ELSEVIER
Field
Crops
Research
Field Crops Research 66 (2000) 37-50
www.elsevier.com/locate/fcr
Photosynthesis of wheat in a warm, irrigated environment
I: Genetic diversity and crop productivity
M.P. Reynolds u,*, M.1. Delgado B. b , M. Gutierrez-Rodrfguezb , A. Larque-Saavedrab
'1IIlemationai Mai::.e and Wheat ImprOl'emelll Celllre (C1MAnT), Apartado 370. PO Box 60326, HOUSIOIl, TX 77205. USA
hColegio de Postgraduados, Carretera Mhico-Texcoco Km. 36.5, 56230 MOllleci/lo, Mexico. Mexico
Received 19 July 1994; accepted 29 November 1999
Abstract
Net photosynthetic rate (An), stomatal conductance (gs)' chlorophyll content and aa~ron rate were measured on 16
wheat cultivars (Triticum aestivum L.), grown in replicated yield trials in a warm, irrigated, and low relative humidity
environment in central Mexico. Measurements were made on flag leaves in full sunlight at three different stages of plant
development (booting. anthesis, and grain fil1ing), and at different times of the day. Two experiments were conducted with
sowing dates in December 1991 and March 1992. whose average daily temperature for their respective growing cycles were 21
and 25°C. Physiological measurements were compared with agronomic performance on the same field plots. An 'was fairly
stable during the day between 10:00 and 14:00 h, and across experiments, despite differences in leaf temperature of up to 4°C.
An fell noticeably at successively later stages of plant development. however, and there were clear differences among cultivars.
With both sowing dates. An and g, measured at all three stages of development correlated significantly with yield and biomass
of the cultivars. An during the grain filling period was also strongly associated with chlorophyll loss. The data indicate that
differences in An throughout the crop cycle as well as variation in the onset of senescence may be important variables affecting
wheat yield potential in warm environments. (' 2000 Elsevier Science B.Y. All rights reserved.
Key\\'(mls: Genetic variability: Heat tolerance: Photosynthesis; Physiological selection traits; Wheat; Yield potential
Abbrel'iations: An. Net photosynthetic rate; !-:,. Stomatal conductance; C,. Intercellular CO 2 concentration; ChI a:b. Chlorophyll a:b ratio; R.
Dark respiration rate
1. Introduction
The productivity of wheat decreases as mean daily
temperatures rise above approximately 15 'c, in part
because accelerated crop development rate reduces
Corresponding author. Td.; + 1-650-833-6655: fax:
833-6656.
.E-mail address: [email protected] (M.P. Reynolds)
+ 1-650-
crop duration (Midmore et aI., 1982). Common wheat
cultivars differ in performance under warm conditions
(Midmore et al.. 1982: Rawson, 1986), but not all of
the genetic variation was explained by response of
development rate when comparing lines with uniformly high genetic yield potential (Reynolds et a1..
1998). It is well-established that high temperatures can
affect many of the processes involved in photosynthesis (Berry and Bjorkman. 1980). In wheat, differ-
" .', ""\''I'l>o(
~~.
•
037X-4290/{XJ/S -, sec lront matter «' 2000 Elsevier Science B. V. All rights
PH: S037H-47°I)'9lJ)00077-5
reservedr""-~
"
"'~~'-~.".;"
,
• __ -'
~,
•• 1":<-
~l
\
~..f.'I
""Ji""'-.z.'"
~;t
.
I
I
•
.
38
M.P. Reynolds et al.l Field Cmps Research 66 (2000) 37-50
ences in net photosynthetic rate (An) among cultivars
at high temperature have been shown to be associated
with lower leaf chlorophyll concentration and a
change in the chlorophyll a:b ratio (ChI a:b) due to
accelerated leaf senescence (AI-Khatib and Paulsen,
1984; Harding et aI., 1990). Differences in An have
been related to performance under high temperature
for a number of crops including soybean (Wells et aI.,
1982), cotton (Cornish et aI., 1991), and rice (Sasaki
and Ishii, 1992). Studies with different wheat cultivars
in controlled environments under elevated temperatures have indicated associations between plant
growth and the response of photosynthetic traits
(Blum, 1986; AI-Khatib and Paulsen, 1990) as well
as dark respiration (Wardlaw et a!., 1980). However,
the relationship between the performance of wheat
crops at high temperature in field environments and
the response of photosynthetic parameters has not
been well studied.
The relationship between grain yield and An is not
straightforward for a number of reasons. Firstly, yield
differences in wheat are more often associated with
harvest index than with differences in radiation-use
efficiency (Calderini et aI., 1995). Where yields are
primarily limited by assimilate supply, an association
between photosynthetic capacity and performance
cannot necessarily be expected. There are a number
of physiological factors that reduce the amount of net
carbon fixed which is then available for growth,
principally respiration of assimilates during the dark
period (Amthor, 1989), as well as loss of carbon from
root exudates, senescence and other processes. Finally,
in order to relate accurately crop productivity to leaf
photosynthesis, quantification of canopy photosynthesis is required. Measurement of whole-canopy carbon-exchange rate for just a short period of time is
expensive (Harrison et a!., 1981). Furthermore, even
when measurements of canopy photosynthesis integrated over the crop cycle have been attempted (Puckridge, 1971). they did not always explain yield
differences among cultivars (Gent and Kiyomoto.
1985).
Models of canopy photosynthesis can produce reasonable estimates of gross photosynthesis if total
canopy light interception over the whole crop cycle
and light extinction are estimated well, if standard
responses of photosynthesis to light intensity and
temperature are known. and when factors such as
water and nutrition are assumed to be non-limiting.
However. to model differences among genotypes
would require a considerable a priori knowledge about
the unique characteristics of each genotype including:
(i) rate of canopy establishment and leaf area index
development: (ii) canopy architecture; (iii) nitrogen
distribution in the canopy; and (iv) dynamic changes
in light extinction over the crop cycle. The possibility
for unique genotypic responses of photosynthetic
metabolism to light and temperature should not be
ruled out. The fact that leaf metabolism can adapt to
different light flux densities according to their position
in the canopy (Evans, 1993) may even necessitate
multiple light-response relationships. Furthermore.
the various mechanisms that dissipate excess light
energy and thereby influence photoinhibition and
radiation-use efficiency (Bjorkman and DemmigAdams, 1994) could also be subject to genetic
variation. Once gross carbon fixation rate has been
simulated. net carbon fixation can be calculated by
estimating the cost of growth, maintenance, and
photorespiration (Loomis and Amthor, 1996). However, genetic variation cannot be ruled out for these
factors either.
