Published May 3, 2018

Crop Ecology and Physiology

Acute High Temperature Response in Wheat

James G. Nuttall,* Kirsten M. Barlow, Audrey J. Delahunty, Brendan P. Christy, and Garry J. O’Leary

H
Abstract igh temperatures for short periods (acute heat
stress as heat waves) have the potential to significantly
Heat waves have a significant impact on crop production and qual-
reduce grain production and quality of arable cropping
ity of many staple grains including wheat. Under climate change,
systems. Along with expected global increases in atmospheric
changing weather patterns including greater temperature volatility
CO2 concentration and average ambient temperature, due to
are also likely to further affect yield stability. Simulation modeling
climate change, there will be an increase in the frequency of heat
provides a powerful tool to investigate the interactive effects of abi-
waves combined with increasingly severe terminal drought for
otic factors and develop adaptive strategies; however, many of these
many cropping regions (IPCC, 2012). Wheat (Triticum aestivum
models do not adequately account for the step change response to
L.) is a significant staple grain with worldwide production of
high temperature occurring during the crop reproductive phase.
672 million tonnes in 2012 (FAOSTAT, 2014) and providing
Empirical response data will support the development of robust
an important source of human nutrition. Sustaining produc-
algorithms for crop models. We present results from three experi-
tion into the future requires the ongoing adaption of cropping
ments on the response of wheat to a range of acute high-tempera-
systems through breeding and appropriate agronomic strategies
ture treatments. For 35, 37, and 42°C and 1, 3, and 5 d of exposure
which limit the impact of abiotic stresses including high-temper-
(~6 h d–1), expressed as heat sum, °C×h (above 32°C), high tem-
ature effects. In the development of adaptive management strate-
perature applied 5 d prior to anthesis reduced grain number and
gies, simulation modeling provides a powerful tool to investigate
yield by 0.16 and 0.15% per °C×h respectively, whereas individual
the effects of climate and weather variability on wheat produc-
grain weight and grain nitrogen concentration increased by 0.03
tion (Semenov and Porter, 1995; Wang et al., 2017), where those
and 0.06% per °C×h, respectively. For high temperature applied
insights are possible due to the mechanistic nature of biophysical
after anthesis, individual grain weight decreased by 0.05% per
models (Jamieson and Semenov, 2000). Currently, however, few
°C×h, grain nitrogen concentration increased by 0.03% per °C×h,
crop models adequately account for the response of wheat to
and yield was reduced by 0.07% per °C×h. The often asymptotic
high temperature as heat wave conditions during the reproduc-
response meant exponential functions provided a superior fit.
tive and grain filling phase (Barlow et al., 2015). Consequently
Water availability prior to anthesis attenuated wheat response to
there is a need for algorithms which describe the crop response to
high temperature. Such algorithms could contribute to improv-
such high temperature (Barlow et al., 2015; Zheng et al., 2012),
ing our prediction of the step change response of wheat to high
with an emphasis on response during the reproductive and grain
temperature within crop models and more broadly contribute to
filling phases (Sánchez et al., 2014).
developing strategies for crop adaptation to climate change using a
Wheat production is affected by high temperatures through
modeling approach.
the plants response to both (i) above-optimum temperatures for
an extended period (Fischer, 1985), or (ii) heat-shock response
Core Ideas which is triggered by a few days of extremely high air tem-
• Heat waves can significantly reduce wheat production and quality in peratures, particularly during the reproductive phase (>32°C)
arable cropping regions. (Blumenthal et al., 1994; Stone and Nicolas, 1994; Wardlaw and
• Modeling could aid the development of adaptive strategies to cli- Wrigley, 1994). The optimum temperature for grain develop-
mate and weather variables. ment ranges from 12 to 22°C (Farooq et al., 2011) and although
• Further model refinement for step-change response of wheat to high increasing temperature and photosynthesis boosts supply of
temperature is required.
assimilates, this may not fully compensate for shortened dura-
• High temperature applied 5 days prior to anthesis reduced grain set
tion of starch deposition, where generally higher temperature
by 0.16% per °C×h (>32°C).
produces smaller grains and limits yield (Andrew, 1987; Spiertz
• High temperature applied after anthesis reduced individual grain
weight by 0.05% per °C×h (>32°C).

