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Phil. Trans. R. Soc. B (2012) 367, 1580–1588
doi:10.1098/rstb.2011.0242
Research
Can we improve heterosis for root growth of
maize by selecting parental inbred lines
with different temperature behaviour?
Andreas Hund*, Regina Reimer, Peter Stamp and Achim Walter
Institute of Agricultural Sciences, ETH Zurich, 8092 Zurich, Switzerland
Tolerance to high and low temperature is an important breeding aim for Central and Northern
Europe, where temperature fluctuations are predicted to increase. However, the extent to which
genotypes differ in their response to the whole range of possible temperatures is not well understood. We tested the hypothesis that the combination of maize (Zea mays L.) inbred lines with
differing temperature optima for root growth would lead to superior hybrids. This hypothesis is
based on the concept of ‘marginal overdominance’ in which the hybrid expresses higher relative fitness than its parents, summed over all situations. The elongation rates of axile and lateral roots of
the reciprocal cross between two flint and two dent inbred lines were assessed at temperatures
between 158C and 408C. Indeed, the cross between UH005 and UH250 with lateral root growth
temperature optima at 348C and 288C, respectively, resulted in intermediate hybrids. At temperatures below and above 318C, the hybrids’ root growth was comparable to the better parent,
respectively, thereby increasing temperature tolerance of the hybrid compared with its parents.
The implications of and reasons for this heterosis effect are discussed in the context of breeding
for abiotic stress tolerance and of putatively underlying molecular mechanisms. This finding
paves the way for more detailed investigations of this phenomenon in future studies.
Keywords: flint; dent; corn; marginal overdominance; root; abiotic stress
1. INTRODUCTION
Maize is a chilling-sensitive species of tropical origin,
with severely hampered development at atmospheric
temperatures below 158C. In agricultural history,
the so-called flint types of maize adapted to higher latitudes, first as the result of selection by native American
farmers, later by European farmers [1] and in the past
century by modern plant breeders. North of the Alps,
maize formerly grew only in the warmer areas such as
the alpine foehn valleys [2]. Today, maize is cultivated
as far north as southern Scandinavia [3,4]. At least
part of this success was achieved by lowering the temperature limit at which maize can still grow [4]. As a side
effect, such lines are likely to suffer from heat sensitivity
[4]. However, according to climate models for Europe
[5], future crops will have to cope with an even greater
variability of high and low temperatures throughout
the season [6]. It is therefore advisable to select genotypes that are capable of tolerating a wide range of
temperature conditions.
Shoot growth and yield strongly depend on the
performance of the root system [7]. In maize, it is well
known that root zone temperature strongly affects leaf
* Author for correspondence ([email protected]).
Electronic supplementary material is available at http://dx.doi.org/
10.1098/rstb.2011.0242 or via http://rstb.royalsocietypublishing.org.
One contribution of 18 to a Theme Issue ‘Root growth and
branching’.
growth and shoot biomass [8,9], mediated by pronounced alterations in shoot metabolism [10] and shortterm growth dynamics [11]. Low root zone temperatures
induce decreased root growth and this in turn hampers
shoot development by altered water relations [12,13]
and carbohydrate metabolism [11]. Because root zone
temperatures are modulated not only throughout the
season, but also throughout day–night cycles in topsoil
regions, the question as to how intensely root growth is
hampered by sub- or supra-optimal temperatures is
highly relevant also in the context of the overall development of the shoot, which is a main trait of plant breeding.
Plant breeders usually develop hybrids to benefit
from heterosis. Heterosis is defined as the superior
performance of an F1 hybrid compared with the average performance of the distinct homozygous inbred
parents. The phenomenon of heterosis has been
described not only for shoot traits and yield, but also
for root traits of maize [14] and wheat [15,16]. To
benefit from heterosis, breeders combine the so-called
heterotic groups. Inbred lines are kept and selected
separately within these groups. For the cool climate of
Central and Northern Europe, the Northern Flints
and the Corn Belt Dents are the basis for hybrid crosses
[17]. The flint lines are adapted to a cool temperate
climate, contributing to chilling tolerance, while the
warm-temperate-adapted dent lines contributed to a
high-yield potential [4,18].