Because both direct measurement and simulation of
canopy photosynthesis on several genotypes is generally impractical, crop physiologists have measured
maximum leaf photosynthetic rate as a surrogate.
perhaps encouraged by the fact that little genetic
variation for photosynthetic rate at subsaturating light
intensities has been reported (McCree, 1971: CharlesEdwards. 1978). While high values of An have been
recorded, e.g. in wheat diploid progenitors (Austin
et al.. 198~). such results are rarely associated with
greater productivity. This lack of association is not
surprising for many of the reasons stated above related
to the complex relationships between leaf photosynthesis. canopy photosynthesis. and growth. Not least of
these is the fact that individual leaves generally operate well below light saturation. with incident radiation
levels depending on leaf poshion in the canopy, leaf
angle. and solar-track. At best. differences in An can be
expected to make modest contributions to yield (Nelson. 1988).
Higher An at saturating or near saturating light
levels. however. may have a significant impact on
performance in warm. low relative humidity environments because: (i) the canopy is exposed to direct
·.
:19
M.P. Remolds el al./ Field Crops Research 66 (200th 37-50
radiation for most of the daylight period. (there being
little cloud cover); (ii) a relatively large proportion of
leaves in the canopy are exposed to direct radiation
because accelerated development tends to result in a
lower leaf area index and therefore less mutual shading when compared with temperate crops (unpublished data); and (iii) grain yield is more assimilate
limited as indicated by the high association between
yield and biomass (Reynolds et al.. 1994) in comparison to temperate environments (Sayre et al.. 1997).
Even a relatively modest association between An and
crop yield in this environment may indicate the value
of using An to select breeding lines that are better
adapted to warm environments. and these issues are
discussed in an accompanying paper (GutierrezRodriguez et aJ.. 2000). The association that has been
observed of yield with stomatal conductance (g,) and
canopy temperature depression in this environment
further supports this possibility (Amani et al.. 1996).
The principal objectives of the present study were to:
(i) determine genetic differences in flag leaf An in a set
of 16 widely used wheat cultivars grown under irrigation in a warm. low relative humidity. field environment; (ii) observe whether An of different cultivars
interacted with time of day. phenological stage. and
growing environment (i.e. sowing date); (iii) compare
An and related parameters with agronomic performance; and (iv) add to the understanding of the
physiological mechanisms underlying genetic diversity for heat tolerance in wheat. A number of photosynthetic parameters including An' g,. chlorophyll
content. chlorophyll a:b ratio (Chi a:b). intercellular
CO 2 concentration (Cj ). and dark respiration rate (R)
were measured on flag leaves of 16 cultivars grown in
replicated yield plots. In a companion paper (Gutierrez-Rodriguez et al.. 2000). the potential for making
genetic gains in yield by selecting leaf photosynthesis
and related traits was evaluated in the progeny of a
cross between two of the 16 lines which contrasted in
An and heat tolerance.
2. Materials and methods
2.1. Test materials
Test materials used in this study were 16 wheat
cultivars (Triticum aestivum L.). The cultivars were
chosen to meet one or more of the following criteria:
broadly adapted: high yielding under irrigation; grown
or bred in warm areas: heat sensitive (i.e. checks). All
of the cultivars had b~en evaluated for field performance in a number of countries as part a collaborative
project between their national wheat improvement
programs and the International Maize and Wheat
Improvement Center (CIMMYT), for further details
see Reynolds et al. (1994).
2.2. Growing conditions
The study was conducted under field conditions
at the CIMMYT experiment station in Tlaltizapan.
central Mexico 08.4 c N, 99.I W, 940m a.s.l.). The
climate is warm. sunny and dry during the winter
<Table I). and it is representative of many warm
wheat-growing environments in the developing world
(Reynolds et al.. 1994). Soil is a calcareous vertisol
(isothermic Udic Pellustert: USDA taxonomy).
G
Table 1
Long-tcnn weather data for winter sowing cycle. Tlaltizapan. Mexico
Month
!\ovember
December
January
February
1\tan:h
April
1\13:
Mean temperature ( C)
Rain (mm)
Maximum
Minimum
Mean
30.7
30.1
30.1
31.5
D.n
35.2
35.1l
11.7
9.9
21.2
21l.1l
IY.5
20.9
22.9
25.1
!U~
10.2
12.\
15.1
17.7
26.4
6.9
3.1
7.7
2.8
6.'10.6
56.3
Sunhours
Y.I
8.1\
9.1
9.7
10.1
9.9
9.3
-.
40
M.P. Remolds et alJrieiiCrops Research 66 (2000) 37-50
The wheat cultivars were drilled in plots 6 m long
by eight rows with 15 cm between rows. and 30 cm
between rows of adjacent plots. Plant density was 200
plants m -2. Plots were well managed with respect to
fertility: 200 kg N ha -I was supplied as ammonium
sulfate and 30 kg P ha -I as triple superphosphate.
Plots were irrigated using overhead sprinklers every
7-14 days to match potential evaporative losses from
the crop (based on measured pan evaporation). Two
tons per hectare of elemental sulfur was incorporated
with the other fertilizers to reduce the risk of soilborne
disease. Folicur (0.5 kg ha- I ) was applied every 14
days to prevent foliar fungal diseases. Metasixtos
(I I ha- I) was applied twice between booting and
maturity to control insects.
There were two sowing dates considered here as
Experiments I and 2. The dates of plant emergence for
the experiments were 10 December 1991 (Experiment
I) and 9 March 1992 (Experiment 2). The design in
each experiment was a randomized complete block
with three replications.
2.3. Photosynthetic parameters
Net photosynthetic rate (An) (Jlmol CO2 m- 2 S-I)
was measured on flag leaves (lamina) using an IR gas
analyzer in an open-system (IRGA, LCA-2. ADC,
Hoddesdon, England). The measurements were made
on portions of leaves exposed directly to the sunlight
in the six inner rows of each plot, while the leaves
were maintained at right angles to incident solar
radiation.
Due to phenological differences among the cultivars, three approximate growth stages were designated
for measurements of An' i.e.: "booting". when all
cultivars were between Zadoks stages 37 and 49;
"anthesis" when cultivars were between Zadoks
stages 55 and 70: and "grain filling" when cultivars
were between Zadoks stage 75 and 85 (Zadoks et aI.,
1974). Actual dates of sampling were 20-24 January,
10-14 February, and 24-28 February for Experiment
I; and 13-17 April. 27-30 April and II-IS May for
Experiment 2 for booting, anthesis and grain filling
stages, respectively. Measurements were taken at
10:00, 11 :00, 12:00, and 13:00 h in Experiment I;
and at 10:00, 11 :00. 15:00. and 16:00 h in Experiment
2. One leaf was measured per cultivar for each sampling time on one of the replications in a single day.
Sampling procedure was repeated on successive days
for each replication. At the same time. stomatal conductance (gd. leaf temperature and light intensity
were recorded with the IRGA.
For simplicity. ambient CO 2 was employed in the
study. The levels declined linearly during the day from
a high near 380 ppm (v/v) at 10 AM to near 365 ppm
at 3 PM. This introduced slight variation into observed
values of An but did not affect ranking of means or our
interpretations and conclusions. For more critical
work, one could use cylinder gas or correct the
observations through covariate analysis.