J.G. Nuttall, A.J. Delahunty, G.J. O’Leary, Agriculture Victoria,

Published in Agron. J. 110:1296–1308 (2018)
doi:10.2134/agronj2017.07.0392
Available freely online through the author-supported open access option
Copyright © 2018 by the American Society of Agronomy
5585 Guilford Road, Madison, WI 53711 USA
This is an open access article distributed under the CC BY license
(https://creativecommons.org/licenses/by/4.0/)
Dep. of Economic Development, Jobs, Transport and Resources, 110
Natimuk Road, Horsham, Victoria, 3400, Australia; K.M. Barlow,
B.P. Christy, Agriculture Victoria, Dep. of Economic Development,
Jobs, Transport and Resources, 124 Chiltern Valley Road, Rutherglen,
Victoria, 3685, Australia; A.J. Delahunty, Univ. of Melbourne,
Parkville, Victoria, 3000, Australia. Received 13 July 2017. Accepted 8
Mar. 2018. *Corresponding author (James.Nuttall@ecodev.vic.gov.au).
Abbreviations: DAA, days after anthesis.

1296 A g ro n o my J o u r n a l   •  Vo l u m e 110 , I s s u e 4  •  2 018

et al., 2006). For wheat exposed to very high temperature the
response includes accelerated senescence, decreased chlorophyll
of leaves, lower CO2 assimilation, and increased photorespira-
tion (Farooq et al., 2011). Grain set and/or small shrunken
grains can also result, depending on timing of the stress relative
to grain development (Tashiro and Wardlaw, 1990).
The response of wheat to very high temperatures (>32°C)
around anthesis can induce a non-recoverable reduction in yield
by adversely effecting ovary development as well as pollen and
floret viability, reducing grain set (Pradhan et al., 2012). Reduced
grain number may only be partially compensated by increased
grain filling due to proportionally greater allocation of assimilate
to the remaining kernels (Jenner et al., 1991). For wheat, grain set
was most severely affected 2 d prior to anthesis, inducing 55% ste-
rility of floret basal (a) grains when exposed to 36°C for 2 d, but
less sensitive 2 d after anthesis (Tashiro and Wardlaw, 1990) and
largely unaffected 10 to 30 d after anthesis (Stone and Nicolas,
1994). For a single day of high temperature (35°C) at anthesis,
grain number and yield were reduced by up to 33 and 35% respec-
tively, where there was also significant variation in response across
the range of cultivars tested (Talukder et al., 2014).
Short-term very high temperature (>32°C) occurring after
anthesis produces grains that are small and shrunken. This is
due to a reduction in starch synthesis and translocation to the
developing grain (Jenner et al., 1991) and overall reduced rate
and duration of grain filling (Lobell et al., 2012; Stone and
Nicolas, 1995a). This reduction in individual grain weight and
damaged grains due to high temperature has been observed to
occur as early as 2 to 10 d after anthesis (Tashiro and Wardlaw,
1990). For individual grain weight, important factors to cap-
ture in terms of the effects of high temperature throughout the
grain filling phase are rate and duration (Ugarte et al., 2007).
The pattern of response to elevated temperature also varies
across genotypes, beyond thermal time effects (Stone and Nicolas,
1995a) which provides insight to account for genetic effects in
modeling high-temperature response. High-temperature stress
during grain filling is also observed to increase nitrogen concen-
tration (Stone and Nicolas, 1995a), where the resultant nitrogen
accumulation is less sensitive than that of starch. Irrespective,
heat-shock response induced by acute high temperature, alters the
composition of protein and starch within the grain (Wardlaw and
Wrigley, 1994), and adversely affects end-use properties such as
dough strength, extensibility and loaf volume (Blumenthal et al.,
1993; Farooq et al., 2011; Jenner, 1994).
Crop biophysical models can be of benefit in investigating
crop adaptation strategies in the context of the complex interac-
tions between broad scale feedbacks between climate change,
increasing weather variability, and agricultural systems at a
regional level (Wang et al., 2017). However, model mechanistic
processes need to reflect the response of plants to the key abiotic
stresses linked with climate change drivers such as (i) elevated
atmospheric CO2 , (ii) changes in seasonal water availability,
(iii) above-optimum (chronic) temperature for an extended
period, and (iv) extremely high temperature (>32°C) for short
periods (heat wave). Most contemporary models used through-
out the world can adequately account for the first three factors;
however, fewer consider the step change response in wheat
yield potential associated with very high temperature response
Agronomy Journal   •   Volume 110, Issue 4  •  2018 1297
occurring during the reproductive and grain filling phase
(Barlow et al., 2015).
Modeling high-temperature response requires the feedback
effects of a range of physiological process in simulating yield
response. These processes include: (i) reduced grain number in
response to sterility and abortion of grains (ii) reduced duration
of grain filling, (iii) accelerated senescence, and (iv) reduced grain
growth rate. A recent review of crop models and extreme temper-
ature effects, identified the need for improved sub-routines which
describe these processes (Barlow et al., 2015). Model comparison
studies under a range of climate scenarios will also provide util-
ity for crop yield projections (Zheng et al., 2012). Sánchez et al.
