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Euphytica (2013) 191:223230

DOI 10.1007/s10681-012-0784-z

Best linear unbiased prediction of triticale hybrid


performance
Manje Gowda Yusheng Zhao
Hans Peter Maurer Elmar A. Weissmann
Tobias Wurschum Jochen C. Reif

Received: 26 March 2012 / Accepted: 20 August 2012 / Published online: 1 September 2012
Springer Science+Business Media B.V. 2012

Abstract Predicting single-cross performance is of


special interest in hybrid breeding of triticale. We used
molecular and phenotypic data of factorial triticale
crosses and compared several approaches to predict
their single-cross performance. Twenty-three inbred
lines and their 76 incomplete factorial crosses were
field evaluated for grain yield, plant height, and
heading time at five locations in Central Europe. In
addition, the parental lines were genotyped with 52
SSR markers. Plant height and heading time were
predicted with high accuracy based on mid-parent
performance. In contrast, prediction of hybrid performance based on mid-parent value was not accurate for
grain yield. Using general combining ability effects
led to an enhanced prediction accuracy of hybrid grain
yield performance. This accuracy could be slightly
improved using best linear unbiased prediction
approaches. The prediction accuracy was considerably
high even if the number of tested hybrids was small.
Electronic supplementary material The online version of
this article (doi:10.1007/s10681-012-0784-z) contains
supplementary material, which is available to authorized users.
M. Gowda  Y. Zhao  H. P. Maurer  T. Wurschum 
J. C. Reif (&)
State Plant Breeding Institute, University of Hohenheim,
70599 Stuttgart, Germany
e-mail: jochreif@uni-hohenheim.de
E. A. Weissmann
Saatzucht Dr. Hege GbR, Hohebuch 1, 74638
Waldenburg, Germany

Consequently, best linear unbiased prediction of


hybrid performance is a promising tool for hybrid
triticale breeding programs.
Keywords Best linear unbiased prediction  General
combining ability  Hybrid performance  Specific
combining ability  Triticale

Introduction
Hybrid breeding was suggested as promising approach
to increase grain yield performance in triticale (X
Triticosecale Wittmack) (Oettler et al. 2003, 2005;
Fischer et al. 2010). Requirements to conduct hybrid
breeding in triticale such as the availability of a
cytoplasmic male sterility (CMS) system are fulfilled
and first commercial hybrids have been released in
France and Germany (www.hybrid-triticale.de). Nevertheless, hybrid breeding in triticale is still hampered
by the time- and resource-demanding production and
phenotypic evaluation of the large number of singlecross combinations. Consequently, there is a strong
demand for methods to predict performance of triticale
hybrids with high accuracy.
For qualitative traits, prediction of single-cross
performance based on mid-parent values is very
accurate (Oettler et al. 2005). For complex traits such
as grain yield, however, accuracy is too low to be of

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224

Euphytica (2013) 191:223230

predictive value (Fischer et al. 2010). Promising


parental lines can alternatively be identified applying
the concept of general (GCA) and specific combining
ability (SCA, Hallauer et al. 1988). Selecting promising triticale hybrids based on GCA effects of their
parents, possesses a moderate to high accuracy as
reflected by a predominance of r2GCA over r2SCA
(Fischer et al. 2009, 2010). Nevertheless, presence of a
significant proportion of r2SCA still limits the accuracy
to predict triticale hybrid performance.
Best linear unbiased prediction (BLUP, Henderson
1985) is a potential strategy to predict the single-cross
performance. BLUP based hybrid prediction exploits
the relatedness between tested and untested hybrids to
estimate the single-cross performance (Bernardo
2002). Thereby, relatedness can be determined using
pedigree records or even more precisely based on
molecular markers. Experimental data in maize (Bernardo 1994, 1996; Charcosset et al. 1998), soybean
(Panter and Allen 1995), rice (Xu and Virmani 2000),
and sunflower (Reif et al. 2012) suggests that the
BLUP approach can be successfully applied to predict
single-cross performance of untested hybrids. Despite
these promising results, the BLUP approach has not
yet been applied and evaluated in small grain cereals
hybrid breeding programs.
We used molecular and phenotypic data of factorial
crosses gathered in our triticale hybrid breeding program and compared several approaches to predict the
single-cross performance. In particular, the objectives of
our study were to (1) investigate the efficiency of the
prediction of hybrid performance based on mid-parent
value as well as GCA effects and (2) assess the potential
of BLUP based prediction of single-cross performance
in triticale using different cross validation strategies.