2.4. Dark respiration
After An was measured dark respiration was estimated on the same leaf by completely excluding light
from the IRGA cuvette. The rate of CO 2 evolution was
recorded after 5 min of dark acclimation. It was found
in preliminary measurements that the rate of CO2
evolution stabilized after approximately 3-4 min of
dark adaptation (Decker, 1955). Respiration was
recorded after only one of the photosynthesis measurements between 15:00 and 17:00 h in Experiment
1. and between 13:00 and 15:00 h in Experiment 2.
Rate of CO2 respired was expressed as mg CO2 g-l
dry leaf. Specific leaf weight was estimated on three
leaf disks (11 mm diameter) taken from flag leaves
which were oven-dried and weighed.
2.5. Chlorophyll estimations
After the measurements of physiological parameters. the flag leaves of the 16 cultivars were separated from the plants and placed at approximately S"·C
on moist filter paper, wrapped in aluminum foil. and
taken to the laboratory in a cooler. Six disks of II mm
diameter were cut from each leaf; three of them were
placed in a drying oven to estimate dry weight.
Chlorophyll was extracted from the other three disks
by crushing them in a mortar with 80l/c acetone-water
solution (v/v) and a pinch of calcium carbonate. The
extract was centrifuged at 3500 rpm for 7 min. The
supernatant was made up to a known volume and
absorbency was measured at 663 and 645 nm in a
spectrophotometer (SP8-1 00. Pye Unkam. England).
Chlorophyll a. chlorophyll b. and tOlal chlorophyll
were estimated using Harborne's (197.1) equation~.
ofl
M.P. Reynolds et at. / Fidd Crops Research 66 (2000) 37-50
2.6. Anthesis, maturity, and yield components
In both sowings, the number of days to anthesis and
maturity were measured from seedling emergence to
when 50% of the spikes had extruded anthers, and
when 50% of the spikes had no green color remaining.
Yield was measured after physiological maturity by
harvesting and threshing the six inner rows of the
plots, excluding a 0.5 m border at each end. Prior to
grain harvest. a random subsample of 100 spikebearing culms (SBC) were removed from the inner
six rows of the plots. The subsample was oven-dried,
weighed, and threshed. The grain weight was recorded
and individual kernel weight estimated using a subsample of 200 kernels. These data along with plot
yields were used to calculate harvest index. abO\'eground biomass. grains m- 2 • spike'i m- 2 (calculated
as aboveground biomass weight per SBC), and grains
per spike.
2.7. Statistical analysis
Data of the two experiments were combined and
analyzed in a factorial design, i.e. with two sowing
dates. three stages of development, four times of day,
and 16 cultivars. Sowing dates were considered statistically as different locations. To assess whether
cultivar differences in development stage within each
of the three sampling periods had a significant interaction with the photosynthetic parameters measured,
data were also analyzed using a covariate. namely the
number of days between the date on which measurements were taken and the anthesis date of the cultivar.
The covariate. however, was not found to be significant for An.
3. Results
3. J. Cultil'ar effects on An and interaction with
phenology
Analysis of variance for An (Table 2) revealed
highly significant differences among the 16 cultivars.
Interactions of cultivars with environment (i.e. Experiment I and Experiment 2) and with measurement
time during the day were not significant but there
was an interaction between cultivars and stage of
development in Experiment I. The interaction did
not appear to be related to major changes in the
rankings of cultivars across different phenological
stages (Table 3), and was probably caused by the
fact that the absolute range of values for An among
cultivars was larger during grain filling than at earlier
Table 2
Analysis of variance for net photosynthetic rate of 16 wheat cultivars in Tlaltizapan. Mexico. 1991-1992
Source of variation
Degrees of freedom
Pr>P'
Cultivar (16 genotypes)
Experiment (2 sowing dates)
Stage (3 stages of development)
Time (4 times of day)
Experiment x eultivar
Experiment x stage
Experiment xtime
Experiment x stage x eultivar
Experiment x stage x time
Stagexcultivar
Stage x time
Cultivarx time
Stage x cultivarx time
Experiment x stage x cultivar x time
15
0.0001
0.0017
0.0001
0.0005
0.5640
0.0001
0.0001
0.7137
0.7069
O.011l9
0.2642
0.3621
0.9861
0.9825
J
2
I or 3
15
2
I
30
2
30
2 or 6
15 or 45
JO or 90
30
.. Analyzed using two planting dates and two sampling lil11~~ ( 10:00 anJ 11:00 It).
h Experiment I with four sampling time.. (10:00. II :00. I ~:oo and 13:00 h).
, Experiment 2 with four sampling time.. (10:00. II :00. 1:':00 anJ Ih:OO h).
0.0001
0.0001
0.0001
0.2489
0.0001
0.0001
0.0001
0.0002
0.9413
0.9995
0.2854
0.0001
0.7344
0.4701
M.P. Reynolds e1 al. / Field Crops Research 66 (2000) 37-50
42
Table 3
Net phot~synthetic rate (An) at three stages of deye]opment. chlorophyll content during grain filling. days to maturity, yield. and biomass for 16
spring wheat cultivars (in order of grain yicld I. Experiment 1. Tlaltizap.in. Mexicu. 1991-1992
Cultivar
An (~mol m- 2 S-I)
Chlorophyll grain
filling (mg m- 2)
Maturity
(days)
Yield
(t ha- I )
Biomass
(t ha- I )
104
103
93
102
103
101
97
102
103
103
97
98
91
90
90
104
4.69
4.53
4.24
4.24
4.23
4.11
4.00
4.00
4.00
3.98
3.89
3.87
3.50
3.13
2.43
2.21
11.49
10.32
10.04
10.52
9.98
9.96
9.81
9.40
10.31
9.83
9.28
9.41
9.25
8.65
6.08
7.89
Booting
Anthesis
Grain filling
Debeira
Seri-M82
Fang Sixty
Glennson-81
Genaro-81
Nesser
ClAND-79
Siete Cerros-T66
Anza-87
Bacanora-88
Nacozari-76
Pavon-76
Kanchan
IP4
Sonora-64
Trigo-3
22.5
25.1
27.0
22.7
24.0
25.9
26.2
23.8
24.4
23.3
25.1
25.5
25.4
24.3
21.0
20.9
20.2
21.9
21.3
22.6
23.6
21.9
21.0
18.9
22.9
19.0
21.9
22.1
18.0
21.8
18.1
18.3
12.9
20.3
15.8
19.0
19.6
16.7
15.7
16.0
16.9
16.2
16.9
16.5
13.8
14A
11.8
13.0
265
481
457
479
447
466
417
427
403
393
440
461
333
337
248
350
Mean
LSD
r with yield
24.2
2.9
0.55*
20.9
2.6
0.56*
16.0
2.7
0.65**
400.3
37.0
0.53*
stages (Fig. la). A similar pattern was observed in
Experiment 2 (Fig. 1b). Overall, these results reveal
that cultivars were not interacting significantly with
time of day or environment, but that differences in An
became greater at later stages of phenology.