The success of the flint – dent combination in the
cool regions of Europe raises the question of whether
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Temperature-dependent heterosis A. Hund et al.
the combination of different temperature optima of
these groups partially explain heterosis. It is well established that plants of different geographical origin [19],
as well as cultivars of one and the same species that are
adapted to different regions [4,20,21], possess different
temperature optima. However, for roots, detailed information about their temperature optima is lacking.
A few studies investigating the relation of root growth
parameters in different genotypes to temperature have
focused either on high or low temperature stress
[22,23], not taking into account the dynamic response
across a wider range of temperatures and not investigating specific responses of different traits of the root
system (e.g. lateral versus axile roots). Although it is
likely that genotypes differ with respect to their response
of root growth to a range of temperatures, it has not
been tested yet (i) whether clear-cut distributions of
growth response towards differing temperatures exist
and (ii) whether such differences could be used to increase
temperature-dependent heterosis. Mc William & Griffing
[24] studied temperature-dependent heterosis of shoot
growth of maize. In their study, the largest heterosis
effect was found at temperature extremes, i.e. below a
day temperature of 218C and above a day temperature
of 338C. However, their study did not involve genotypes
with different temperature optima.
There are several potential explanations for how
temperature response of plants might be controlled
mechanistically. For example, temperature may act
via networks governed by thermodynamic laws (e.g.
rise and decline of various enzyme activities from suboptimal via optimal to supraoptimal temperatures).
Most likely, subordinate metabolic processes would
be controlled by key enzymes. Rubisco activase is a
candidate for such a key enzyme controlling the temperature response of photosynthesis [25]. There, the
temperature response of rubisco activase determines
photosynthesis response to an extent that it may even
set boundaries to the geographical distribution of
different plant species [25]. However, Parent et al.
[26] found that the temperature response of photosynthesis does not follow the same function as growth
processes. Alternative to thermodynamic dependencies, other molecular control processes exist. For
example, heat stress transcription factors and other
pathways mediated by abscisic acid, salicylic acid,
hydroxgen peroxide and ethylene induce heat acclimation (for review, see [27]). It is still unclear which
enzymes or pathways would be the major factors governing the response of root growth to temperature in
breeding material of maize. The mapping of quantitative trait loci (QTLs) is a straightforward approach to
identifying genomic regions controlling root growth
[28] and their response to temperature [29]. The protocol developed here may be used for selection or QTL
mapping in order to (i) identify genomic regions
controlling the response to temperature and (ii) to elucidate whether such regions are involved in temperaturedependent heterosis. Heterosis in a modern context can
be explained as ‘quantitative genetic frameworks involving interactions in hierarchical networks’ [30]. Allele
expression studies suggest that the two parental alleles
of a hybrid can be regulated differentially in response
to environmental stress [31]. This observation supports
Phil. Trans. R. Soc. B (2012)
1581
the concept of marginal overdominance where
‘Multiplied through all situations—temporal, spatial or
developmental—the heterozygote emerges with the
highest relative fitness’ [32]. Thus, if the heterozygous
individual follows the better parent under all environmental conditions, it outperforms its parents summed
across these conditions.
On the basis of this concept, we hypothesize that
different temperature responses of parental inbred
lines may lead to marginal overdominance. To test
this hypothesis, a Gaussian function will be used as
the mathematical baseline model describing the
relation between observed root growth rates and temperatures to which the roots are exposed. Such peak
functions are widely used to model the temperature
response of plant productivity (for review, see [33]).