in Switzerland in 2010. The experimental design was an


11 9 10 a-lattice with two replications at each location.
The seeding rate was 280 seeds per m2 for both hybrids
and parental lines. The plot size ranged from 5.0 to
7.0 m2. Harvesting was performed with a mechanical
harvester and data on grain yield (Mg ha-1 adjusted to
140 g kg-1 moisture), plant height (cm), and heading
time were recorded. Heading time was recorded as the
developmental stage (BBCH, Hack et al. 1992) at the
time when ears of approximately half of the genotypes
were fully visible. Recording heading time was severely
affected in one location therefore heading time data was
analyzed based on only four locations.

Materials and methods

Combined analyses of variance were performed with


the data from each of the five different locations.
Dummy variables were used to separate genotypes
into parental lines, hybrids, and checks. The phenotypic data of the parental inbred lines and hybrids were
analyzed based on following linear model:

Plant materials and field trials


A set of 18 female CMS lines were crossed in an
incomplete factorial mating design with 5 male restorer
lines (Supplementary Figure S1). The female and male
lines are adapted to Central Europe and were selected
based on divergent heading time and plant height to
promote cross pollination. The 76 hybrids were evaluated with their 23 parental lines and 11 commercial
varieties at four locations in Germany and one location

123

Molecular analyses
Genomic DNA of all 23 parental lines was extracted
by using the modified CTAB method (Doyle and
Doyle 1990) and screened with 52 polymorphic SSR
markers distributed throughout the genome following
the protocol described by Tams et al. (2004). The
molecular data was used to estimate the coefficient of
coancestry hij between inbreds i and j as outlined by
Bernardo (2002) with the exception that we assumed a
base-line identical by descent probability equal to the
minimum simple matching coefficient among pairs of
lines observed in our data set. In addition, we applied
principal coordinate analysis (Gower 1966) based on
the modified Rogers distances among pairs of inbred
lines (Wright 1978). Molecular marker analyses were
carried out by using the software Plabsoft (Maurer
et al. 2008) which is linked to the R environment
(R development core team 2010).
Field data analysis and predicting hybrid
performance

yijkno l lk cij pij g0i g00j sij


clijk plijk g0 lik g00 ljk slijk rnk
bonk eijkno
where yijkno was the phenotypic performance of the ijth