98.9
2.5
0.43
3.82
0.52
1.00
9.51
0.97
0.91**
3.2. Effects of time of day, phenology, and
environment on An
The main effect of time of day was significant only
in Experiment 2. and this was probably a function
Table 4
Net photosynthetic rate (An), light flux density. and leaf temperature (1',) <It different times of day. The values are averaged for flag leaves of 16
wheat cultivars at three growth stages grown at Tlaltizapan. Mexico, IlJlJl-I992"
Time of day
£y;periment I
An (~mol m- 2 S-I)
Light nux density (~mol m - 2 s- I)
1'1 ("'C)
10:00
11:00
12:00
13:00
LSDb
S.E.
20.3
1316
19.7
1426
31.5
20.1
1450
32.7
20.3
1371
33.3
1.2
61
0.5
0.2
10.7
0.11
LSD"
S.E.
1.2
43
0.37
0.22
9.9
0.11
29A
10.00
11.00
15.00
16.00
Experiment 2
An (~mol m- 2 5- 1)
Light flux density (~mol m- 2 s -I)
1'. (C)
19.7
ID7
31.8
22.1
1243
33.7
17.9
1070
36.6
15.6
871
36.6
"Mean of leaf chlorophyll contcnt was ~S mg m-:: fllr Expcrimclll L <lnd 4X6 mg m-:: for Experiment 2.
"Least significant diffcrence atll~{).05.
M.P.
M.P. Reyllolds
ReynuldseTelal.
al./ /Fidd
FiddCrops
CropsI<l!searcil
Research66
66(2000)
(2000)37-50
37-50
25
•
•
..
')IE 20
"5
(a)
•
."
pOSI.antheS~iS'''=081•
~
•••
"",0.74
I I)
:
•
E
-
Pre-anthesls. "=0.59Anthes,s, "=0.81-
.
••
•
•
•
.... .
m..a.99 •
::J.
«c
.
15
""'1.3
10
25
-+--""-------'----""--------'----1
•
•
..
P.....nthe.is. '>=0.79Anthes.s. ""0.77Post-anlllesis. '>=0.88-
(b)
-
":11)
N
'E 20
"5
E
::J.
<t
15
_1.3 ..
10
....L-_,..--_ _-,-_ _--,.
16
18
20
-,--_ _
22
Fig.
Fig. 1.1. Regression
Regressionofofnet
netphotosynthetic
photosyntheticrate
rate(An)
(An)atatthree
threegrowth
growth
stages
stageson
onthe
theaverage
averagevalue
valueofofphotosynthesis
photosynthesisover
overthe
thethree
threestages
stages
for
16·wheat
wheatcultivars
cultivarssown
sown(a)
(a)ininDecember
December 1991
\99\ (Experiment
(Experiment I)\)
for 16
and
and (hI
(h) March
March 1992
1992 (Experiment
(Experiment 2).
2). Each
Each point
point represents
represents aa
foursampling
samplingtimes
timesthroughout
throughoutthe
theday.
day.
cultivar
cultivarand
andisisthe
themean
meanofoffour
(**)
(**)significant
significantatatp~O.OI.
p:SO.OI.
of
of reduced
reduced light
light flux
flux density
density atat the
the latter
latter sampling
sampling
times
times (Table
(Table 4).
4). The
The main
main effect
effect of
ofphenology
phenology was
was
aa reduction
reduction inin An
An atat successive
successive growth
growth stages
stages for
for
both
both experiments
experiments (Table
(Table 5).
5). For
For example.
example, inin
Experiment
Experiment I I between
between booting
booting and
and grain
grain filling.
filling, An
An
declined
declinedby
by 14-44%
14-44%depending
dependingon
oncultivar
cultivar(Table
(Table 3).
3).
This
This reduction
reduction inin An
An (average
(average 14%
14% inin Experiment
Experiment I 1
and
and 7%
7% inin Experiment
Experiment 22 between
between booting
booting and
and
anthesis)
anthesis) was
was not
not accompanied
accompanied by
by aa loss
loss of
of chlorochlowphyll
phyll content.
content. However.
However, aa similar
similar reduction
reduction inin An
An
later stage.
stage, i.e.
i.e. between
between anthesis
anthesis and
and grain
grain
atat aa later
filling.
filling. was
was associated
associated with
with aa reduction
reduction of
of abollt
abollt
20%
20% inin chlorophyll
chlorophyll content
content inin both
both experiments
experiments
43
43
(Table
(Table 5).
5). There
There was
was aa main
main effect
effect of
of environment
environment
when
whencomparing
comparingmeasurements
measurementsmade
madeatatthe
thesame
sametime
time
inin the
the morning
morning (Table
(Table 2)
2) with
with Experiment
Experiment 22 having
having
5'1159Cgreater
greaterAn
Anthan
thanExperiment
Experiment II(Table
(Table44l.l.associated
associated
with
with aa8%
8% higher
higher leaf
leafchlorophyll
chlorophyll content
content inin ExperiExperiment
ment 22(Table
(Table 5).
5).
Interaction
Interaction between
between time
time of
of measurement
measurement and
and
environment
environment was
was significant
significant considering
considering the
the mornmorning
ing measurements
measurements (Table
(Table 2).
2). but
but the
the result
result does
does
not
not appear
appear toto have
have any
any obvious
obvious biological
biological signifisignificance
cance (Table
(Table 4).
4). The
The interaction
interaction between
between time
time of
of
measurement
measurement and
and growth
growth stage
stage was
was not
not significant
significant
considering
considering only
only the
the morning
morning measurements.
measurements. but
but
was
was significant
significant when
when considering
considering readings
readings taken
taken
throughout
throughout the
the day
day for
for both
both environments
environments (Table
(Table 2).
2).
InIn Experiment
Experiment I.I. An
An decreased
decreased slightly
slightly throughout
throughout
the
the day
day atat booting.
booting. but
but revealed
revealed the
the opposite
opposite
trend
trend atat anthesis
anthesis and
and grain
grain filling
filling (data
(data not
not shown).
shown).
The
The differences
differences were
were relatively
relatively small
small and
and itit
would be
be difficult
difficult toto ascribe
ascribe any
any biological
biological signifisignifiwould
cance toto them.
them. Similarly.
Similarly, no
cance
no biologically
biologically meaningmeaningful
ful pattern
pattern could
could be
be observed
observed inin the
the interaction
interaction
between
between growth
growthstage
stageand
and time
time of
ofday
day ininExperiment
Experiment
2.2. None
None of
ofthe
the threethree- or
or four-way
four-way interactions
interactions were
were
significant.
significant.
3.3.