The assumption of a symmetrical, Gaussian function
is justified by findings reported for root growth in
potatoes [19] and it fits well to many parameters of
plant performance modulated by temperature
[7,25,33]. The Gaussian model allows estimation for
each genotype of a distinct temperature optimum, a
maximal growth rate at this optimum and a temperature range in which sufficient performance is
maintained. Genotypes may differ with respect to all
three variables. The combination of extreme genotypes
may give rise to hybrids that perform better across the
whole temperature range. This concept can be illustrated by two hypothetical combinations: (i) inbred
lines that differ with respect to temperature optimum
(figure 1a), and (ii) inbred lines that differ with respect
to their temperature range and their maximal growth
at the temperature optimum (figure 1b). In the first
case, the parents contribute both heat and chilling tolerance to the hybrid; in the second case, the parents
contribute tolerance to temperature extremes and the
ability to perform well at optimal temperatures.
Given the earlier mentioned considerations, we
aimed to elucidate (i) whether the temperature behaviour of root growth of maize can be described with a
simple, nonlinear function, such as a Gaussian function, (ii) whether inbred lines or heterotic groups
differ with respect to the parameter estimates of this
function, and (iii) whether the resulting hybrids of
these differing inbred lines follow the performance of
the better parent, i.e. express marginal overdominance
with respect to different traits of root system growth
(lateral versus axile roots).
2. MATERIAL AND METHODS
(a) Plant material and environmental conditions
Two flint inbred lines (UH002 and UH005), two dent
inbred lines (UH250 and UH301) and their reciprocal
hybrids were used. The material was obtained from the
University of Hohenheim, Germany. The seed surface
was sterilized with 2.5 per cent aqueous sodium hypochlorite (NaOCl (aq)) for 15 min and rinsed three
times with water. The seeds were germinated in Petri
dishes on moist germination paper at 278C for 2
days. Germinated seeds were transferred to growth
pouches consisting of blue germination blotting
paper (24 29.5 cm; Anchor Paper, St Paul, MI,
USA) covered by black plastic sheets. The pouches
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A. Hund et al.
Temperature-dependent heterosis
(a)
(b)
Dy
µ P2
µ P1
trait value
Dx
temperature
Figure 1. Schematic of performance profiles of hypothetical homozygous inbred lines (P1 (short dashed lines) and P2 (long
dashed lines)) and their heterozygous F1 (solid lines) hybrid dependent on growth temperature. It is assumed that the trait
value Y decreases symmetrically from its2 maximum value Ymax at the temperature optimum m and that the temperature operating range s can vary: Y ¼ Ymax eðxmÞ =s . Assuming that the alleles of the better parent are always dominant, the F1 always
performs as well as the best parent (solid line). Examples where this leads to marginal overdominance are: both inbred lines
show the same s and Ymax but differ in m by Dx (a), and both inbred lines show the same m but differ for s and Ymax (b).
(a)
(b)
d
axile
b
c
lateral
a
Figure 2. Temperature box (a); root growing on germination paper in a pouch (b). The box is shown with two pouches (a), a
heat exchanger (b) connection to the Julabo heating and cooling device (not shown) and a water pump (c) connected to a hose
with small holes at 2 cm intervals for uniform cooling (d ). The box was insulated by 2 cm Styrofoam. When operating, the box
was closed with a 2 cm Styrofoam lid, leaving only space for the shoots.
were placed in custom-made cooling boxes (figure 2)
allowing root zone temperatures to be set independently
from shoot-zone temperatures. The bottom of the
pouch was submerged in a nutrient solution (0.23%
(v/v) of Wuxal; Aglukon Spezialdünger GmbH, Düsseldorf, Germany). The composition per litre nutrient
solution was 230 mg N, 230 mg P2O5, 173 mg K2O,
437 mg Fe, 373 mg Mn, 235 mg B, 186 mg Cu, 140 mg
Zn, 23 mg Mo. Each box contained a full set of 12
plants, one per genotype. For the first 2 days after the
onset of the experiment, plants were kept at 258C.