(2014) highlights the need to improve the response functions
for extreme temperatures, with a priority on the response during
anthesis and grain filling. Currently crop models are evolving to
accommodate the nonlinear response to temperature (Asseng et
al., 2011; Wang et al., 2017) and the step reduction in grain num-
ber associated with a short periods (1–2 d) of heat or cold shock
(Challinor et al., 2005; Maiorano et al., 2017). From a modeling
perspective, separating the direct environmental effects on grain
set and sterility (e.g., pollen viability) from indirect effects within
the plant (e.g., grain growth rate) should contribute to the devel-
opment of more robust mechanistic models (O’Leary, 1983).
The objective of this study was to define the response of
wheat to a range of high-temperature treatments which reflect
extreme (heat wave) conditions (>32°C), imposed during the
reproductive and grain filling phases, where the results of three
controlled environment experiments are presented. Specifically,
the objective of the first experiment was to define the main and
interactive effects of timing, duration and intensity on crop
response and test the degree of step change response which
occurs in yield potential. The objective of the second experi-
ment was to determine the cumulative effects of multiple high-
temperature events during the early grain-filling phase and test
if the impact to crop is additive and at what point the response
reaches a plateau. For the third experiment, the interaction of
high temperature with crop water supply was tested to deter-
mine if limiting water compounds high-temperature effects.
Materials and methods
The experimental work was conducted in naturally lit,
controlled environments at Horsham, Victoria, Australia
(36°43ʹ18.6˝ S, 142°10ʹ26.8˝ E; 128 m a.s.l.). A range of simu-
lated high-temperature treatments were applied to wheat dur-
ing the reproductive and grain-filling phase, and the effects
of timing, temperature and duration of heat, as well as water
availability, were investigated through three separate experi-
ments: (i) Anthesis high temperature, (ii) Cumulative high
temperature events, and (iii) Water supply and high-temperature
interactions.
Experimental Design
Experiment 1. Anthesis High Temperature
Wheat (Triticum aestivum ‘Yitpi’), an Australian commercial
cultivar, was sown on 30 July 2012 in a polyhouse environ-
ment (95% photosynthetic active radiation [PAR] transmis-
sion) within square pots (160 mm width, 160 mm depth, 240
mm height) containing generic potting mix packed to a bulk
density of 0.7 Mg m–3. Prior to sowing, basal nutrients were
applied to the potting mix in a batch mixing process where
each pot received a basal application of 2.7, 0.72, 1.5, 0.36,
and 0.006 g pot–1 of N, P, K, S and Zn, respectively, using a
combination of Osmocote controlled release fertilizer and
trace element fertilizer, incorporated throughout the media.
Lime was also added to balance the growth media pH to mildly
alkaline conditions. Six wheat seeds were planted per pot in
a single ring and thinned to four plants at the 3-leaf stage to
provide equivalent plant density and vigor across pots. High-
density polyethylene granules were placed on the soil surface, at
the thinning stage, to minimize variation in evaporative losses
due to differences in crop canopy cover across treatments. Pots
were watered using metered amounts of reverse osmosis water
at regular intervals (every 2 to 3 d) to maintain a moist grow-
ing medium where pots were free-draining. Watering during
the heat-treatment phases occurred daily prior to plants being
exposed to heat to limit confounding effects of plant water
stress.
High-temperature treatments were applied at three growth
stages, 5 d prior to anthesis and 5 and 15 d after anthesis
(−5 DAA, 5 DAA and 15 DAA, respectively), using mobile heat
chambers installed within the polyhouse. At these times, the
duration of heat treatments were 1, 3 and 5 d (centered on the
target growth stage) with target high temperatures of 35, 37, and
42°C respectively and a control of ambient polyhouse conditions
which was <32°C. The wheat plants reached 50% anthesis (Z65)
(Zadoks, Chang et al., 1974) on the 30 Oct. 2012 and accord-
ingly heat treatment were applied, centered on the 25 Oct. 2012,
4 Nov. 2012 and 14 Nov. 2012 which corresponded to −5 DAA,
5 DAA and 15 DAA. Collectively there were 36 treatment com-
binations (4 temperatures × 3 crop periods × 3 durations) and
four replicates of each combination, with pots organized within
the polyhouse environment in a randomized complete block
design. Wheat was harvested on the 18 Dec. 2012 (141 d after
sowing), with four plants harvested per pot for all treatments and
replicates.