Euphytica (2013) 191:223230

entry (check i = j; line i = j, or hybrid i = j) at the


kth location of the nth replicate in the oth incomplete
block, l was an intercept term, lk was the effect of the
kth location, cij and pij, were the genetic effect of the
check and parental line, respectively, g0 i was the GCA
effect of the ith female line, g00 j was the GCA effect of
the jth male line, sij was the SCA effect of crosses
between lines i and j, (cl)ijk was the interaction effect
of ijth check with kth location, (pl)ijk was the
interaction effect of the ijth parental line and the kth
location, (g0 l)ik and (g00 l)jk, were GCA 9 location
effects of female and male lines, and (sl)ijk was
SCA 9 location interaction effects, rnk was the effect
of the nth replicate at the kth location, bonk was the
effect of the oth incomplete block of the nth replicate
at the kth location, and eijkno was the residual. Except
replications, checks, and check by location interactions, all other effects were treated as random.
The variance of the random genetic parental line
effects was assumed to be Var(pi) = 2Hr2G, where
r2G refers to the genetic variance of the lines estimated
by REML and H was a 23 9 23 matrix of coefficients
of coancestries that define the degree of genetic
covariance between all pairs of lines.
The variance of the g0 and g00 effects was assumed to
be Var(g0 ) = H0 r2GCA-F and Var(g00 ) = H00 r2GCA-M,
where r2GCA-F and r2GCA-M refer to the variance of
GCA effects estimated by REML for the female and
male lines, respectively. H0 was 18 9 18 and H00 was a
5 9 5 matrix of coefficients of coancestries that define
the degree of genetic covariance between all pairs of
female and male lines, respectively. H0 and H00 were
estimated as outlined above. The variance of the
random effects s was assumed to be Var(s) = Dr2SCA,
where r2SCA refers to the variance of SCA effects
estimated by REML. D was a 76 9 76 matrix defining
the probability that both alleles at a locus are identical
by descent (for details see Reif et al. 2012). All
variance components were determined by the REML
method implemented in the software ASReml (Gilmour et al. 2009). Significance of the variance
component estimates was tested by model comparison
with likelihood ratio tests (Stram and Lee
1994).Hybrid performance was estimated as:
yij l g^i g^j s^ij
where yij was the phenotypic performance of the
hybrid between parental lines i and j, l was an overall
mean, gi was the GCA effect of the ith female line,

225

gj was the GCA effect of the jth male line, sij was the
SCA effect of crosses between lines i and j.
Mid-parent heterosis was calculated as the difference between the performance of a hybrid and the
mean performance of its two parental inbred lines.
Rogers genetic distances (Rogers 1972) were estimated among all pairs of parental inbred lines. Pearson
product moment correlations (r) between Rogers
distances and heterosis were calculated. Significance
tests for correlations were performed using the Mantel
test (Mantel 1967).
Prediction of hybrid performance
Performance of untested hybrids (yU) was predicted
based on the GCA effects of their parents i and j as:
yU l g^i g^j
The performance of hybrids were also predicted by
using the information from the inverse of the variancecovariance of the tested hybrids (C-1
TT ) and the
covariance among untested and tested hybrids (CUT)
as: (Bernardo 2002)
1
yU CUT CTT
y^T

The elements of CUT between hybrids with male a and


female b and another hybrid with male c and female
d have been determined as {r2GCA-Mhac ? r2GCA2
Fhbd ? r SCA (hac hbd ? had hbc)/2}. The off-diagonal
elements of CTT were also estimated as elements of CUT.
The diagonal elements of CTT were calculated as {r2GCA2
2
2
2
M ? r GCA-F ? r SCA ? r e}, where r e is the variance
of the residual errors. In addition to the above outlined
method where covariance of both GCA and SCA were
considered (BLUP-GCA/SCA), we evaluated another
approach by ignoring covariance of SCA effects i.e.,
BLUP-GCA.
Evaluating the prediction methods for hybrid
performance
The accuracy of the above outlined prediction
approaches were evaluated by five-fold cross validations as described in detail by Zhao et al. (2012). Briefly,
the full data set was split into five parts. Four of those
were used as training data of tested hybrids and the
performance of the remaining 20 % of the hybrids were
predicted using the different approaches described

123

Results
We observed on average 3.1 alleles per SSR locus with a
minimum of two and a maximum of six alleles. The first
two principal coordinates together explained 22.1 % of
the total genotypic variation. Male lines tended to
cluster together but were not separated from the female
lines (Fig. 1). This was further supported by coancestry
coefficients among male (mean h = 0.49) and female
lines (mean h = 0.55), which were of comparable
magnitude than coancestry coefficients among male
times female lines (mean h = 0.52) (Fig. 2).
The genotypic variances of the parents were
significantly larger than zero (P \ 0.01) for all three
evaluated traits (Table 1). The magnitude of genotypic
variance was higher for the hybrids than for the parents
for all three traits. The estimates of r2GCA-F were
significantly different from zero (P \ 0.05) for all
three traits, whereas estimates of r2GCA-M were only
significantly different from zero for plant height and
heading time. Estimates of r2SCA were significantly
larger than zero for grain yield and plant height. The
r2GCA was predominant over r2SCA for plant height
and heading time. In contrast, for grain yield, the
magnitude of r2SCA was slightly higher than r2GCA.
Heritability was almost similar for hybrids and
parental lines with values above 0.89.
The contrast of hybrids versus parental lines was
significantly different from zero (P \ 0.01) for
grain yield but not for plant height and heading time.
Mid-parent heterosis for grain yield ranged from

