Expression of the Narrow Leaflet Gene for
Yield and Agronomic Traits in Soybean
R. D. Dinkins, K. R. Keim, L. Farno, and L. H. Edwards
Genes that affect plant form and function may be used to enhance the yield of
soybean [Glycine max (L.) Merr.]. Most soybean cultivars have broad (ovate) leaflets. A single gene, ln, controls inheritance for the narrow leaflet characteristic.
Narrow leaflet cultivars (ln/ln) also tend to have a higher percentage of four-seeded
pods than ovate (Ln/Ln) leaflet cultivars. Heterozygous (Ln/ln) plants have a leaflet
shape intermediate between narrow and ovate. Determining the agronomic effects
of the narrow leaflet allele (ln) in the heterozygous (Ln/ln) condition in soybean may
have applications in practical plant breeding. We studied an ovate leaflet and a
narrow leaflet cultivar, crosses between them in the F1 and F2, and backcrosses to
both cultivars. The ratio of leaflet width to leaflet length accurately distinguished
among narrow, ovate, and intermediate leaflet plants in the F2 and backcross generations. In the F2 generation, differences occurred among plants with different
leaflet morphology. Narrow leaflet plants produced more seeds per pod and lower
seed weight than ovate leaflet plants. Narrow and ovate leaflet plants produced
comparable numbers of pods per plant and plant yield. Compared to ovate leaflet
plants, intermediate leaflet plants produced similar numbers of seeds per pod and
seed weight. Intermediate leaflet plants produced significantly more pods per plant
and plant yield than plants with either ovate or narrow leaflets. The heterozygous
condition at the locus for leaflet morphology resulted in heterosis for plant yield
and may be of benefit in association with commercialization and development of
hybrid soybean.
From the Department of Plant and Soil Sciences,
Oklahoma State University, Stillwater, OK 74078 ( Keim,
Farno, and Edwards). R. D. Dinkins is currently at the
Department of Agronomy, University of Kentucky, Lexington, KY 40546. L. H. Edwards is Professor Emeritus.
Published with the approval of the Director of the
Oklahoma Agricultural Experiment Station, Oklahoma
State University, Stillwater, OK. This work was supported in part by the Oklahoma Agricultural Experiment Station and the Oklahoma Soybean Board. Address correspondence to K. R. Keim at the address
above, or e-mail: [email protected].
q 2002 The American Genetic Association 93:346–351
346
Most soybean cultivars grown in the United States have broad (ovate) leaflets. This
is considered the ‘‘normal’’ leaflet type. A
few cultivars from the United States and
Asia have distinctive narrow or lanceolate
leaflets. A single gene, ln ( Bernard and
Weiss 1973), controls inheritance of the
narrow leaflet character. The heterozygote
(Ln/ln) was reported to be intermediate
between the two leaflet types, narrow (ln/
ln) and ovate (Ln/Ln), but difficulty occurred in distinguishing between some
ovate and intermediate leaflet plants ( Bernard and Weiss 1973). Domingo (1945)
used various leaflet measuring techniques
in an attempt to differentiate ovate and intermediate leaflet types, but found no reliable index to use. However, only a few
plants were measured from each cross.
An association between narrow leaflet
and the number of seeds per pod was first
observed by Takahashi (1934). Narrow
leaflet cultivars tend to have a higher percentage of four-seeded pods compared to
ovate leaflet cultivars. Domingo (1945)
studied crosses between ovate and nar-
row leaflet types and suggested a crossover percentage of 7.9 6 0.8 between the
narrow leaflet gene and a presumed gene
for the number of seeds per pod. Johnson
and Bernard (1962) considered a high
number of seeds per pod and narrow leaflet to be pleiotropic effects of the same
allele. Weiss (1970) concluded that the
narrow leaflet allele exerts a major pleiotropic effect in increasing the frequency of
four-seeded pods, but expression of the
four-seeded trait was decidedly influenced
by the vigor of the plant and modifying
genes.