Experiment 2. Cumulative High-Temperature Events
Wheat (Triticum aestivum ‘Yitpi’) was sown on 2 Sept. 2013
in a glasshouse environment with an establishment set up
equivalent to that of Exp. 1. In contrast, five wheat seeds were
planted per pot in a single ring and thinned to three plants at
the 3-leaf stage to obtain equivalent plant density and vigor
across pots. Prior to applied heat treatment, pots were watered
to limit water stress during the high-temperature period and
the confounding effects of drought stress. Treatment design
was two high temperatures treatments (35 and 38°C) where
pots were transferred to a growth chamber and a control main-
tained at ambient air temperature within the glasshouse. The
duration of heat treatment ranged from 1 to 13 d with heat
applied every second day starting from 1 d postanthesis (Z65)
over a period of 26 d. Collectively there were 20 treatment
combinations (2 temperatures × 10 time durations) and four
replicates for each combination where pots were organized in a
randomized complete block design. For the high-temperature
treatments, plants were periodically transferred from the
glasshouse to a growth cabinet where the 35 and 38°C treat-
ments commenced on 14 and 15 Nov. 2013, respectively. The
growth cabinet (Thermoline Scientific) controlled humidity
1298 Agronomy Journal   •  Volume 110, Issue 4  •  2018
and lighting by a combination of incandescent and high pres-
sure sodium lamps, where PAR was 800 to 1000 μmol m–2
s–1 which was comparable light intensity to the glasshouse
environment. Wheat was harvested on 2 Jan. 2014 (122 d after
sowing); three plants were harvested per pot for all treatments
and replicates.
Experiment 3. Water Supply and High-
Temperature Interactions
Wheat (Triticum aestivum ‘Yitpi’) was sown on 4 June 2014
in a medium clay soil in a glasshouse environment. Soil was
collected from the 5- to 15-cm layer of a gray Vertosol soil,
air-dried (40°C for 4 d) and passed through a 5-mm sieve.
Soil was packed in large sealed square pots (160 mm width,
160 mm depth, 240 mm height) with 5500 g of soil per pot,
which equated to a bulk density of 0.95 Mg m–3. The large
pot size was used to limit the artifact effects of pot volume on
treatment response (Bourgault et al., 2017). The field capac-
ity (–30 kPa) and wilting point (–1500 kPa) of the soil was
0.44 and 0.23 Mg m–3 respectively, where field capacity was
determined using a sintered glass filter funnel under a 30 kPa
suction (Passioura, 2006) and wilting point using pressure plate
apparatus. Pots were pre-watered to weight to the equivalent of
0.35 Mg m–3 water content and each pot received a basal appli-
cation of 0.15 and 0.07 g pot–1 of N and P, respectively, through
a combination of Mallee Mix 1 and urea. Six wheat seeds were
planted per pot in a single ring and thinned to four plants at
the 3-leaf stage to obtain equivalent plant density and vigor
across pots. High-density polyethylene granules were placed on
the soil surface, at the thinning stage, to minimize variation in
evaporative losses due to differences in crop canopy cover across
treatments.
For water treatments, the experiment tested four factorial
combinations of high water and low water imposed during the
preanthesis and postanthesis growing periods. High-water and
low-water treatments equated to water contents of 0.35 (57%
relative available water) and 0.29 Mg m–3 (29% relative avail-
able water), respectively, and were maintained by watering to
weight to limit the risk of hypoxia. Reverse osmosis water for
irrigation was stored in a tank at equilibrium with the glass-
house temperature to reduce temperature differential with
soil and impact on roots (Passioura, 2006). High-temperature
treatments (ambient and 38°C) were applied at two growth
stages: 5 d preanthesis and 15 d postanthesis (−5 DAA and 15
DAA, respectively) commencing on 23 Sept. and 13 Oct. 2014,
respectively. At these times, the duration of heat treatments
were 3 d (centered on the target growth stage). Wheat reached
50% anthesis (Z65) on 28 Sept. 2014 (116 d after sowing) at
which time water regimes were split to reflect the four possible
water treatment combinations. Wheat reached physiological
maturity on 10 Nov. 2014 (159 d after sowing).
Application of Heat Treatments
For all three experiments, temperature and relative humidity
were logged at 6-min (Exp. 1) and 5-min (Exp. 2 and 3) intervals
using a combination of TinyTag Ultra 2 sensors (TGU-4017,
temperature; TGU-4500, temperature and relative humid-
ity). The sensors were positioned at the head height of main
stems within the wheat plants. The ambient temperatures of
the various growing environments were also recorded to define
conditions outside the high-temperature treatment periods.
