This was particularly observed for the common
interspecific parent and, to a lesser extent, the F2-
progenies. Although, there was no direct relation to yield,
stem DW at harvest correlated negatively with PHI and
positively with seed P concentration and DPM in the
favorable environment. No such correlations with PHI and
seed P concentration were observed for SBR in the
favorable environment. One may conclude that stem
reserve remobilization is a crucial stage of plant efficiency
for reproductive growth under drought, but it alone does
not ensure plant efficiency under favorable conditions. In
contrary, remobilized photosynthates in some cases
seem to be used for non-reproductive purposes such as
the maintenance of “stay-green” vegetative structures. In
fact, efficient partitioning and good response to favorable
conditions are associated with the ability to harness
vegetative growth independently of the ability to later
remobilize stem reserves, as indicated by low stem DW
at harvest.
Harnessing the vegetative growth may thus be related
with a clear transition from vegetative to reproductive
growth under favorable conditions.
F2-populations
The mean score of the progenies was between that of the
drought-adapted parents and the common interspecific
parent for most of the traits discussed. Under favorable
conditions, this was not obvious at first glance in the field,
as most progenies were actually more vigorous than MIB
755, as indicated by shoot biomass DW and LAI.
Nevertheless, mean stem DW of progenies at MPF and
harvest were below that of MIB 755, indicating that they
did not accumulate as much excessive stem reserves as
MIB 755. The significant negative relation of progeny
yields under irrigation with DF of respective parents, as
well as their stem DW at harvest under irrigation indicates
that parents having ability of harnessing vegetative
growth under favorable conditions and generally making
an early transition to reproductive growth resulted in
progenies with a better response to the favorable
environment. The LAI of parents under drought related
negatively with progeny yield potential, suggesting that
even under water-stress, some drought-adapted parents
were overly vigorous and passed on this trait to
progenies. However, yield differences among progenies
were non-significant. The selection of drought-adapted
parents with a range of remobilization and partitioning
capacities according to past experience was expected to
lead to a range in progeny yields. In fact, the PHI, which
correlated strongly with yields when including all geno-
types was similarly high for all drought-adapted parents in
this trial: Only SMR 4 and ALB 49 significantly differed
from other drought-adapted parents under irrigation and
no significant differences were found under drought.
Crossing MIB 755 with the drought-adapted parents
thus generally improved the dry matter partitioning within
pods in the progenies, but the limited range of PHI
represented did not allow for a strong differentiation
among progenies concerning this trait. On the other
hand, differences in plant efficiency of drought-adapted
parents in both environments were reflected in progenies
as earliness to mature under favorable conditions. Apart
from DPM of parents in both environments, traits
associated with efficient dry matter partitioning at all
levels under drought related with earliness of progenies
under favorable conditions. Early maturing progenies
were also produced by drought-adapted parents beginning
to senesce at MPF, as indicated by lower SCMR, and
having a strong capacity to remobilize photosynthates to
seeds within pods and produce high yields under
favorable conditions. Thus, those drought-adapted
parents that were able to counterbalance MIB 755‟s
excessive vegetative growth under favorable conditions
and “lazy pod syndrome” in both environments produced
more efficient progenies, although this efficiency was
expressed more by earliness than in grain yields. The
progeny of SER 16 stood out for its above-mean yields in
both environments, in line with the yields and the
remobilization and partitioning capacities of SER 16,
particularly concerning PHI. Except for ALB 49, it is the
only advanced line in the trial having race Durango
parentage, known for its rapid and complete transition to
reproductive growth with rapid seed filling and high HI
(Kelly et al., 1999). Race Durango germplasm has been

identified as an important source of drought resistance in
interracial crosses (Beebe et al., 2008; Porch et al.,
2009).