3.3. Association
Associationof
ofAll
All with
with agronomic
agronomicpeiformance
performance
Leaf
Leaf An
An measured
measured atat all
all growth
growth stages
stages inin both
both
environments
environments was
was associated
associated with
with final
final yield
yield of
of the
the
16
16cultivars
cultivars(Table
(Table6).
6).Carbon
Carbonuptake
uptakeisisdependent
dependenttotoaa
large
largeextent
extenton
onstomatal
stomatalconductance
conductancewhich
which was
wasmeameasured
suredatatthe
thesame
sametime
timeasasAn
Anininthese
theseexperiments.
experiments.The
The
g,
g, measured
measured atat all
all growth
growth stages.
stages. also
also correlated
correlated
strongly
strongly with
with yield.
yield. and
and regression
regressionanalysis
analysis indicated
indicated
that
that average
average values
values of
ofAn
An and
and g,g, explained
explained approxiapproximmely
mately half
half of
ofthe
the variability
variability inin performance
performance of
ofthe
the
cultivars
cultivars (Fig.
(Fig. 2).
2). Other
Otheragronomic
agronomic traits
traits were
were assoassociated
ciatedwith
withAn
Anincluding
includingbiomass
biomass(Table
(Table7)
7)and
andharvest
harvest
index
index (data
(data not
not shown).
shown). though
though not
not as
asstrongly
strongly asas for
for
yield
yield itself.
itself.
Earlier
Earlier analyses
analyses of
of these
these data
data demonstrated
demonstrated that
that
An
All and
and ,l{,
g, were
were associated
associated with
with performance
performance of
of the
the
same
same 16
16cultivars
cultivarswhen
when grown
grownatatinternational
internationaltesting
testing
sites
sitC's that
that experienced
experienced high
high temperatures
temperatures such
such asas
those
those inin Brazil.
Brazil. Egypt.
Egypt. Sudan
Sudan and
and India
India (Reynolds
(Reynolds
etet '11..
al.. 1994).
1994).
,\f.P. Reynolds et al. / Field Crops Research 66 (2000) 37-50
44
Table 5
Average net photosynthetic rate lA n ). chlorophyll content. and dark respiration (R) of 16 wheat genotypes measured at four different times of
the day in the field a
R
(mg g-I)
An
(Ilmol m- 2 S-I)
g.
Cj
(mmol CO 2 mol-I air)
Chlorophyll
(mg m- 2 )
Chi a:b
(mmol m- 2 S-I)
Experiment I
Booting
Anthesis
Grain filling
LSDb
24.2
20.8
16.0
0.12
0.68
0.59
0.32
0.03
276
290
264
32
464
490
390
21
3.6
3.3
3.2
0.10
6.4
6.3
4.3
0.98
Experiment 2
Booting
Anthesis
Grain filling
LSD
20.5
19.1
18.0
0.99
0.36
0.43
0.28
0.03
240
270
251
43
513
519
425
23
3.6
3.5
3.4
0.13
10.4
9.3
5.8
1.21
a
b
Measurements were taken at three growth stages in two sowing dates (Experiment I and 2).
Least significant difference (p~0.05).
3.4. Physiological factors associated with An and
performance
loss of the cultivars was strongly associated with An
during grain filling (Fig. 3a), as well as being associated with differences in final yield (Fig. 3b).
Another trait that was sometimes associated with
performance of cultivars was Cj , the association being
apparent in the cooler of the two environments Cfable
6). Cj was also associated with gs in the cooler
environment (Table 7). A positive association of Cj
with performance and gs would indicate that differences in cultivar performance may have been partially
limited by factors relating to gas exchange.
An and gs were the only traits that, irrespective of
phenological stage, were consistently associated with
performance of these cultivars. However. chlorophyll
content measured during grain filling was associated
with performance (Table 6). Loss of chlorophyll
between anthesis and grain filling stages was apparent
in both environments (Table 5). Furthermore, regression analysis revealed that the degree of chlorophyll
Table 6
Correlation coefficients between grain yicld and physiological variables measured on 16 wheat cultivars at each development stage for two
sowing dates (Experiment I and 2) in central Mexico
An
g,
Cj
Experiment I
Booting
Anthesis
Grain filling
0.55"
0.56·
0.65"
0.82"·
0.79··
0.78··
0.62··
0.48
0.56·
0.12
0.16
0.53"
Mean
0.70""
0.88""
0.62""
0.38
Experiment 2
Booting
Anthesis
Grain filling
0.61"
0.50·
0.56·
0.63··
0.36
0.61·
0.15
0.00
0.03
-0.01
0.02
0.68··
-0.08
0.07
0.09
-0.12
0.63·
-0.12
Mean
0.64"·
0.58·
0.18
0.36
-0.01
-0.31
OverJII mean
0.73··
0.82··
0.23
0.47
-0.14
-0.38
• Correlation coefficients significant at 0.05 probability.
•• Correlation coefficients significant at 0.0 I probability.
Chlorophyll
Chi a:b
R
-0.25
0.03
0.02
0.30
-0.28
-0.29
0.09
-0.12
M.P. Reyllolds et al./Field Crops Research 66 120(0) 37-50
Fig. 2. (a) Relationship between net photosynthetic rate (An) and
grain yield. and Cb) between stomatal conductance (g,) and grain
yield. averaged over three stages of plant development and two
liOwing dates (Experiments I and 2). T1altizapan. Mexico. 19911992. C**) Significant at p~O.Ol.
Traits that indicated no apparent association with
perfonnance (Table 7) were Chi a:b. and dark respiration rate (R). Chi a:b tended to decline over the
growing cycle, while R declined substantially between
anthesis and grain filling. The average of R was 50%
greater in Experiment 2 than in Experiment I (Table
6). Average of leaf temperatures recorded during the
measurements of dark respiration for the booting.
anthesis. and grain-filling stages were 27.6. 30.2.
32.7"C in Experiment I. and 34.1. 35.8. 34.8T in
Experiment 2. respectively.
Associations between all traits (averaged across
growth stages and times) can be seen in the correlation
45
Fig. 3. Relationship of (a) net photosynthesis rate (An) and (b)
grain yield during grdin filling for 16 wheat cultivars on the change
in chlorophyll content between anthesis and grain tilling in
Experiment I. and between booting and grain filling in Experiment
2. Each point represents a cultivar and it is the average of four
~amplin!! times during the day. C*, **) significant at p~O.05 and
Cl.O I. respectively.
matrix for Experiment 1 (Table 7). The same pattern
was observed for Experiment 2 with the exception of
Cj • which was not correlated with either yield or gs.
<However. C j was negatively correlated, r=-0.58*,
with dark respiration in Experiment 2.) Average chlorophyll content was correlated with a number of traits.