Experiment 1. Anthesis High Temperature
Mobile heat chambers were used to induce the heat treat-
ments and consisted of right-angle hollow section frame boxes
(1200 mm width, 800 mm depth, 500 mm height) that were clad
with Sun Tuff Greca Laserlite. Electric fan heaters (1000 W) were
mounted at the top of the chambers with the temperature con-
trolled by a thermocouple mounted at the height of the main stem
spikes which controlled heater elements and fan was continuously
running at constant speed. Heat was applied by removing the
pots from their randomized design to heat chambers for 1, 3, or
5 d. The application of heat commenced at 9:00 AM and reached
the target temperature, either 35, 37 or 42°C, by 10:00 AM; this
was maintained for a 6-h period each day. Relative humidity was
not controlled during the high-temperature treatments, but was
measured as between 20 and 25%. An ambient (control group)
was put in a blank heat chamber without applying heat and the
temperature rarely exceeded 32°C. The design of the chamber
allowed the pots to remain at ambient air temperatures of the
polyhouse, while the high-temperature conditions were imposed
to the reproductive component of the wheat. This design limited
the impact of elevated root temperatures on early senescence
and cessation of grain development (Kuroyanagi and Paulsen,
1988). After the high-temperature treatment, the chambers were
allowed to return to ambient temperature and the overnight
night temperature (12°C) matched that of the open-air polyhouse
(ambient night temperature). When heat treatments were com-
pleted, pots were returned to their randomized design within the
open-air polyhouse, this process being staggered depending on
the duration of heat exposure. During the growing period, aver-
age minimum and maximum temperatures in the polyhouse were
8 and 22°C, respectively, in the preanthesis period and increased
to 12 and 30°C, respectively, postanthesis. Within this environ-
ment, PAR was 860 μmol m–2 s–1, and relative humidity across
day and night ranged from 40 to 95% in the preanthesis period
and from 25 to 80% in the postanthesis period.
Experiment 2. Cumulative High-Temperature Events
Commencing at 50% anthesis, wheat was exposed to a range
of cumulative high-temperature treatments of 1, 2, 3, 4, 6, 8,
10, 12, and 14 d using a growth chamber. Between progressive
cumulative-heat episodes, plants were returned to the glasshouse
environment and rested for 1 d and watered ahead of sequential
episodes. Cumulative heat treatments spanned from 1 to 28 d
after anthesis. Episodes constituted one of two high-tempera-
ture treatments, both having elevated temperatures lasting 6 h
per day. The first regime was a day/night cycle of 35:15°C with
the temperature transition occurring over 3 h at the rate of
6.3°C h–1; the second regime was a day/night cycle of 38:15°C
with the temperature transition occurring over 3 h at the rate of
7.3°C h–1. High-temperature treatments within the Thermoline
Scientific growth chamber commenced at 9:00 AM. Lights were
run for 14 h per day to reflect local daylength and were switched
on at 6:00 AM. Relative humidity was regulated by the growth
chamber, and set to 20 and 60% for the day and night cycles,
respectively. Although soil within the pots was covered with
reflective granules to reduce heating effects, pots within the
Agronomy Journal   •   Volume 110, Issue 4  •  2018 1299
growth chamber were generally 8°C warmer than the ambient
controls, which is likely to exacerbate the high-temperature
response of wheat (Kuroyanagi and Paulsen, 1988).
Experiment 3. Water Supply
and High-Temperature Interactions
For heat treatments, wheat was exposed to high temperature
(target 38°C) for 3 d (6 h per day) at 5 d preanthesis and 15 d
postanthesis using a growth chamber. The day/night tempera-
ture regime was 38:15°C with temperature transition occurring
over 3 h at the rate of 7.7°C h–1. Relative humidity was set to
20 and 60% for the day and night cycles, respectively. Plants
that were exposed to the high-temperature treatments were
watered to their upper limit weight, associated with their con-
trasting water treatment, ahead of being transferred from the
glasshouse environment to the growth chamber.
Heat Loads
To account for the different heat-wave treatments (tempera-
ture × duration) across the three experiments, we calculated the
heat load as the sum of °C above a threshold value for the logged
temperature data to give °C∙h. This calculation of the heat
sum used a temperature threshold of 32°C based on previous
critical temperature response of wheat (Alexander et al., 2010;
Blumenthal et al., 1994; Stone and Nicolas, 1994; Talukder
et al., 2014; Wardlaw and Wrigley, 1994). Although the 32°C
threshold was used in calculating heat load, the temperature of
the control treatments coincide with that of the ambient air of
the glasshouse which was typically <30°C (Table 1).
Crop Measurements
At crop maturity, wheat plants were harvested and samples
oven-dried at 40°C to constant weight. Dependent variables
of total biomass and yield components of grain number and
individual grain weight (based on 1000-grain weight) were
measured on both the main and tiller stem heads. This allowed
for potential temperature gradients within the heat chamber
to be accounted for, which could have an impact on whole
plant response to high-temperature response if the shorter tiller
heads were exposed to lower temperatures. Grain nitrogen was
determined by the Dumas combustion method (AACC 2000)
using the Leco TruMac equipment based on Approved Method
46.30.01 (AMAAC Chemists, 2000).