Previous studies have been conducted
that compared the narrow and ovate leaflet types for yield, but not the intermediate leaflet type ( Hartwig and Edwards
1970; Jain and Singh 1978; Mandl and Buss
1981). Results of these studies indicated
no differences in seed yield between ovate
and narrow leaflet types.
The need exists to determine what, if
any, effects the heterozygous condition at
the locus controlling leaflet morphology
may have on yield and other agronomic
Figure 1. Phenotypic expression of narrow ( left), intermediate (middle), and ovate (right) leaflet types in soybean.
traits as an expression of heterosis. Utilization of hybrid vigor or heterosis has
been successful in cross-pollinated crops,
of which maize (Zea mays L.) is a primary
example. The success of hybrid maize has
produced interest in developing hybrids in
autogamous crops. Hybrids are being utilized in autogamous crops such as rice
(Oryza sativa L.) ( Virmani 1999) and
wheat (Triticum aestivum L.) (Jordaan et
al. 1999). Due to the autogamous nature of
soybean, obtaining large quantities of hybrid seed via manual hybridization is extremely difficult, but there are techniques
with potential for commercial development and application of hybrid soybean.
Aspects of producing and evaluating hy-
brid soybean have been reviewed recently
by Palmer et al. (2001).
Heterosis in soybean has been studied
using space planting. Of 48 F1 hybrids, 32
yielded better than the midparent and 12
yielded better than the high parent (Cerna
et al. 1997). Kunta et al. (1997) reported
six F1 hybrids yielded more than both the
midparent and high parent, with average
midparent and high-parent heterosis percentages of 28% and 18%, respectively.
Heterosis has also been studied where
adequate seed was available for replicated, bordered plots. Average midparent
and high-parent heterosis were reported
to be 28% and 20%, respectively, for two
hybrid combinations ( Brim and Cocker-
Figure 2. Distribution for parental and F1 generations for ratio of leaflet width to leaflet length in soybean.
ham 1961). Of the 10 F2 progeny populations derived from five ancestral founding
strains of southern U.S. soybean, five exhibited heterosis for yield, with mean heterosis of 9.3% (range –1% to 19%) (Gizlice
et al. 1993). For 27 hybrids, 5 yielded significantly more than the high parent in at
least one season of testing, with yield increases ranging between 13% and 19%, but
only 1 hybrid yielded more than the best
pure line cultivar ( Nelson and Bernard
1984).
Various studies have investigated the
contributions of yield components to expression of heterosis for yield. Increases
in heterosis for yield were expressed by
an increased number of pods per plant
rather than increased seeds per pod or increased seed weight (Gadag and Upadhyaya 1995). No significant heterosis for
seed weight was reported by Gizlice et al.
(1993). Seed weight increased in 22 hybrids compared to the midparent value,
but only two hybrids were significantly
greater than the high-parent seed weight
( Nelson and Bernard 1984). Using approximately 1000 hybrid combinations, heterosis for soybean yield was expressed by
increased pod number (Sun et al. 1999).
For a study using space planting, heterosis
for yield was accompanied by an increased number of pods per plant, but not
increased seeds per pod or seed weight
(Gadag and Upadhyaya 1995). For hybrids
with significant heterosis, no significant effect was attributed to seed weight (Gizlice
et al. 1993). High-parent heterosis for number of pods and seeds per plant were reported by Ma et al. (1983). Yield heterosis
was reported to be accompanied by and
attributed to the increased weight per
seed ( Huang et al. 1993).
Instances have been observed where
heterozygous genotypes at a single locus
have had a significant effect on yield. Examples include wheat ( Flintham et al.
1997), maize (Garber and Rowley 1927;
Jones 1945; Mangelsdorf 1928), barley
(Hordeum vulgare L.) (Gustafsson 1946;
Robertson and Austin 1935), and sorghum
[Sorghum bicolor ( L.) Moench] ( Karper
1930; Quinby and Karper 1946). Many of
the genes involved, particularly with
maize, often caused detrimental effects on
plant growth and yield in the heterozygous condition.