There were associations with An and !:,. although these
appear to have been driven entirely by chlorosis during
grain filling (Fig. 3a) since they were not apparent at
earlier phenological stages (data not shown). Chlorophyll content was negatively associated with ChI a:b.
although this was not related to any specific phenological stage and presumably indicates that lines with
M.P. Reynolds et al./ Field Crops Research 66 (2000) 37-50
46
Table 7
Correlation coefficients between yield. biomass. net photosynthetic rate (An L stom:Jtal conductance (.li, I• .:hlorophyll cClntent (Chi). chlorophyll
a:b ratio (Chi a:bl and dark respiration (R). for 10 wheat culti\'ars using means from three stages of development. Experiment I. Tlaltizap:in.
1991-1992
Yield
Yield
Biomass
Maturity
An
g,
Cj
ChI
ChI a:b
R
1.00
0.91*'
0.42
0.70'·
0.83"
0.5S"
0.31
-0.02
om
Biomass
Maturity
An
x,
Ci
Chi
Chi a:b
R
1.00
0.55"
0.60"
0.67"
0.31
0.21
0.16
0.15
1.00
0.18
0.17
-0.17
0.10
0.26
0.26
1.00
0.86*'
0.28
0.67'
-0.32
-0.02
1.00
0.61"
0.60"
-0.41
-0.08
1.00
0.12
-0.35
-0.41
1.00
-0.67"
-O.OR
1.00
0.25
1.00
• Correlation coefficients significant at 0.05 probability.
•• Correlation coefficients significant at (Ull probability.
lower leaf nitrogen levels invested it preferentially in
reaction centers rather than light harvesting complexes.
Maturity of the cultivars did not appear to be
associated with any of the physiological parameters
(Table 7) nor with performance.
leaf temperature was 2 C higher in Experiment 2. An
measured in the afternoon (15:00-17:00 h) was lower
than that in the morning and coincided with leaf
temperatures that were 3-4 C higher. The decrease
in An' however, was most probably a result of low
levels of light (Table 4) as both An and g, respond to
lil!ht (Gerber and Dawson, 1990: Cornish et aI., 199
I:
.
Girma and Krieg, 1992). In conclusion, An appeared to
be quite stable during the day, with rates of carbon
fixation depending more on incident radiation than on
leaf temperature.
Regarding the stage of development, most of the
physiological parameters were relatively stable
between booting and anthesis. However, An' g" chlorophyll content. Chi a:b. and R. all declined some
between anthesis and grain filling (Table 5). C by
contrast remained relatively stable across developmental stage~ (Table 5). An was an exception. It
declined moderately between booting and anthesis
(Table .3) in a manner consistent with data coJJected
in a temperate environment, where An of wheat cuJtivars declined between booting and early grain filling
(Fischer et al.. 1998).
This study was conducted with sowing dates
approximately 3 months apart in order to collect data
in two distinct thermal environments (Table 1), both of
which are considcn:d supraoptimal with respect to
temperature. Generally speaking the physiological
parameters measured were very similar for the two
environments. with the exception of R which was
approximately SOlie higher in the warmer environment
~
4. Discussion
4. t. Effect of time of da)~ phenology, and
environment on An
While the cultivars differed in All' there was no
interaction with time of day or environment although
the differences between cultivars in An tended to
increase with phenological stage. Therefore, the main
effect of cultivars can be used to interpreted the
influence of other factors on An.
An appeared [Q be relatively stable with respect to
the time of day when light levels were approaching
saturating. Light levels in aJJ measurements taken in
Experiment I (>1300 J,lmol m- 2 S-I) were close to
saturating photosynthetic capacity in wheat
(1500 Ilmol m- 2 S-I) (Blum, 199m. Mean leaf temperature became progressively higher between 10:(X)
and 14:00 h, but this did not apparently affect An
(Table 4). In Experiment 2, measurements were also
made later into the afternoon (15:00-17:00 h). An
measured in the morning did not differ !!reatly
between experiments. despite the fact that the mean
..
M.P. Reynolds et al.fField Crops Research M (2000) 37-50
(Experiment 2. Table 5). Yields and biomass were
approximately 40c;o lower in Experiment 2 compared
with Experiment 1. Given that An did not vary. the
difference in productivity may be explained partly by
the fact that the crop duration averaged only 80 days
(versus 100 days for Experiment 1). and partly
because of increased rates of dark respiration observed
in Experiment 2. The idea that dark respiration may
use up a substantial proportion of the fixed carbon
throughout the crop cycle is supported by other studies
with wheat (Mitchell et aI., 1991).
4.2. Differential response of cultivars to wann
environments
The differential response of cultivars to the experimental environments was quite complex. In the earlier
development stages (i.e. booting and anthesis) cultivar
differences in Anwere independent of differences in
chlorophyll content. Furthermore, An was associated
with grain yield while chlorophyll content was not
(Table 6). In the grain-filling stage, however, differences in An were associated with both chlorophyll
content (Table 3) and chlorosis (Fig. 3a). and both An
and chlorophyll content were strongly associated with
yield (Table 6). These data inferred that differential
performance of cultivars was associated with both
intrinsic differences in An. as well as with differences
in photosynthetic capacity that were determined by
chlorosis during grain filling. While there was a preferential decline in chlorophyll a over chlorophyll b. as
evidenced by the decline in a:b ratio oyer time (Table
5). the value of the a:b ratio itself was not correlated
with yield of the cultivars (Table 6). Further support
for the idea that one of the causal mechanism of heat
sensitivity was accelerated senescence and an associated loss of chlorophyll carne from the apparent
interaction between cultivars and growth stages for An.
When An for cultivars at each stage of development
was plotted against the mean An over all three stages of
development. the gradient of the fitted slope became
steeper at successive growth stages (Fig. I). The
increase in slope indicated that the more heat sensitive
cultivars become progressively less capable of An over
time in comparison with the more heal tolerant lines.
It is worth pointing out that this latter phenomenon
cannot be explained simply in terms of differences in
. maturity among cultivars. While differences in matur-
47
ity were a potentially confounding factor, maturity
was not significantly associated with An or chlorophyll
content during grain filling. nor with yield performance. Furthermore. while several early-maturing
lines were lower yielding and had low An or chlorophyll content during grain filling, there were also late
cultivars that had similarly low values. as well as early
cultivars that had high values for the same traits (Table
3).
In controlled environments, differences in photosynthetic rate at high temperatures have been reported
for wheat (Blum, 1986; Al- Khatib and Paulsen, 1990),
as well as in other species including cotton (Wells et
aI., 1986). potato (Reynolds et aI., 1990). and rice
(Sasaki and Ishii. 1992). Midmore et a1. (1982)
reported that the main effect of high temperature on
wheat is to accelerate phenological development,
which seems to be associated with premature leaf
senescence (AI-Khatib and Paulsen, 1984; Harding
et al.. 19'JO). The present data confirm the role of
premature leaf senescence as a mechanism associated
with gen~tic differences in heat sensitivity but also
indicate that intrinsic differences in An may playa role
in deternlining performance under high temperature.