ALB 49 is a selection from an interspecific cross
including SER 16 as recurrent parent. Under irrigation, its
progeny yielded well above the best yielding parent. On
one hand, the significant result found in this particular
cross may be explained by the wide genetic distance
between parents, which resulted from interspecific
crosses with different Phaseolus species. On the other, it
may indicate that SER 16 produces efficient progenies
even when operating indirectly through offspring
containing SER 16 germplasm. The PPI and PHI of ALB
49 under drought were not high, but certainly acceptable
compared to the values obtained for MIB 755. The
comparatively high partitioning efficiency for an
interspecific bean line is attributable to the SER 16
parentage of ALB 49. The negative SBR values in both
environments constitute an inconsistent transition to the
reproductive phase inherited from the P. coccineus
parent, although overall vigor was low. Hence, the
combination of ALB 49 and MIB 755 germplasm entailed
the combination of acceptable dry matter partitioning with
vigor, leading to the compensation of reciprocal
unfavorable traits. Interestingly, SER 155 combined very
well with MIB 755 concerning yield potential, but poorly
regarding drought resistance, despite SER 155‟s
intermediate performance in both environments. The
parent‟s yield limitations under favorable conditions can
be explained by the extremely short growing cycle of
SER 155, restricting the genotype from producing high
grain yield despite high EGR. However, in its progeny, a
significantly longer duration of growth and maturity was
inherited from MIB 755, although it remained earliest to
mature among progenies. Combined with the highest PHI
and EGR among progenies, this led to the highest-
yielding progeny. As found for the progeny of ALB 49, it
seems that the combination SER 155 and MIB 755 led to
the compensation of reciprocal unfavorable traits for yield
potential. Low yields of the SER 155 progeny under
drought may be attributed to a shallow rooting system
inherited from SER 155, as detected on the parent in a
greenhouse trial.
In contrast, SMR 4 produced the lowest yielding
progeny. The shoot dry matter accumulation of the SMR
4 progeny was among the lowest under irrigation, but
above that of high-yielding drought-resistant check SER
118. So, vigor was not a limiting factor, but PHI below the
progeny mean indicates “lazy pod syndrome”. SMR 4
indeed had below average PHI and lacked seed filling in
the favorable environment as did MIB 755. Crossing the
two bean lines thus led to a similarly inefficient, low-
yielding progeny. Given their dry matter partitioning traits,
the black-seeded lines SEN 46 and SEN 74 combined
with interspecific MIB 755 in an unexpected manner.
Although the yield of the progeny of SEN 74 cor-
responded with the intermediate performance expected
Klaedtke et al. 59
from the intermediate remobilization and partitioning
capacity of SEN 74, the patterns of dry matter partitioning
within the progeny were quite different than that of SEN
74. Conversely, the progeny of SEN 74 had the lowest
PPI of all progenies under drought, although SEN 74
produced highest PPI. In contrast to the efficiency
observed in both the irrigated and drought environment
for the other black-seeded drought-adapted parent SEN
46, its progeny lacked efficiency to exploit the high
amount of dry matter accumulated in shoots despite very
high SBR. This progeny was, however, among the
earliest to mature under favorable conditions, again
indicating that plant efficiency inherited from drought-
adapted parents can be expressed more as earliness
than as yield potential in some progenies. On one hand,
SEN 46 and its progeny may indicate that high
remobilization and partitioning capacities as recorded by
high SBR and PHI values are not sufficient to
counterbalance inefficiencies inherited from MIB 755 in
progenies. On the other hand, the traits of progenies of
SEN 46 and SEN 74 with MIB 755 suggest that black-
seeded (SEN) lines do not combine well with MIB 755 as
do red-seeded (SER) lines.
Indeed, differences in combining abilities have been
found between the market classes. For example red-
seeded Mesoamerica lines have been found to combine
better with race Durango than black-seeded ones for
enhanced drought resistance (Beebe et al., 2008).