123

0.1
0.0
0.3 0.2 0.1

PC2 (10.5%)

0.2

Female lines
Male lines

0.3

0.2

0.1

0.0

0.1

0.2

0.3

PC1 (11.6%)
Fig. 1 Principal coordinate analyses of 23 triticale inbred lines
based on modified Rogers distances estimated using 52 SSR
markers. Values in parentheses refer to the proportion of
variance explained by the principal coordinates
8
Female lines
Male lines
Female x male lines

7
6
5

Density

above. Then the correlation between predicted and


observed genotypic values of the 20 % remaining
untested hybrids was calculated. The correlation was
divided by the square root of the heritability to
determine the accuracy (Dekkers 2007). Through the
division by the square root of heritability values above
one are possible and as default we set those values to
one. Moreover, we evaluated the BLUP based hybrid
prediction approaches based on leave-one-parent-out
cross validation by calculating the correlation between
predicted and observed genotypic values divided by the
square root of the heritability. We also investigated the
influence of the population size on the prediction
accuracy and sampled an increasing number of tested
hybrids (P = 15, 25, 35, 45, 55, and 65). The sampling of
training and validation set was repeated for 1,000 times.

Euphytica (2013) 191:223230

0.3

226

4
3
2
1
0
0.0

0.2

0.4

0.6

0.8

1.0

Coefficient of coancestry
Fig. 2 Histogram of coancestry coefficients estimated based on
marker data among the 18 female lines, the 5 male lines, and
among the male and female lines

-21.1 to 21.5 % (absolute values from -1.6 to


1.6 Mg ha-1) (Supplementary Figure S2). The association between mid-parent and hybrid performance
was not significant for grain yield (r = 0.28) but was
highly significant for plant height and heading time
(Table 2). Per se performance of inbred parents and
GCA effects were weakly associated (r = 0.14) for

Euphytica (2013) 191:223230

227

Table 1 Means and ranges of inbred and hybrid performance,


and estimates of variance components for inbred lines
(r2G = genotypic; r2G9L = genotype 9 environment interaction; r2e = pooled error) and hybrids (r2GCA-M = variance of
general combining ability effects of males; r2GCA-F = variance

of general combining ability effects of females; r2SCA = variance of specific combining ability effects; r2GCA-M9L, r2GCA2
F9L, and r SCA9L refer to variance of interactions with
environments), and heritability estimates (H2) evaluated for
grain yield, plant height, and heading time

Grain yield (Mg ha-1)

Plant height (cm)

Mean

7.19

110

58.8

Min
Max

5.82
8.86

91
126

57.5
59.7

r2G

0.59**

167.12**

4.49**

Source

Heading time (EC-stage)

Parents

0.21**

6.80**

1.82**

r2ae

0.24

10.03

0.68

H2

0.90

0.98

0.91

Mean

7.84

113

58.9

Min

5.91

87

56.1

Max

G9L

F1 hybrids

8.94

133

61.0

r2GCA-F

0.27*

111.82***

0.96***

r2GCA-M

0.13

149.32***

4. 83***

r2SCA

0.47***

13.94***

0.09*

r2GCA-F9L

0.07***

2.62***

0.18***

r2GCA-M9L

0.10***

9.05***

1.56***

r2SCA9L
H2

0.07***
0.92

1.01
0.97

0.09**
0.91

r2SCA/(r2GCA-M ? r2GCA-F ? r2SCA)