This study was designed to evaluate expression of yield and yield components
within ovate, intermediate, and narrow
leaflet types in a population derived from
crosses between an ovate and a narrow
leaflet soybean cultivars.
Dinkins et al • Narrow Leaflet Gene in Soybean 347
Figure 3. Distributions for F2 and backcross generations for ratio of leaflet width to leaflet length in soybean.
Materials and Methods
Parents chosen for this study were cultivars Douglas ( Nickell et al. 1982), which
has ovate (normal) leaflets, and Miles
( Kenworthy and Schillinger 1980), which
has narrow leaflets. Both cultivars are in
maturity group IV and are well adapted to
the geographic area of this study. Original
crosses between parent plants were made
in the field. In the next cropping season,
confirmed F1 plants were grown in the field
and backcrossed to each parent using
Douglas and Miles as females. The F1
plants were also allowed to self-pollinate
to produce the F2 generation. Additional
crosses to produce F1 seed were made between Douglas and Miles.
This study was conducted during one
season at the Perkins Agronomy Research
Station, Perkins, Oklahoma. Experimental
units were individual plants. A total of 130
F1 seeds, 50 backcrossed seeds to Douglas,
56 backcrossed seeds to Miles, 300 seeds
from each of Douglas and Miles, and 353
F2 seeds were planted in hill plots. Three
seeds were planted in each hill plot for
Douglas and Miles, and following emergence, plants were thinned to one per hill.
Because of the limited number of seeds,
two cowpea [Vigna unguiculata ( L.) Walp.]
seeds were planted in each hill with either
a single F1, F2, or backcross seed. This was
to aid soybean seedlings in emerging
through the soil surface, and thus avoid
hypocotyl breakage. Following emergence,
any emerged cowpea seedlings were removed. Available seeds were distributed
as equally as possible among 10 replications. Each replication contained approximately 78 plants. Within a replication,
seeds of each generation were planted in
consecutive hills at a grid spacing of 76
cm 3 76 cm. Replications were arranged
so that each measured a rectangular area
of 7 m 3 9 m. Rows of experimental hill
plots were separated by a row of similarly
spaced control soybean plants of the cultivar Douglas. A row of similarly spaced
Table 1. Number of soybean plants within leaflet type for each generation in crosses with Douglas and
Miles
Leaflet type
Observed
a
Generation
Narrow
Intermediate
Ovate
Expected
ratio
x2
Probability
Douglas
Miles
F1a
F2
Douglas 3 F1
Miles 3 F1
0
72
0
70
0
24
0
0
71
126
11
16
58
0
0
58
18
0
0:0:1
1:0:0
0:1:0
1:2:1
0:1:1
1:1:0
—
—
—
1.15
1.69
1.60
—
—
—
0.7–0.5
0.2–0.1
0.3–0.2
Douglas used as female parent.
348 The Journal of Heredity 2002:93(5)
control plants was planted across the
ends of the rows. Seeds for control plants
were also planted in experimental hill
plots where emergence failed. The soil
type was a Teller loam soil (fine-loamy,
mixed, thermic, Udic Argiustoll). Irrigation
water was applied during the cropping
season as needed. Other cultural practices
of tillage, cultivation, herbicide application, and fertility were conducted as considered standard for the region. Hand
weeding was done to supplement mechanical cultivation.
The center leaflet of the most recent fully expanded leaf on the main stem was
used for leaflet measurements. Leaflet
measurements were done on July 27–29.
All other measurements were done at harvest. The following traits were measured
for each experimental plant: leaflet length
(in centimeters) from the leaflet tip to petiolule attachment; leaflet width (in centimeters) at the widest part of the leaflet;
plant height (in centimeters) from the top
of the terminal raceme to the ground just
prior to harvest; plant biomass at harvest
and after leaves (not recovered) were
drop measured as grams of all remaining
air-dried, above-ground plant materials;
seed weight was measured in grams of a
random sample of 100 seeds; plant yield
was measured as total seed weight (in
grams); number of pods; total number of
seeds (calculated by dividing seed yield
by single seed weight); average seeds per
pod (calculated by dividing total number
of seeds by the number of pods); and harvest index (calculated by dividing plant
yield by plant biomass).