Conclusions
The results of the present study highlight problems that
are inherent in interspecific crosses of common bean with
its secondary gene pool. The evolution of species such
as P. dumosus or P. coccineus has favored a vigorous
vegetative growth at the expense of efficiency in grain
production. We have referred to the many attempts to
utilize these species to improve common beans,
especially as sources of disease resistance and in spite
of the number of attempts, very few common bean
cultivars carry genes derived from these species. We
suggest that the problems of poor photosynthate
remobilization that were documented in MIB 755 are
symptomatic of the poor quality of such interspecific
progenies. Using parents with enhanced photosynthate
remobilization capacity should be part of the strategy to
tap the vast genetic diversity of the secondary gene pool.
Under scenarios of climate change in which some
regions of the tropics are expected to receive significantly
more rainfall, these species may become more attractive
as sources of traits for humid environments, in which
case their use in breeding programs may be more
frequent (Beebe et al., 2011). For further investigation, it
is recommended that corresponding field trials be re-
peated with a higher number of drought-adapted parents
and various interspecific parents to verify relations found

60 J. Plant Breed. Crop Sci.
in this study. Maternal effects involved when the
interspecific or drought-adapted parent is used as
maternal parent also need to be further examined.
Finally, the combining ability of black-seeded lines with
interspecific lines should be investigated.
ACKNOWLEDGEMENTS
The first author wishes to recognize the support of the
Advisory Service on Agricultural Research for
Development (BEAF) of the Deutsche Gesellschaft für
Technische Zusammenarbeit GmbH (GTZ) for the
accomplishment of this study. The field work was partially
supported by the Tropical Legumes II project managed
by the International Crops Research Institute for the Semi
Arid Tropics (ICRISAT) and is funded by the Bill and
Melinda Gates Foundation.
Abbreviations: Al, Aluminum; CIAT, International Center for
Tropical Agriculture; DF, days to flowering; DII, drought intensity
index; DPM, days to physiological maturity; DW, dry weight;
EGR, economic growth rate; Fe, iron; HI, harvest index; HSD,
honestly significant difference; LAI, leaf area index; MPF, mid-
pod filling; P, phosphorus; PHI, pod harvest index; PPI, pod
partitioning index; SCMR, SPAD chlorophyll meter reading;
SBR, stem biomass reduction; Zn, zinc.
REFERENCES
Beebe S, Ramirez J, Jarvis A, Rao IM, Mosquera G, Bueno JM, Blair M
(2011). Genetic improvement of common beans and the challenges
of climate change. In: Yadav SS, Redden RJ, Hatfield JL, Lotze-
Campen J and Hall AE (eds), Crop Adaptation to Climate Change.
John Wiley and Sons, Ltd. Published by Blackwell Publishing Ltd.,
pp. 356-369.
Beebe SE, Rao IM, Blair MW, Acosta-Gallegos JA (2010). Phenotyping
common beans for adaptation to drought. In: Ribaut JM and
Monneveux P (eds), Drought phenotyping in crops: from theory to
practice, Generation Challenge Program Special Issue on
Phenotyping, pp. 311-334.
Beebe SE, Rao IM, Blair MW, Butare L (2009). Breeding for abiotic
stress tolerance. In: Common Bean: Present and Future Challenges,
Keynote addresses from the 14th Australasian Plant Breeding and
11th SABRAO Conference. Cairns, Queensland, Australia:
http://km.fao.org/gipb/index.php?option=com_contentandview=categ
oryandlayout=blogandid=156andItemid=409andlang=en (last
accessed on October 10th 2010 at 23:35 CET).
Beebe SE, Rao IM, Cajiao C, Grajales M (2008). Selection for drought
resistance in common bean also improves yield in phosphorus limited
and favorable conditions. Crop Sci., 48: 582-592.
Beebe SE, Rao IM, Terán H, Cajiao C (2006). Breeding concepts and
approaches in food legumes: The example of common bean.
Proceedings of the Second National Workshop on Food and Forage
Legumes, 22.-27. September, 2003, Addis Abeba, Ethiopia, pp. 23-
29.