0.54

0.05

0.01

* ** *** Significantly different from zero at the 0.05, 0.01 and 0.001 level of probability, respectively
a

we assumed that parents and F1 hybrids have the same error variance

grain yield but the correlation was highly significant


for plant height and heading time. For all three traits,
genetic distance was only weakly associated with
hybrid performance.
Five-fold cross validation for GCA prediction and
both BLUP based prediction (BLUP-GCA and BLUPGCA/SCA) revealed high accuracies to predict hybrid
performance for all three traits (Table 3). Leave-oneparent-out cross validations resulted in lower prediction accuracies than five-fold cross validation. Among
the different combinations of number of tested hybrids
in the training population, the pooled correlation
between predicted and observed hybrid performance
ranged from 0.45 to 0.68 for grain yield (Fig. 3). With
33 % of tested hybrids we observed a prediction
accuracy of 0.56, which corresponds to 82 % of the
total accuracy explained by the full data set.

Discussion
Intensive research on hybrid breeding in triticale was
started two decades ago and the first hybrid Hybridel
based on chemical hybridizing agent was released in
1999 and the first CMS based commercial hybrid
HYT Prime was officially released in 2010 (Longin
et al. 2012). Hybrid breeding in triticale is very
resource demanding, as the GCA test for the females
requires introgression of the lines into CMS background. Consequently, methods to pre-select promising single-cross hybrids are central to enhance the
efficiency of hybrid breeding. This stimulated us to use
a data set generated in the hybrid triticale breeding
program of the State Plant Breeding Institute of the
University of Hohenheim to compare the accuracies of
different hybrid prediction approaches.

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Euphytica (2013) 191:223230

Table 2 Pearson product moment correlations (r) between


hybrid (HP) and mid-parent performance (MP), between
Rogers distances (RD) and mid-parent heterosis (MPH), and
Grain yield

between general combining ability effects and per se performance for grain yield, plant height and heading time for 76
hybrids evaluated in multi-location field trials
Plant height

Heading time

r(Per se; GCA)

0.14

0.90**

0.77**

r(MP; HP)

0.28

0.88**

0.81**

r(RD; MPH)

-0.29

-0.17

-0.18

** Significantly different from zero at 0.01 level of probability

Table 3 Accuracy (rG) of predicted hybrid performance (HP) for three traits determined by five-fold cross validation and leave-oneparent-out cross validation
Grain yield

Plant height

Heading time

0.57

0.95

1.00*

Five-fold CV
r(GCA; HP)
r(BLUP-GCA; HP)

0.69

0.96

1.00*

r(BLUP-GCA/SCA; HP)

0.68

0.96

1.00*

Leave-one-male-out CV
r(BLUP-GCA; HP)

0.61

0.65

0.36

r(BLUP-GCA/SCA; HP)

0.55

0.64

0.36

Leave-one-female-out CV
r(BLUP-GCA; HP)

0.56

0.77

0.99

r(BLUP-GCA/SCA; HP)

0.54

0.77

0.99

* Prediction accuracy values C1 were set to 1


HP was predicted based on (1) general combining ability effects (GCA), (2) best linear unbiased prediction using covariance due to
GCA effects (BLUP-GCA), and (3) best linear unbiased prediction using covariance due to GCA and specific combining ability
(SCA) effects (BLUP-GCA/SCA)

Estimating hybrid performance through its


decomposition into mid-parent performance
and heterosis

1.0
0.9
0.8

Accuracy

0.7
0.6
0.5
0.4
0.3
0.2
0.1
0.0
0

15

25

35

45

55

65

Training population size


Fig. 3 Dependency of prediction accuracy of hybrid performance for grain yield on the size of the training population