After this phase, the temperature in the boxes was set
at either 158C, 168C, 218C, 248C, 288C, 328C, 368C
or 408C. The temperature was measured at the seed
level in the pouch. A pump (figure 2a) distributed the
nutrient solution along the walls of the container to
achieve more uniform temperatures within the box.
The root zone temperature was set to the desired temperature by a heat or cold exchanger (Julabo Labortechnik
GmbH, Seelbach, Germany). The boxes were placed in
a growth chamber (E16; Conviron, Winnipeg, Canada)
Phil. Trans. R. Soc. B (2012)
set at 258C shoot-zone temperature, photosynthetic
active radiation of 300 mmol m22 s21 and relative
humidity of 75 per cent.
(b) Experimental design
The experimental design was a split plot experiment
with two independent replications. Temperature was
the whole plot and genotype the subplot factor. Each
experimental unit consisted of one plant. Thus, each
genotype was tested at eight temperatures allocated to
four independent growth chamber replications. Each
replication harboured four of the eight temperatures.
One of the four replications resulted in an overall poor
plant performance, likely due to malfunction of the
growth chamber, and was discarded from the analysis.
The remaining replications summed up to 12 biological
replications (plants) per genotype in total.
During the treatment phase, the pouches were
scanned daily within a period of 5 days to determine
root elongation rates. The images were acquired using
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Temperature-dependent heterosis A. Hund et al.
a flatbed scanner (HP scanjet 4600 series, ‘see-through’;
Hewlett-Packard Company). Images were processed as
described by Hund et al. [34] to obtain binary images
containing root objects and background. These were
analysed using WinRHIZO 2003b (Regent Instruments, Montreal, Quebec, Canada) to obtain the rootlength in diameter class distribution of the scanned
roots. Objects below a threshold of 0.5 mm were classified as lateral roots; those above this threshold were
considered as axile roots.
(c) Models and statistical treatment
The elongation rate of the axile roots (ERAx) was modelled as linear, and the elongation rate of the lateral
roots (klat) was modelled as exponential as described
in more detail elsewhere [34,35]. The corresponding
models were
9
xðtÞ ¼ xðt0 Þ ER Ax t >
=
and
ð2:1Þ
xðtÞ xðt0 Þ >
;
ER Ax ¼
t
for axile root elongation, where x(t) is the root length
at time t after germination and x(t0) is the root
length at the first scanning day, and
9
xðtÞ ¼ xðt0 Þ eklat t >
=
and
ð2:2Þ
lnðxðtÞ xðt0 ÞÞ >
;
klat ¼
t
for lateral root elongation rate.
The temperature response of each genotype was
modelled using a Gaussian function
Y ¼ Ymax eðxmÞ
2
=s
ð2:3Þ
in which the trait value (Y) is a function of the maximum elongation rate (Ymax) at the temperature
optimum (m) and the temperature operating range
(s). The nonlinear least squares estimated of the
Gaussian function and their 95% CI were computed
using the function nlsList() in R [36]. The model
was fitted as described by Pinheiro & Bates [37,
pp. 338ff.]. To estimate the effect of the heterotic
group used as a mother and of the combining ability,
nonlinear mixed effect models were fitted using the function nlme() in R [36]. In this case, the genotypes were
set as a random factor and the desired contrast was set
as a fixed factor following the procedure described by
Pinheiro & Bates [37, pp. 354ff]. Since there was no
self-starting function available, the starting values were
estimated based on the scatterplots of growth rates
versus temperature of the whole population.
Mid-parent values were calculated to compute
parent– offspring correlations. As a specific form of
mid-parent value (MP), the combination of the
range (R) and temperature shift of the parents (O)
was calculated as
MP ¼
RP1 þ RP2 OP1 OP2
þ
;
2
2
ð2:4Þ
where R is the temperature range of the respective
parent (P1 or P2) and O is its temperature optimum.
This calculation was conducted to take into account
Phil. Trans. R. Soc. B (2012)
1583
that the shift in the temperature optimum of the
parents may affect the temperature range of the
respective hybrids.