Statistical Analysis
Randomized complete block designs were applied to the
three experiments. Analysis of variance (ANOVA) was used
to test for the main effects and interaction of the independent
variables, high temperature, duration and growth stage (Exp. 1),
cumulative high-temperature duration (Exp. 2) and high tem-
perature and preanthesis and postanthesis water supply (Exp. 3).
Linear and nonlinear regression models were also fitted to the
temperature response data, expressed as heat sums. For the
postanthesis effects of high-temperature treatments on grain
yield, we had two independent data sets (Exp. 1 and 2) where
Exp. 1 was used for model development, and Exp. 2 was used for
independent validation. All statistical analyses were performed
using GenStat version 17 (VSN International, 2011).
Table 1. Heat loads (°C∙h, >32°C) to which wheat (‘Yitpi’) was Table 2. Response of wheat (‘Yitpi’) grain number and individual
exposed for a range of short-term durations (1, 3, or 5 d) and grain weight to a range of high-temperature treatments applied
temperature combinations at different growth stages across three during the reproductive and grain filling phase in Experiment 1.
experiments. High-temperature treatments commenced on day of High-temperature treatments (T) are 35, 37, and 42°C, which
year (DOY) 298, 308, and 318 for –5, 5, and 15 DAA, respectively, were applied in factorial combination at three growth stages
in Experiment 1 (Exp. 1); DOY 318 and 319 for 35 and 38°C treat- (GS; –5, 5, and 15 d after anthesis [DAA]) and for three dura-
ments, respectively, in Experiment 2 (Exp. 2); and DOY 266 and tions (D) of 1, 3 or 5 d.
286 for –5 and 15 DAA, respectively, in Experiment 3 (Exp. 3). Temperature (T)
Average ambient (Amb) air temperatures are for control plants
where the average is based on the equivalent time frame over Growth stage Duration Ambient 35°C 37°C 42°C
which the high-temperature treatments were imposed. (GS) (D) Grain number
Duration Heat load d ––––––––––– No. plant–1 ––––––––––
Growth
stage† d ———–———— °C∙h ——————— 1 108 105 95 91
Exp. 1. Anthesis heat shock –5 DAA 3 101 81 76 59
28°C (Amb) 35°C 37°C 42°C 5 125 105 67 55
–5 DAA 1 0 10 35 48 1 91 110 81 96
3 0 39 99 178 5 DAA 3 121 102 96 97
5 12 78 173 353 5 83 95 92 92
5 DAA 1 18 14 31 129 1 100 104 111 83
3 18 55 127 295 15 DAA 3 101 101 91 96
5 22 84 202 454 5 98 100 97 99
15 DAA 1 1 15 32 109 LSD(0.05) GS × D × T = 24
3 1 61 93 281 Growth stage Duration Individual grain weight
5 1 104 161 425 d –––––––––––––– mg –––––––––––––
Exp. 2. Cumulative heat shock 1 45.0 44.4 45.3 46.0
35°C 38°C –5 DAA 3 46.0 47.9 46.6 49.9
1 DAA‡ 1 20 41 5 38.2 41.5 50.5 49.1
2 39 83 1 46.4 42.7 47.1 41.0
3 59 124 5 DAA 3 37.3 44.5 43.6 38.5
4 79 166 5 48.2 44.3 43.0 34.3
6 118 248 1 45.6 43.2 42.5 47.7
8 158 331 15 DAA 3 43.7 43.7 45.2 44.1
10 197 414 5 45.4 42.3 43.3 41.8
12 236 497 LSD(0.05) GS × D × T = 5.5
14 276 579
Exp. 3. Water and heat interactions applied −5 DAA, with grain number reduced by 27% when
24°C (Amb) 38°C comparing the ambient and pooled duration and temperature
–5 DAA 3 0 127 treatments (p < 0.05). In contrast, the equivalent set of tempera-
15 DAA 3 0 123 ture treatments either individually or pooled occurring at 5 and
† DAA, days after anthesis; days of heat application were centered 15 DAA did not reduce grain number relative to their respective
around this growth stage. controls. Moreover, for the heat treatments applied at −5 DAA
‡ Days of heat application started from this growth stage; ambient the pattern of response across the temperature range changed
temperature of 22°C.
depending on the duration at which these temperatures were
Results applied, where for a single day, grain number was not signifi-
Experiment 1. Anthesis High Temperature cantly reduced. In contrast, when the temperature treatments
Heat Loads were applied over either three or five consecutive days, grain
number decreased at 37 and 42°C compared with the controls
On average, the 35, 37, and 42°C temperature treatments (p < 0.05). For the 3-d duration, there was a 33% reduction in
applied a heat load of 17, 35, and 84°C∙h (>32°C) per day of heat grain number pooled across these two high-temperature treat-
treatment, respectively (Table 1). This meant that heat sums ments compared with their respective controls and for 5-d dura-
within this experiment varied between 0 and 454°C∙h (>32°C). tion a 51% reduction for the equivalent temperature comparison.