The ratio of leaflet width to leaflet
length was used to classify each plant as
narrow, intermediate, or ovate leaflet type.
Leaflet types were assumed to equate with
genotypes as follows: narrow leaflet, ln/ln;
intermediate leaflet, Ln/ln; ovate leaflet,
Ln/Ln. Ranges for the ratios for each leaflet type were based on the measurements
obtained from parental and F1 plants. Chisquare analyses were performed to test
the homogeneity of expected ratios for
each genotype. The expected ratio for F2
plants was 1 narrow:2 intermediate:1
ovate. Ratios for backcrosses were expected to be 1 intermediate:1 ovate and 1
narrow:1 intermediate for backcrosses to
Douglas and Miles, respectively.
The experimental design was a randomized complete block. A total of 530 plants
were used in the analyses. Analyses of variance (ANOVAs) were conducted to compare narrow, intermediate, and ovate leaflet types in the F2 and backcross
Table 2. Analyses of variance for traits in the F 2 generation in crosses with Douglas and Miles soybean
cultivars
dfa
Block
Leaflet
Block 3 leaflet
Error
CV (%)b
9
2
18
224
Plant
height
Plant
biomass
Seed
weight
Seeds
per pod
Pods per
plant
Plant
yield
Harvest
index
219.4**
12.2
105.4
73.4
12.6
11,414**
38,284**
3473
3326
28.7
10.3**
22.7**
2.4
1.8
9.9
0.1236*
0.1926*
0.0414
0.0548
10.0
12,236*
51,263**
5435
5243
26.8
2701**
6548**
797
716
30.6
0.01451*
0.00043
0.00202
0.00142
8.7
Degrees of freedom.
Coefficient of variance.
* Significant at the 0.05 probability level; ** significant at the 0.01 probability level.
a
b
generations. The assumption was made
that all genes other than leaflet type
would segregate independently. Thus any
differences among plants of varying leaflet
type would be due to an association with
leaflet type.
Results and Discussion
Representative leaflet type phenotypes
are presented in Figure 1. Ranges measured for ratio of leaflet width to leaflet
length were 0.32–0.45, 0.52–0.65, and 0.65–
0.87 for Miles (ln/ln), F1 (Ln/ln), and Douglas (Ln/Ln) plants, respectively ( Figure 2).
Although ranges for Douglas and F1 ratios
met at 0.65, there was no overlap. Based
on parental and F1 ratios, a value of 0.47
was used to differentiate between narrow
and intermediate leaflet types, and a value
of 0.65 was used to differentiate between
intermediate and ovate leaflet types in the
F2 and backcross generations ( Figure 3).
Observed distributions of F2 and backcross generations for leaflet type confirmed expected distributions. However, in
the F2, a definitely lower frequency of
plants expressing ratio values centered on
0.5 occurred.
The observed number of plants relative
to that expected for each leaflet type are
presented in Table 1. If leaflet type is con-
trolled by a single gene pair without dominance, the expected ratio in the F2 should
be 1 narrow:2 intermediate:1 ovate, and
the expected ratios in backcross generations should be 1 ovate:1 intermediate for
backcrosses to Douglas and 1 narrow:1 intermediate for backcrosses to Miles. Probability levels indicated that observed data
represented a good fit to expected ratios
in the F2 and backcross generations.
ANOVAs indicated significant differences among leaflet types in the F2 generation
for most traits studied ( Table 2). Enhanced experimental design due to a
blocking arrangement was apparent from
significant block effects for all traits. The
only difference detected between leaflet
types in the backcross generations for any
trait was the number of seeds per pod in
the backcross to Miles ( Table 3). For backcrosses, the reason no more differences
were detected may be due to sampling error, because of the small numbers of backcross plants, or because of interaction of
the parental genotype with the backcross.