3. RESULTS
(a) Differences among genotypes existed for the
maximum elongation of ERAx and klat as well as
for the temperature optimum of klat
Overall, the Gaussian model was well suited to describe
the temperature response of the 12 genotypes (figures 3
and 4). Thus, optimum temperature, temperature
range and maximum elongation rate at optimum temperature (‘maximum elongation’) were extracted from
this model (table 1). Growth of axile roots of all genotypes practically ceased at temperatures of 158C and
408C, respectively, with maximum values being found
between 258C and 308C (figure 3). For lateral roots,
variability of the temperature response for individual
genotypes and variability between genotypes were
higher (figure 3). Owing to poor germination, inbred
line UH250 had five plants only. Accordingly, its
parameter estimates could not be estimated reliably,
resulting in large 95% CI (table 1). Differences between
genotypes with respect to the temperature range and the
temperature optimum were least pronounced for axile
roots (figure 1). Their CI did not overlap (table 1; see
electronic supplementary material, S1 for visualization). However, there was significant variation for the
maximum growth. It ranged from 7.9 cm d21 for
UH005 to 33 cm d21 for UH301, with a population
average of 22 cm d21. For lateral roots, there was a significant variation of the optimum temperature and of
the maximum elongation of klat (table 1; electronic supplementary material, S2). The optimum temperature of
klat ranged from 288C for the cross between UH250 and
UH002 to 348C for UH005 with a population average
of 298C. The maximum klat ranged from 0.47 d21 for
UH005 UH250 to 1.08 d21 for UH250 UH002
with a population average of 0.77 d21. There was
neither a tendency for increased chilling tolerance
of the flint group nor for increased heat tolerance of
the dent group. Contrary, the flint line UH005 was
the most heat tolerant inbred line with highest temperature optimum of klat. Thus, the hypothesis that the
response of root growth to temperature of the two
groups is determined by their geographical origin can
be rejected.
(b) The optimum shift among specific inbred
lines may be used to select hybrids with altered
optimum and increased temperature range
We used parent– offspring correlations to evaluate
whether differences among inbred lines could be
passed on to their hybrids. For most traits with low
variability among the inbred lines, this was not the
case (table 2). However, the mid-parent values of the
temperature optimum of klat were strongly correlated
with klat of the hybrids (r ¼ 0.85). This was mainly
due to the fact that the cross between UH005 and
UH250, with an optimum of 348C and 288C, respectively, resulted in hybrids with an average of 318C (cf.
figure 4).
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1584
A. Hund et al.
Temperature-dependent heterosis
35
UH005 F
UH250 D
D*F
F*D
ERAx (cm d–1)
30
25
(a)
UH005 F
UH301 F
D*F
F*D
(b)
20
15
10
5
0
35
UH002 F
UH250 D
D*F
F*D
ERAx (cm d–1)
30
25
(c)
UH002 F
UH301 D
D*F
F*D
(d)
20
15
10
5
0
15
20
25
30
35
root zone temperature (°C)
40 15
20
25
30
35
root zone temperature (°C)
40
Figure 3. Temperature response of the elongation rate of axile roots (ERAx) for different combinations of crosses between flint
(dotted lines) dent (dashed lines) parents and their reciprocal hybrids using either the dent inbred (dot-dashed lines) or the
flint inbred as mother (solid lines). The curves were derived from the estimated model parameters presented in table 1. Each
point represents one plant cultivated at the particular temperature and scanned at regular intervals to estimate the growth rate.
As outlined for the temperature behaviour of
hypothetical genotypes (figure 1), the temperature
range of a hybrid may not only be affected by the temperature range of the parents but also by a shift of their
temperature optima. Accordingly, we tested whether
the temperature range of the hybrids could be predicted
by the combination of the range and temperature shift of
their parents (equation 2.4). Indeed, there was a reasonably strong parent–offspring correlation (r ¼ 0.54; table
2) for this trait, while the correlation was negative when
the temperature shift was not taken into account
(r ¼ 20.45).