For the ambient treatments, there were some instances, particu- Preanthesis (−5 DAA) heat caused individual grain weight to
larly during the 5 DAA period where polyhouse temperatures increase with increasing temperature. This increase was signifi-
exceed 32°C, which equated to between 0 and 22°C∙h incurred cant for wheat exposed to a 5-d duration at 37 and 42°C, where,
by the control plants, during the treatment period. for these high-temperatures treatments pooled, the increase was
30% relative to the control. In contrast, postanthesis heat caused
Wheat Yield Components a significant reduction in individual grain weight if heat at 42°C
For grain number, there was a significant interaction between was applied at 5 DAA; however, there were no significant differ-
the timing (−5, 5, and 15 DAA), duration (1, 3, and 5 d) and ences between the control, 35°C, and 37°C at this growth stage.
temperature (ambient, 35, 37, and 42°C) across the heat treat- There was no significant effect of heat at 15 DAA, on individual
ments (Table 2). Grain number was reduced by heat treatments grain weight for any temperature.

1300 Agronomy Journal   •  Volume 110, Issue 4  •  2018

Table 3. Response of wheat (‘Yitpi’) grain yield, harvest index, control, 35°C, and 37°C at this growth stage. For heat occur-
and grain nitrogen concentration to a range of high-temperature
ring at 15 DAA, the pattern of response was equivalent how-
treatments applied during the reproductive and grain filling
phase in Experiment 1. High-temperature treatments are 35, 37, ever the absolute impact of 42°C at 15 DAA was less than at 5
and 42°C, which were applied in factorial combination at three DAA.
growth stages (–5, 5, and 15 d after anthesis [DAA]). Results are
pooled for duration of treatment which was 1, 3 or 5 d. Experiment 2. Cumulative High-
Growth Temperature (T) Temperature Events
stage (GS) Ambient 35°C 37°C 42°C Heat Loads
Grain yield For the nine cumulative heat treatments where the maxi-
——————— g plant–1 ——————— mum temperature was set to 35°C, the associated heat sum was
–5 DAA 4.70 4.12 3.73 3.22 approximately 20°C∙h (>32οC) per day, while the 38°C treatment
5 DAA 4.12 4.31 3.96 3.54 applied an approximate heat load of 41°C∙h (>32οC) (Table 1).
15 DAA 4.41 4.24 4.26 4.07 Consequently, for the set of cumulative heat treatments at 35°C,
LSD(0.001) GS × T = 0.39 plants were exposed to nine increments between 20 and 276°C∙h
Harvest index (>32οC). For the 38°C set of treatments the equivalent range was
–5 DAA 0.40 0.37 0.35 0.31 41 to 579°C∙h (>32°C). For control plants within the glasshouse
5 DAA 0.38 0.38 0.37 0.34 environment, maximum temperatures did not exceed 26°C.
15 DAA 0.40 0.38 0.38 0.38
LSD(0.001) GS × T = 0.03 Wheat Yield Components
Grain nitrogen concentration For individual grain weight there was a significant interaction
––——————— % ———————–– between temperature and duration (Table 4). For those crops
–5 DAA 3.11 3.30 3.44 3.52 exposed to 35°C the impact of high temperature plateaued at a
5 DAA 3.18 3.19 3.30 3.43 15% reduction in individual grain weight after four heat days,
15 DAA 3.14 3.17 3.13 3.29 where the fourth day coincided with 8 DAA. In contrast for crops
LSD(0.05) GS × T = 0.14 exposed to 38°C there was a progressive reduction in individual
grain weight up to 29% after seven heat days where the seventh day
For grain yield there was a significant interaction between the coincided with 14 DAA. Grain number was not affected by any
timing and temperature across the heat treatments (Table 3). of the postanthesis high-temperature regimes. For yield this was
For heat occurring prior to anthesis (−5 DAA), temperatures of progressively and significantly reduced with increasing duration;
35, 37, and 42°C reduced yield by 12, 21, and 31%, respectively, however, there was no significant interaction with temperature
compared with the control (duration treatments pooled due to treatment. There was no yield penalty for either one or two heat
non-significance). Postanthesis heat caused a significant reduc- days occurring between 2 and 4 DAA for pooled temperature
tion in yield if heat at 42°C was applied at 5 DAA; however, treatments. In contrast, four heat days reduced yield by 15% with
there were no significant differences between the control, 35°C, yield decreasing with duration, whereas for nine heat days there
and 37°C at this growth stage. There was no significant effect of was a 30% reduction in yield where these 9 d occurred between 1
heat at 15 DAA on grain yield for any temperature. and 28 DAA. For harvest index, high temperature for one and two
Crop harvest indices followed a similar trend to yield, where heat days induced a significant increase compared with the control.