Trait means for generations are presented based on leaflet type ( Table 4). The cultivars Douglas and Miles indicated differences in plant height expression. No
significant differences for plant height occurred among leaflet types in the F2 and
backcross generations. Therefore plant
Table 3. Analyses of variance for traits in backcross generations to Douglas (upper portion) and to
Miles (bottom portion) cultivars in soybean
dfa
Block
Leaflet
Block 3 leaflet
Error
CV (%)b
Block
Leaflet
Block 3 leaflet
Error
CV (%)
9
1
9
22
9
1
9
35
Plant
height
Plant
biomass
Seed
weight
Seeds
per pod
Pods per
plant
Plant
yield
Harvest
index
105.1
221.2
105.4
44.7
10.2
84.1
0.4
53.4
79.9
13.1
3529
412
2988
4276
30.8
1353
44
1794
3299
31.5
1.18
1.44
0.38
2.64
11.5
1.59
1.88
0.72
2.27
11.7
0.04013
0.00150
0.02566
0.04647
9.2
0.07332
0.22807*
0.05082
0.04344
8.6
4286
475
1358
4217
23.0
2745
14
2412
5486
28.8
893
214
283
958
32.5
337
46
201
774
34.8
0.00365
0.00081
0.00092
0.00122
8.1
0.00206
0.00277
0.00292
0.00291
7.8
Degrees of freedom.
Coefficient of variance.
* Significant at the 0.05 probability level.
a
b
height and leaflet type appear to have segregated independently in the F2 generation. Heterosis for plant height was reported by Lewers et al. (1998), but no
expression for increased plant height was
observed for intermediate leaflet plants in
our study. Plant biomass differed among
leaflet types in the F2 generation. Intermediate leaflet F2 plants produced significantly more biomass than either narrow
or ovate leaflet plants. Results suggested
that greater plant biomass development
was associated with the gene for leaflet
shape in a heterozygous genotype (intermediate phenotype).
In the F2 generation, narrow leaflet F2
plants had smaller seed weight than either
intermediate or ovate leaflet types ( Table
4). Narrow leaflet plants had higher numbers of seeds per pod than intermediate
and ovate leaflet types in the F2 generation
and intermediate leaflet type plants in the
backcross to Miles. The narrow leaflet allele in the homozygous condition has
been reported to have a pleiotropic effect
on the number of seeds per pod ( Hartwig
and Edwards 1970; Jain and Singh 1978;
Mandl and Buss 1981). The results of this
study confirm previously reported results
regarding such a pleiotropic effect.
In the F2 generation, intermediate leaflet
plants produced a significantly higher
number of pods per plant than narrow or
ovate leaflet plants. Results suggest an association between the narrow leaflet gene
in the heterozygous condition and higher
number of pods per plant as an expression
of heterosis. These results of heterosis for
yield accompanied by increased pod number are consistent with previous reports
(Gadag and Upadhyaya 1995; Gizlice et al.
1993; Ma et al. 1983; Sun et al. 1999).
For plant yield in the F2 generation, intermediate leaflet plants produced significantly more plant yield than either narrow
or ovate leaflet plants ( Table 4). In the F2
generation, plant yield of intermediate leaflet plants was 12% and 19% more than
ovate and narrow leaf plants, respectively.
Yield levels of intermediate leaflet F1
plants was comparable to intermediate
leaflet F2 plants.