(c) Dent inbred lines as a mother increased the
maximum elongation rate
For both root orders, i.e. the axile and lateral roots,
the hybrids with the dent as a mother (figures 3 and 4;
D * F) had a consistently higher elongation rate compared with those with the flint as a mother. These
parent-or-origin effects suggest maternal genetic effects,
or genomic imprinting. We tested the significance of
these effects using the hybrids as random variable and
the heterotic group of the mother (flint or dent) as a
fixed factor. Using the dents as mother increased the
maximum klat by 0.20 cm d21 (p , 0.001) and the
maximum ERAx by 9.6 cm d21 (p , 0.001 data not
shown), when compared with the flints as mother.
Phil. Trans. R. Soc. B (2012)
For both root orders, the pattern of the maximum
elongation rate (cf. table 1 and electronic supplementary material, S2) suggested that the flint line UH002
as a parent led to an increased elongation rate compared with the flint line UH005. Adding this
contrast into the fixed term of the model revealed
that UH002 increased klat of the hybrids compared
with UH005 by 0.15 d21 (p , 0.05; data not
shown). However, this effect could statistically not be
verified for ERAx. In summary, the highest klat was
achieved by a combination of the dent group as
mother and UH002 as father. An altered temperature
range or optimum temperature among the hybrids
depending on the heterotic group or genotype could
not be verified statistically.
4. DISCUSSION
We aimed to evaluate whether the response of root
growth to temperature can be described using a nonlinear model. The model of choice was a Gaussian
function, because it allows retrieving biologically
meaningful parameters in a parsimonious model and
because it is consolidated also by other experimental
root growth data [19]. Moreover, this simple model
is sufficient to test the clear-cut hypothesis investigated
here, while in future studies working with a broader
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Temperature-dependent heterosis A. Hund et al.
1.0
klat (d–1)
0.8
UH005 F
UH250 D
D*F
F*D
(a)
UH002 F
UH250 D
D*F
F*D
(c)
1585
(b)
UH005 F
UH301 F
D*F
F*D
0.6
0.4
0.2
0
1.0
klat (d–1)
0.8
UH002 F
UH301 D
D*F
F*D
(d)
0.6
0.4
0.2
0
15
20
25
30
35
root zone temperature (°C)
40 15
20
25
30
35
root zone temperature (°C)
40
Figure 4. Temperature response of the relative elongation rate of lateral roots (klat) for different combinations of crosses
between flint (dotted lines) and dent (dashed lines) parents and their reciprocal hybrids using either the dent inbred
(dot-dashed lines) or the flint inbred as mother (solid lines). The curves were derived from the estimated model parameters
presented in table 1. Each point represents one plant grown at the particular temperature.
Table 1. Parameters estimates, describing the response of the elongation rates of axile and lateral root to temperature of four
inbred lines and their reciprocal hybrids. The parameters were estimated using a Gaussian function. Errors indicate 95% CI.
axile roots
UH002_F
UH005_F
UH250_D
UH301_D
UH002 UH250
UH002 UH301
UH005 UH250
UH005 UH301
UH250 UH002
UH250 UH005
UH301 UH002
UH301 UH005
population mean
lateral roots
temperature
rangea (8C)
temperature
optimum (8C)
maximum
growth at temp.