The differential response of stomatal conductance
of thes~ cultivars illustrated a similar pattern to that of
An (Fig. :!b. Tables 5-7). This result is consistent with
data of Cornish et a1. (1991) who reported that in
cotton th~ highest yielding cultivars in their study had
higher An and greater ~s' The positive correlation
between .\:, and grain yield was to be expected considering that this variable is closely linked to An
(Cornish et aI.. 1991). In the present study. the correlation lx·tween g, and performance was higher than
with An. Evaporative cooling associated with gs may
be an additional mechanism conferring heat tolerance
through heat escape. In parallel studies. canopy temperatures were measured on the same 16 cultivars used
for this study. Cooler canopies measured during booting. anthesis and grain fil~ing were associated with
better performance of cultivars. and canopy temperature depression was highly correlated with gs (Amani
et a1.. 1996). A negative correlation between leaf
temperature and Rs was found in cotton cultivars with
different levels of productivity indicating that cultivars
bred for increased yield had greater gs and maintain
lower kaf temperatures than older lines (Cornish
et a1.. 1991).
·.
48
M.P. Reynolds et ul. / Field Crops Research 66 (2000) 37-50
Dark respiration rates of flag leaves did not help to
explain differences in cultivar performance. It is possible that grain respiration has a more important effect
on grain dry weight reduction (Wardlaw et aI.. 1980).
than dark respiration rates of leaves.
4.3. Factors detennining genetic differences in All
and its association with performance
It is interesting that measurements of An revealed
good association with yield in this study, given that
there are many reasons why high An measured on flag
leaves would not necessarily be expected to be associated with better performance. In the first case, An
represents the performance of a single light-saturated
leaf. while crop assimilation rate is a function of the
combined photosynthesis of all of leaves in the
canopy, few of which are ever light-saturated (Nelson.
1988). Most leaves are displayed obliquely to sun and
there are usually acclimation changes in the composition of the photosynthetic apparatus at different positions in the canopy (Evans, 1993). Secondly, increased
An will not improve yield if yield is not primarily
assimilate limited.
The demonstration in this study of an association
between yield and An may be related to the experimental environment. Higher An may have a greater
impact on performance in warm environments in
comparison with temperate ones because leaves are
exposed to direct radiation for longer time and because
grain yield is more assimilate limited. as mentioned in
the introduction. In the present study, radiation levels
were approaching that necessary to saturate the photosynthetic apparatus. i.e. 1500 }lmol m-- 2 S- I, and the
results are in agreement with data from a high-radiation environment in Israel where cultivar improvement, between 1968 and 1986 appeared to be
associated with higher An (Blum, 1990). While other
studies have shown an association of An with yield of
different wheat cultivars in temperate environments
(Shimshi and Ephrat. 1975; Fischer et aI., 1998). that
relationship, at least in the latter study. appears to have
been driven by high partitioning of assimilates to yield
during grain filling since crop biomass was not associated with An nor with yield. In our study. the
association between An and yield was consistent with
a significant association of biomass with An (r=O.60).
and of biomass with yield (r=O.91). In other words.
this study provides evidence for an association
between increased flag leaf An and improved radiation-use efficiency of cultivars.
Although differences in An during grain filling were
obviously associated with chlorosis, this study did not
elucidate the physiological basis for the observed
differences in An at earlier development stages. During
booting. An values of the cultivars ranged from 21 to
27 }lmol m- 2 S-I. Net photosynthetic rate is determined by the difference between gross carbon fixation
and carbon respired through dark respiration and
photorespiration (Loomis and Amthor, 1999). Therefore, genetic variability in any of these processes could
contribute to differences in An. In this study. cultivar
differences in dark respiration measured during the
afternoon were apparently not associated with An·
Gross photosynthetic rate may vary at a given light
intensity and chlorophyll density if there are differences in photoinhibition or down regulation of the
photosynthetic apparatus and several mechanisms
may be involved (Bjorkman and Demmig-Adams,
1994). any of which could, in theory, involve genetic
variability and result in cultivar differences in gross
photosynthetic rate. The only mechanism for ~hich
genetic diversity has been observed in these cultivars
that may help to determine genetic differences in An
(via an effect on photoinhibition, rates of dark repiration, or photorespiration) are the small differences in
operating temperatures detected using IR thermometry (Amani et aI., 1996).
5. Conclusions
With reference to the stated objectives of the study:
(i) determine genetic differences in All' of cuItivars.. 0'
(ii) observe whether An of cultivars interacted with
time of day, phenological stage, and environment, (iii)
compare An and related parameters with agronomic
performance; the data demonstrated clear differences
in An among cultivars, the differences were consistent
across time of measurement, phenological stage. and
environment, and revealed a significant association
with field performance, (iv) add to understanding of
the physiological mechanisms underlying genetic
diversity for heat tolerance in wheat; differences in
An and g, at all growth stages were associated with
culti\'ar differences in performance in warm condi-
M.P. Reynolds eT al./Field Cmps Research 66 (2000) 37-50
tions. the latter (gs) possibly having a role in heat
escape: in addition. the role of chlorosis as a determinant in heat tolerance was confirmed.
Acknowledgements
The authors wish to express thanks to Dr. Gregory
Edmeades (formerly CIMMYT maize physiologist)
for his critical comments to the manuscript.
References
AI-Khatib. K.. Paulsen. G.M .. 1984. Mode of high temperature
injury to wheat during grain development. Physiol. Plant 61.
363-368.
AI-Khatib. K.. Paulsen. G.M .• 1990. Photosynth.:sis and productivity during high temperature stress of wheat cultivars from
major world regions. Crop Sci. 30. 1127-1132.
Amani. I.. Fischer. R.A.• Reynolds. M.P.. 1996. Canopy temperature depression associated with yield of irrigated spring wheat
cultivars in a hot climate. J. Agron. Crop Sci. 176. 119-129.
Amthor. J.S.. 1989. Respiration and Crop Productivity. Springer.
New York.
Austin. R.B .. Morgan. C.L.. Ford. M.A.. Bhagwat. S.G .. 1982. Flag
leaf photosynthesis of Triticum ae.l·tivl/lll and related diploid
and tetraploid species. Ann. Bot. 49. 177-189.
Berry. J.. Bjorkman, 0.. 1980. Photosynthetic response and
adaptation to temperature in higher plants. Ann. Rev. Plant
Physiol. 31, 491-543.
Bjorkman. 0 .. Demmig-Adams. B.. 1994. Regulation of photosynthetic light energy capture. conversion. and dissipation in
leaves of higher plants. In: Schulze, E.-D.. CaldwelL M.M.
(Eds.). Ecophysiology of Photosynthesis. Eco!. Studies 100.
Springer. Berlin, pp. 17-70.
Blum. A.. J 986. The effect of heat stress on wheat leaf and ear
photosynthesis. J. Exp. Bot. 37. 111-118.