Much of the plant yield increase for intermediate leaflet plants relative to narrow
or ovate leaflet plants could be attributed
to pods per plant. Even though plants with
narrow leaflets produced smaller seed
weight and more seeds per pod than
plants with intermediate or normal leaflets, such differential expression for these
two yield components was not accompanied by increased plant yield. Results of
Dinkins et al • Narrow Leaflet Gene in Soybean 349
Table 4. Trait means within leaflet type for generations in crosses with soybean cultivars Douglas and
Miles
Generation
Douglas
Miles
F1
F2
Douglas 3 F1
Miles 3 F1
a
Leaflet
type
Plant
height
(cm)
Plant
biomass
(g)
Seed
weight
(g)
Pods
Seeds per per
pod
plant
Plant
yield
(g)
Harvest
index
Ovate
Narrow
Intermediate
Narrow
Intermediate
Ovate
Intermediate
Ovate
Narrow
Intermediate
57.8
75.5
67.1
68.0aa
68.7a
67.8a
72.1
62.9
70.0
66.3
188.5
181.7
211.3
182.3b
220.7a
196.8b
223.3
214.4
184.0
185.9
14.1
12.4
14.2
13.1b
14.1a
14.1a
14.3
14.1
12.6
13.4
2.32
2.44
2.35
2.43a
2.34b
2.31b
2.35
2.33
2.47a
2.34b
81.2
76.3
93.6
80.5b
96.2a
85.6b
98.9
92.2
81.4
80.1
0.4308
0.4173
0.4429
0.4343a
0.4350a
0.4304a
0.4406
0.4297
0.4460
0.4262
249
248
278
250b
292a
262b
289
277
261
258
Values for leaflet types for each trait within a generation unlettered or followed by the same letter are not significantly different at the 0.05 probability level using least square differences.
our study indicate heterosis for plant yield
to be the result of an increase in the number of pods per plant rather than increased seeds per pod or seed weight. Intermediate leaflet plants producing more
pods per plant than either narrow of ovate
leaflet plants may not occur using increased plant densities. Unanswered questions remain: How would plant response
change over various plant densities? How
would plant response affect yield and
yield components?
In the F2 generation, harvest index was
very similar among leaflet types ( Table 4).
This trait was measured at harvest after
plants had dropped leaves. Leaves were
not recovered and thus were not included
in plant weight. Differences among leaflet
types in the F2 generation occurred for
both components of the harvest index—
plant biomass and seed yield. Since intermediate leaflet type plants were highest
compared to narrow and ovate leaflet
plants for both traits, the effect was cancelled in the ratio.
Since all genes except the leaflet type
gene were assumed to be segregating at
random, no differences except those that
were associated with the leaflet gene
would be expected. However, the possibility of genes closely linked to the leaflet
type gene cannot be ruled out completely.
Such genes could exert effects on the measured traits. Traits would be those other
than seeds per pod due to pleiotropic effect of the narrow leaflet allele. In such an
event, leaflet width may represent a usable marker, as originally described by Sax
(1923). Molecular techniques could also
be used to further enhance marker-assisted selection in the chromosomal region,
including the leaflet type gene.
To summarize, the system developed in
our study to classify plants as narrow, intermediate, or ovate leaflet types was suc-
350 The Journal of Heredity 2002:93(5)
cessful. Intermediate leaflet plants expressed superior performance for plant
yield compared to either narrow or ovate
leaflet plants in the F2 generation. Increased plant yield of intermediate leaflet
plants compared to narrow and ovate leaflet plants was largely attributable to an increase in the number of pods per plant as
a yield component. The results of our
study indicate that yield heterosis for intermediate leaflet plants compared to narrow or ovate leaflet plants was expressed
through increased efficiency in partitioning increased plant biomass into seeds filling more pods. For ovate and narrow leaflet plants, an apparent compensatory
effect occurred between the yield components of number of seeds per pod and
seed weight. Similar numbers of pods per
plant and resultant plant yield were expressed for narrow and ovate leaflet type
plants. Plant yield of intermediate leaflet
F2 plants and F1 plants was quite similar.
An interesting prospect would be to evaluate additional generations to determine
if intermediate leaflet plants continue to
produce higher yield than ovate or narrow
leaflet plants. Also, additional crosses
should be made using different parental
sources of narrow and ovate leaflet genes.
Such crosses could be used to determine
if similar results are obtained or if results
of this study are a consequence of specific
interactions between the parents used. If
heterosis for yield is expressed in a diverse array of crosses between narrow
and ovate leaflet parents, such heterosis
could be utilized for soybean yield improvement with commercial hybrid development.
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Received January 2, 2002
Accepted June 26, 2002
Corresponding Editor: Reid G. Palmer
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