opt. (cm d21)
5.22 + 1.71
5.07 + 4.53
8.1 + 26.01
4.56 + 1.02
5.28 + 1.65
4.83 + 1.59
4.89 + 1.65
5.25 + 1.44
5.04 + 1.11
6.03 + 1.68
5.37 + 1.23
5.94 + 1.41
5.22 + 0.36
27.96 + 1.56
29.49 + 4.5
25.65 + 18.96
27.69 + 1.08
29.4 + 1.65
28.2 + 1.5
28.38 + 1.59
28.11 + 1.35
28.35 + 1.05
29.01 + 1.56
28.83 + 1.11
28.68 + 1.32
28.38 + 0.39
21.41 + 6.97
7.87 + 6.6
3.62 + 11.58
32.76 + 7.88
21.71 + 6.5
21.64 + 7.25
20.62 + 7.15
25.01 + 6.91
31.89 + 7.02
24.22 + 6.19
32.03 + 6.75
27.75 + 6.31
22.2 + 5.2
temperature
range (8C)
temperature
optimum (8C)
maximum
elongation at
temperature
optimum (d21)
8.22 + 3.09
5.34 + 2.55
6.45b
5.04 + 1.35
6.78 + 2.55
6.51 + 2.46
8.43 + 5.4
6.69 + 2.67
5.31 + 1.38
6.57 + 2.22
5.88 + 1.71
6.15 + 2.25
6.45 + 0.66
28.29 + 2.49
34.05 + 2.28
28.28
28.14 + 1.38
28.5 + 2.25
29.04 + 2.25
30.99 + 4.95
28.95 + 2.4
27.54 + 1.26
30.45 + 2.09
28.8 + 1.5
28.68 + 2.07
28.86 + 0.66
0.75 + 0.21
0.77 + 0.22
0.770
1.05 + 0.31
0.72 + 0.23
0.71 + 0.24
0.47 + 0.21
0.67 + 0.24
1.08 + 0.28
0.83 + 0.23
1.03 + 0.26
0.74 + 0.24
0.765 + 0.092
a
The temperature range is given as one s.d.
CI were not available because data were estimated from the mixed nonlinear model.
b
base of genotypes, more differentiated models might
be adequate. Also, this model may not be adequate
for other traits or studies, where the response to
Phil. Trans. R. Soc. B (2012)
temperature results in a more asymmetric distribution
of values above and below the temperature optimum.
In these cases, the beta function proposed by Yin
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1586
A. Hund et al.
Temperature-dependent heterosis
Table 2. Parent –offspring correlations for parameter
estimates, describing the response of the elongation rates of
axile (ERAx) and lateral (klat) root to temperature. The
parameter ‘range and temperature shift’ adds the difference
in the temperature optima between parents to their
temperature range (equation (2.4)) before correlation with
the temperature range of the hybrids.
parameter
ERAx
klat
temperature range
range and temperature shift
temperature optimum
maximum elongation
20.07
0.07
20.43
0.33
20.45
0.54
0.85
20.028
et al. [38] or the thermodynamic function proposed by
Johnson & Lewin [39] may be better suited. Parent
et al. [26], for example, used Johnson and Lewin’s
function to model the temperature response of
in vitro enzyme activities, developmental processes or
net photosynthesis. These more complex models,
however, have the disadvantage that they require estimating more than three model parameters and are
therefore less parsimonious.
The temperature response of the flint and dent
parents did not differ in all aspects investigated. For
example, the temperature optimum of axile root
growth did not differ between flint and dent lines,
indicating that a systematic utilization of marginal overdominance has not been the background of historical
development of these heterotic groups. This is in line
with the findings of McWilliam & Griffing [24] who
did not find a strong difference with respect to the temperature optima of dent and flint. However, our results
suggest that some genotypes possess the potential to
improve the hybrid’s reaction of root growth to temperatures. Particularly, the cross between UH005 and
UH250 demonstrates this effect for klat. It is unclear
why only the temperature optimum of lateral roots was
affected and not that of axile roots. However, a differential response of axile and lateral roots to temperature was
also reported earlier [22].
It is well conceivable that similar marginal overdominance effects of root elongation response to
temperature are of relevance in laboratory studies or
under greenhouse conditions with plants cultivated in
pots or other small containers. Under such conditions,
temperature variations throughout 24 h can be considerable; especially when plants are grown under
relatively high light intensities. Then, topsoil pot temperatures can exceed air temperature by 108C owing to
the radiative heat input and the negligible thermal
buffering capacity of small pots [11], adding up to the
numerous perils of pot experiments [40]. Minuscule
root systems of plants such as Arabidopsis thaliana
would, under such circumstances, have an enormous
advantage if their growth temperature optimum was
wider than usual. Clear heterosis effects in young
Arabidopsis seedlings bred from accessions of different
geographical origins have been demonstrated [41].