Broughton W, Hernández G, Blair MW, Beebe SE, Gepts P,
Venderleyden J (2003). Beans (Phaseolus spp.) - model food
legumes. Plant Soil, 252: 55-128.
Butare L, Rao IM, Lepoivre P, Polania J, Cajiao C, Cuasquer JB, Beebe
S (2011). New sources of resistance in Phaseolus species to
individual and combined aluminium toxicity and progressive soil
drying stresses. Euphytica, 181: 385-404.
Carvalho IS, Chaves M, Ricardo CP (2005). Influence of water stress on
the chemical composition of seeds of two lupins (Lupinus albus and
Lupinus mutabilis). J. Agron. Crop Sci., 191: 95-98.
Carvalho IS, Ricardo CP, Chaves M (2004). Quality and distribution of
assimilates within the whole plant of lupines (L. albus and L.
mutabilis) influenced by water stress. J. Agron. Crop Sci., 190: 205-
210.
CIAT (Centro Internacional de Agricultura Tropical) (2005). Annual
Report 2004, Project IP-1: Bean Improvement for the tropics, CIAT,
Cali, Colombia.
CIAT (Centro Internacional de Agricultura Tropical) (2006). Annual
Report 2005, Project IP-1: Bean improvement for the tropics, CIAT,
Cali, Colombia.
CIAT (Centro Internacional de Agricultura Tropical) (2008). Annual
Report 2007. Outcome Line SBA-1: Improved beans for the
developing world, CIAT, Cali, Colombia.
CIAT (Centro Internacional de Agricultura Tropical) (2009). Annual
report 2008. Outcome line SBA-1: Improved beans for the developing
world, CIAT, Cali, Colombia.
Debouck D (1999). Diversity in Phaseolus species in relation to the
common bean. In: Singh SE, Common bean improvement in the
twenty-first century, Kluwer, Dordrecht, The Netherlands, pp. 25-52.
Egli D, Leggett J (1976). Rate of dry matter accumulation in soybean
seeds with varying source-sink ratios. Agron J., 68: 371-374.
FAOSTAT (2010): http://faostat.fao.org/site/567/default.aspx#ancor (last
accessed on October 10th 2010, at 23:40 CET).
Fischer R, Maurer R (1978). Drought resistance in spring wheat
cultivars. I. Grain yield responses. Aust. J. Agric. Res., 29: 897-912.
Harlan J, de Wet J (1971). Toward a rational classification of cultivated
plants. Taxon: Journal of the International Association for Plant
Taxonomy / the International Bureau for Plant Taxonomy and
Nomenclature, 20: 509-517.
Kelly J, Schneider K, Kolkman J (1999). Breeding to improve yield. In:
Singh SP, Common bean improvement in the twenty-first century,
Kluwer Academic Publishers, Dordrecht, The Netherlands, pp. 185-
222.
Kornegay J, Cardona C (1991). Breeding for insect resistance in beans.
In: van Schoonhoven A and Voysest O, Common beans. Research
for crop improvement, CAB International, Wallingford, UK and CIAT,
Cali, Colombia, pp. 619–648.
Kwak M, Gepts P (2009). Structure of genetic diversity in the two major
gene pools of common bean (Phaseolus vulgaris L., Fabaceae).
Theor. Appl. Genet., 118:979–992.
Ludlow M, Muchow R (1990). A critical evaluation of traits for improved
crop yields in water-limited envrionments. Adv. Agron., 43: 107–153.
Muñoz-Perea C, Terán H, Allen R, Wright J, Westermann D, Singh S
(2006). Selection for drought resistance in dry bean landraces and
cultivars. Crop Sci., 46: 2111–2120.
Porch TG, Ramirez VH, Santana D, Harmsen EW (2009). Evaluation of
common bean for drought tolerance in Juana Diaz, Puerto Rico. J.
Agron. Crop Sci., 195: 328–334.
Ramirez-Vallejo P, Kelly J (1998). Traits related to drought resistance in
common bean. Euphytica, 99: 127-136.