123

For complex traits such as grain yield, the correlation


between mean performance of parental inbred lines
and their hybrid performance is expected to be low due
to masking dominance effects (Hallauer and Miranda
1988). In line with this expectation, we observed a
poor prediction accuracy of hybrid performance based
on mid-parent values for grain yield (r = 0.28) and
considerably higher accuracies for the less complex
traits heading time (r = 0.81, P \ 0.01) and plant
height (r = 0.88, P \ 0.01) (Table 2).
We tried to improve the prediction accuracy for
grain yield based on mid-parent performance by
predicting heterosis using Rogers distances. The
panel of lines are at least weakly related by pedigree

Euphytica (2013) 191:223230

and, hence, a positive association between Rogers


distances and heterosis is expected (Melchinger 1999).
In contrast to this, we observed no significant association between Rogers distances and heterosis
(Table 2). This is in agreement with a previous survey
of Central European triticale lines reporting absence of
an association between Rogers distances and heterosis (Tams et al. 2006). Our findings may be explained
by the presence of additive 9 additive epistasis,
which could significantly influence the heterosis for
self-pollinating species (e.g., Garcia et al. 2008; Reif
et al. 2009).

Hybrid prediction with general combining ability


effects
For plant height and heading time, r2GCA was more
pronounced compared to r2SCA resulting in high
prediction accuracies of hybrid performance based
on GCA effects (Table 3). In contrast, for grain yield
the association between GCA and hybrid performance
was moderate with prediction accuracy of 0.57. This
moderate accuracy can be explained by the presence of
significant r2SCA . The r2SCA :r2GCA ratio observed in our
survey for grain yield was slightly higher than values
reported previously for triticale (Barker and Varughese 1992; Oettler et al. 2003; Fischer et al. 2009,
2010). Conducting inter-population improvement in
triticale with a clearly defined two-pool concept
possesses the potential to lead to a more favorable
r2SCA :r2GCA ratio on a long term (Reif et al. 2007).
Best linear unbiased prediction of hybrid
performance
In case that GCA values are available, prediction
accuracy based on GCA effects can be considered as
the base-line, which a novel approach should top to
become relevant. For plant height and heading time,
we observed no significant improvement in prediction
accuracy using best linear unbiased prediction compared to GCA effects (Table 3). In contrast, for grain
yield, we observed a slight improvement of best linear
unbiased prediction compared to GCA based prediction. This indicates that at least for complex traits such
as grain yield, best linear unbiased prediction is a
valuable approach for reliable hybrid prediction.

229

We investigated the influence of the size of the


training population on the prediction accuracy by
applying a resampling strategy and observed that even
with a low number of individuals we can predict the
performance of the remaining hybrids with substantial
accuracy (Fig. 3). Our results support previous studies
on best linear unbiased prediction of hybrid performance in maize (Bernardo 1994, 1996; Charcosset et al.
1998). This finding suggests that BLUP based methods
yield consistently high prediction accuracy even with
small numbers of tested hybrids.
We compared two best linear unbiased prediction
approaches using relatedness arising due to GCA
and SCA effects or exploiting only relatedness
arising due to GCA effects. The exploitation of
relatedness due to SCA in addition to GCA did not
yield in significantly improved prediction accuracies
for all three traits (Table 3). This is in accordance
with earlier studies in maize (Bernardo 1994), and
sunflower (Reif et al. 2012) and can be explained by
an increased complexity predicting interaction compared to main effects.
For hybrid triticale breeding, many lines are
available at every cycle of selection for instance from
line breeding programs. For these lines, however, no
information on their GCA effects is available. We
mimic this situation and applied a leave-one parentout cross validation strategy. We observed a decrease
in prediction accuracy but values were still above 0.53
for grain yield (Table 3). If we consider in addition
that production of seeds for GCA tests of new female
lines requires time- and resource demanding backcrossing into sterile cytoplasm, then it is apparent that
best linear unbiased prediction is an approach of high
value in applied hybrid triticale breeding programs.
Acknowledgments Y. Zhao and M. Gowda were supported by
BMBF within the HYWHEAT Project (Grant ID: FKZ0315945D).

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