It will be important to elucidate whether short-term
fitness advantages in laboratory-based pot experiments can be correlated with the performance under
field conditions. In the field, crops have to perform
Phil. Trans. R. Soc. B (2012)
well under changing conditions of abiotic stress
throughout the season.
There are several explanations for how marginal overdominance in the case of klat in the UH005 UH250
cross might have been controlled genetically. First,
hybridization may lead to hemizygous complementation
of many genes with small effects [42]. This complementation may also involve loci that have different
temperature optima, thereby providing one explanation
for marginal overdominance. Second, gene expression
in maize hybrids most frequently follows the mid
parent expression of the two parental alleles, meaning
that one allele is preferably expressed [43]. In response
to abiotic stress, these two alleles can be regulated differentially [31] or their gene products can be broken down
at different threshold temperatures, as shown for
rubisco activase [25]. Consequently, the enzyme with
the lower temperature optimum would deteriorate first
in a hybrid, leaving only its counterpart to function.
We hypothesize that it is possible to combine inbred
lines with optimal response pathways to low and high
temperatures in order to produce a superior hybrid
that would be tolerant to a range of abiotic stresses.
Owing to the observed parent-of-origin effects, it may
be important to select the appropriate maternal line.
Dent inbred lines as a mother increased the maximum elongation rate. Hoecker et al. [14] studied the
same set of genotypes and did not find similar effects
for the length of the primary root. However, there was
a significant heterosis effect on cortical cell size and a
tendency that the dent inbred lines and the hybrids
with dent inbreds as a mother had longer cortical cells.
Such effects could be explained by genomic imprinting
or by maternal genetic effects. Imprinting effects have
been suggested for germination of maize [44]. High
temperature during seed drying (438C) decreased germination of some reciprocal hybrids but had no effect
on others [44]. Certainly, more experimental data
will be necessary to elucidate which are the causal
mechanisms of these parent-of-origin effects.
(a) Conclusion and outlook
Classical research on temperature tolerance focuses on
either cold or heat stress. However, it is becoming
increasingly evident that breeding research has to focus
on the whole range of possible temperatures to which
the plant may be exposed. The linkage between chilling
tolerance and heat sensitivity in very early maize material
[4] demonstrates this need. With advantages in statistical
computing, nonlinear models allow characterization of
genotypes based on model parameters. The major
advantage of this approach is that such experiments
can be carried out without a marked increase in the biological replications. For example, a classical approach
with two treatments would estimate two parameters for
each genotype, i.e. the intercept and the slope. The
model used here requires only one additional mathematical parameter but allows conclusions for more relevant
biological parameters or crop traits.
The presented set of genotypes did not differ markedly
with respect to temperature response. However, it could
be shown at least for the growth of lateral roots of one
cross, that the concept of marginal overdominance for
Downloaded from http://rstb.royalsocietypublishing.org/ on June 18, 2017
Temperature-dependent heterosis A. Hund et al.
temperature response may be exploitable. Appropriate
combinations of maternal and paternal lines may lead
to hybrids with a wider optimum range, an intermediate
optimum temperature and an unaltered maximal root
growth potential compared with both parental lines.
Proper registration and application of this heterosis
effect can lead to successful hybrid lines that can perform
well in a wider range of temperature conditions, thereby
allowing for improved whole-plant performance under
abiotic stress conditions. Further research will have to
elucidate to what extent the effect is accessible for breeding and which traits are the most promising to connect
hybrid performance under controlled conditions
with hybrid performance under productive conditions in
the field or greenhouse.
13
14
15
16
We thank Albrecht Melchinger for the supply of the genotypes.
17
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