Rao IM (2001). Role of physiology in improving crop adaptation to
abiotic stresses in the tropics: The case of common bean and tropical
forages. In: Pessarakli M, Handbook of plant and crop physiology,
2nd edition, Marcel Dekker, New York, 583-613.
Rao IM, Beebe SE, Polanía J, Grajales M, Cajiao C, García R, Ricaurte
J, Rivera M (2009). Physiological basis of improved drought
resistance in common bean: the contribution of photosynthate
mobilization to grain. Paper presented at Interdrought III: The 3rd
International Conference on Integrated Approaches to Improve Crop
Production under Drought-Prone Environments, October 11-16,
2009, Shanghai, China.
Rao IM, Beebe SE, Ricaurte J, Cajiao C, Polanía J, García R (2007).
Phenotypic evaluation of drought resistance in advanced lines of
common bean (Phaseolus vulgaris L.). Paper presented at the ASA-
CSSA-SSSA International Annual Meeting, New Orleans, LA, USA,
4-8 November, 2007.
Rosales-Serna R, Kohashi Shibata J, Acosta Gallegos J, Trejo López
C, Ortiz Cerecerces J, Kelly J (2005). Contenido de carbohidratos en
los órganos de la planta y rendimiento del frijol en sequía.
Carbohydrate content in plant organs and seed yield in common

bean under drought stress. Agric. Téc. Méx., 31: 139-151.
Rosales-Serna R, Kohashi-Shibata J, Acosta-Gallegos J, Trejo-López
C, Ortiz-Cereceres J, Kelly J (2004). Biomass distribution, maturity
acceleration and yield in drought-stressed common bean cultivars.
Field Crops Res., 85: 203-211.
SAS Insitute (2004). The SAS system for windows. Version 9.1. SAS
Inst., Cary, N.C., USA.
Singh S (2001). Broadening the genetic base of common bean cultivars:
A review. Crop Sci., 41: 1659-1675.
Singh S (2007). Drought resistance in the race Durango dry bean
landraces and cultivars. Agron. J., 99: 1219-1225.
Singh S, Debouck D, Roca W (1997). Successful interspecific
hybridization between Phaseolus vulgaris L. and Phaseolus
costaricensis Freytag and Debouck. Annual Report of the Bean
Improvement Cooperative, 40, 40-41.
Smithsonian Institution Bureau of American Ethnology (1950).
Handbook of south American Indians, Volume 6.
Thomas E (2006). Feldversuchswesen. UTB, Stuttgart Germany.
van Schoonhoven A, Pastor-Corrales MA (1987), Standard system for
the evaluation of bean germplasm. Centro Internacional de
Agricultura Tropical, CIAT, Cali, Colombia.
Walinga, I, van Vark W, Houba V, van der Lee J (1989). Plant Analysis
Procedures (Soil and Plant Analysis, Part 7). Department of Soil
Science and Plant Nutrition, Wageningen Agricultural University,
Wageningen, The Netherlands.
Klaedtke et al. 61
Wallace DH, Baudoin JP, Beaver J, Coyne DP, Halseth DE, Masaya
PN, Munger HM, Myers JR, Silbernagel M, Yourstone KS, Zobel RW
(1993). Improving efficiency of breeding for higher crop yield. Theor.
Appl. Genet., 86: 27-40.
White J, Izquierdo J (1991). Physiology of yield potential and stress
tolerance. In: van Schoonhoven A and Voysest O, Common beans.
Research for crop improvement, CAB International, Wallingford, UK
and CIAT, Cali, Colombia, pp. 287-382.
White J, Singh S (1991a). Breeding for adaptation to drought. In: van
Schoonhoven A and Voysest O, Common beans. Research for crop
improvement, CAB International, Wallingford, UK and CIAT, Cali,
Colombia, 501-560.
White J, Singh S (1991b). Sources and inheritance of earliness in
tropically adapted indeterminate common bean. Euphytica, 55: 15-19.