Blum. A.. 1990. Variation among wheat cultivaro; in the respons~ of
leaf gas exchange to light. J. Agric. Sci. 115.305-31 I.
Calderini. D.F.. Dreccer. M.F.. Slafer. G.A.. 1995. Genetic
improvement in wheat yield and associated traits. A reexamination of previous results and the latest trends. Plant
Breeding 114. 108-112.
Charks-Edwards. D.A.. 1978. An analysis of the photosynthesis
and productivity of vegetative crops in the United Kingdom.
Ann. Bot. 42. 717-73 I.
Cornish. K.. Radin. J.w.. Turcotte. E.L.. Lu. Z.-M .. Zeiger. E..
1991. Enhanced photosynthesis and Ii, of pima cotton
(Go.uypil/l11 harhadense L.) bred for incre'lsed yield. Plant
Physiol. 97. 4H4-489.
Decker. J.P.. 1955. A rapid post illumination deceleration of
respiration in green leaves. Plant Physiol. 3ll. H2-H4.
Evans. J.R.. 11)l)3. Photosynthetic acclimation and nitrogen
49
partitioning within a lucerne canopy. 1. Canopy characteristics.
Aust. J. Plant PhysioL 20. 55-67.
Fischer. R.A. Rees. D.. Sayre. K.D.. Lu. Z.-M., Condon. AG.,
Larque-Saavedra. A.. 1998. Wheat yield progress associated
with higher stomatal conductance and photosynthetic rate. and
cooler canopies. Crop Sci. 38, 1467-1475.
Gent. M.P.N.. Kiyomoto. R.K.• 1985. Comparison of canopy and
flag leaf net carbon dioxide exchange of 1920 and 1977 New
York winter wheats. Crop Sci. 25. 81-86.
Gerber, M.A.. Dawson. T.E.. 1990. Genetic variation between leaf
gas exchange. morphology. and development in Polygonum
arenastrtllll. Oecologia 85. 153-158.
Girma, F.S.. Krieg. D.R.. 1992. Osmotic adjustment in sorghum. II.
Relationship to gas exchange rates. Plant Physiol. 99. 583-588.
Gutierrez-Rodriguez. M., Reynolds. M.P.. Larque-Saavedra. A.•
2000. Photosynthesis of wheat in a warm, irrigated environment. II: Traits associated with genetic gains in yield. Field
Crop Res. 66. 51-62.
Harborne. J.B .. 1973. Phytochemical Methods. A Guide to Modem
Techniques of Plant Analysis. Chapman & HaIL Fakentham.
Norfolk. UK. pp. 204-208.
Harding. S.A.. Guikema. J.A. Paulsen. G.M.. 1990. Photosynthetic
decline from high temperature stress during maturation of
wheat. 1. Interaction with senescence process. Plant Physiol. 92.
648-653.
Harrison. S.A.. Boerma. H.R.. Ashley. D.A.. 1981. Heritability of
canopy apparent photosynthesis and its relationship to seed
yield in soybeans. Crop Sci. 21. 2:2-226.
Loomis. R.S.. Amthor. J.S.. 1996. Limits to yield revisited. In:
Reynolds. M.P.. Rajaram, S.. McNab. A. (Eds.). Increasing
Yield Potential in Wheat: Breaking the Barriers. CIMMYT.
Mexico. OF.
Loomis, R.S.. Amthor. J.S.• 1999. 'Yield potential. plant assimilatory capacity and metabolic efficiencies. Crop Sci. 39. 15841596.
McCree. KJ.. 1971. The action spectrum. absorptance and
quantum yield of photosynthesis in crop plants. Agric.
Meteoro!' 9. 191-216.
Midmore. DJ .. Canwright. P.M .. Fischer. R.A.. 1982. Wheat in
tropical environments. 1. Phasic development and spike size.
Field Crops Res. 5. IH5-200.
Mitchell. A.C.. Lawlor. D.W.. Young. A.T.. 1991. Dark respiration
of wintl'r wheat crops in relation to temperature and simulated
photosynthesis. Ann. Bot. 67. 7-16.
Nelson. c.J.. 1988. Genetic associations between photosynthetic
characteristics and yield: review of the evidence. Plant Physiol.
Biochem. 16. 543-554.
Puckridge. D.W.. 1971. Photosynthesis of wheat under field
conditions. Ill. Seasonal trends in carbon dioxide uptake of
crop communities. Aus!. J. Agric. Res. 22. 1-9.
Rawson. H.N .. 1986. High temperature-tolerant whcal: a description or variation and a search for some limitations to
producti\ity. Field Crops Res. 14. 197-211.
Reynolds. !\t.P.. Balota. M.. Delgado. M.I.B .. Amani. L Fischer.
R.A.. 1994. Physiological and morphological traits associated
with spring wheat yield under hot. irrigated conditions. Aust. J.
Plant Physiol. 2 I. 717-73ll.
I.
.~
50
M.P Reynolds et al.fField Crops Research 66 (2000) 37-50
Reynolds. M.P.. Ewing. E.E.• Owens. T.G.. 1990. Photosynthesis at
high temperature in tuber-bearing solal/llm species: a comparison between accessions of contrasting heat tolerance. Plant
Physio!. 93. 792-797.
Reynolds. M.P., Singh. R.P., Ibrahim. A., Ageeb. O.A.A.. LarqueSaavedra, A.. Quick. J.S., 1998. Evaluating physiological traits
to complement empirical selection for wheat in warm
environments. Euphytica 100. 85-94.
Sasaki. H., Ishii., R.• 1992. Cultivar differences in leaf photosynthesis of rice bred in Japan. Photosynth. Res. 32, 139-146.
Sayre. K.D., Rajararn. S.• Fischer. R.A.. 1997. Yield potential
progress in short bread wheats in Northwest Mexico. Crop Sci.
37.36-42.
Shimshi, D.• Ephrat. J., 1975. Stomatal behaviour of wheat
cultivars in relation to their transpiration. photosynthesis and
yield. Agron. 1 67. 326-331.
Wardlaw. J .F.. Sofield. I.. Cartwright. P.M.• 1980. Factors limiting
the rate of dry matter accumulation in the grain of wheat grown
at high temperature. Aust. J. Plant Physio!. 7. 387-400.
Wells. R.. Meredith. W.R.. Williford. J.R.• 1986. Canopy photosynthesis and its relationship to plant productivity in near-isogenic
cotton lines differing in leaf morphology. Plant Physio!. 82.
635-640.
Wells. R.. Schulze. L.L.. Ashley. D.A.. Boerma. H.R.. Brown. R.H.•
1982. Cultivar differences in canopy apparent photosynthesis and
theirrel3tionship to seed yield in soybeans. Crop Sci. 22, 886-890.
Zadoks. le.. Chang. T.T.. Konzak. C.E. 1974. A decimal code for
the growth stages of cereals. Weed Res. 14. 415-421.