there was a significant interaction between the timing and For cumulative durations between 3 and 12 heat days, there was
temperature across the heat treatments. For preanthesis heat no effect on harvest index, and it was only at 14 heat days duration
(−5 DAA), temperatures of 35, 37, and 42°C all caused a signifi- that harvest index was significantly reduced compared with the
cant reduction in harvest indices of 8, 13, and 23%, respectively, control. Harvest index was similar for 35 and 38°C treatments.
compared with the control (duration treatments pooled due to
non-significance). Postanthesis heat caused a significant reduc- Grain Nitrogen
tion in harvest indices if heat at 42°C was applied at 5 DAA, Grain nitrogen concentration progressively and significantly
however, there were no significant differences between the increased with increasing duration of high temperature; however,
control, 35°C, and 37°C at this growth stage. There was no there was no interaction with temperature treatment (Table 4).
significant effect of heat at 15 DAA on harvest indices for any After four heat days the nitrogen concentration was significantly
temperature. higher (6%) compared with the control. Between four and six
heat days there was a large increase (6 to 12%) in nitrogen con-
Grain Nitrogen centration. Hereafter the impact of further cumulative high
There was a significant interaction between the timing and temperature had little effect on nitrogen concentration, where
temperature across the heat treatments on grain nitrogen for the maximum duration of 14 heat days, this induced a 13%
concentration (Table 3). For preanthesis heat (−5 DAA), tem- increase in nitrogen concentration compared with the control.
peratures of 35, 37, and 42°C all caused a significant increase in
nitrogen concentration of 6, 9, and 13% respectively compared Experiment 3. Water Supply and
with the control (duration treatments pooled due to non- High-Temperature Interactions
significance). Postanthesis heat caused a significant increase in Heat Loads
nitrogen concentration if heat at 42°C was applied at 5 DAA; For the preanthesis treatment (−5 DAA) the average tem-
however, there were no significant differences between the perature and corresponding heat load applied was 38°C and

Agronomy Journal   •   Volume 110, Issue 4  •  2018 1301

Table 4. Response of wheat (‘Yitpi’) grain yield and its components to cumulative high temperature applied progressively through the
grain filling phase in Experiment 2. Cumulative effects are tested for two temperatures (35 and 38°C) that were applied from 2 d after
anthesis (DAA) for 1 to 14 d.
Duration (D) in cumulative days
Temperature (T) 0 1 2 3 4 6 8 10 12 14
Individual grain weight
––––––––––––––––––––––––––––––––––––––––––– mg ––––––––––––––––––––––––––––––––––––––––––––
35°C 50.1 50.6 48.5 47.4 43.2 43.5 44.0 46.0 40.6 43.1
38°C 53.5 52.5 53.0 46.7 46.6 43.3 40.5 37.8 38.6 39.2
LSD(0.001) D × T = 3.7
Grain yield
––––––––––––––––––––––––––––––––––––––––– g plant–1 ––––––––––––––––––––––––––––––––––––––––––
35 and 38°C, pooled† 3.34 3.35 3.36 3.10 2.85 2.79 2.75 2.56 2.50 2.34
LSD(0.001) D = 0.35
Harvest index
35 and 38°C, pooled† 0.36 0.38 0.40 0.37 0.37 0.36 0.36 0.34 0.33 0.32
LSD(0.001) D = 0.03
Grain nitrogen concentration
–––––––––––––––––––––––––––––––––––––––––––– % ––––––––––––––––––––––––––––––––––––––––––––
35 and 38°C, pooled† 3.07 3.12 3.15 3.17 3.26 3.43 3.40 3.43 3.48 3.47
LSD(0.001) D = 0.14
Table 5. Response of wheat (‘Yitpi’) grain yield and its compo-
127°C∙h, respectively. Similarly, the postanthesis treatment nents to water availability and high temperature, where the
(15 DAA) average temperature and corresponding heat sums treatment of 38°C was applied at two growth stages (–5 and 15 d
were 37°C and 123°C∙h, respectively. During the periods that after anthesis [DAA]) and are compared with ambient conditions
in Experiment 3. Factorial combinations of low and high water
treatments were applied the average ambient temperature of
availability in the preanthesis and postanthesis phases were also
control plants was 21°C within the glasshouse environment. tested, where only interactive effects of preanthesis water with
other growth stage and temperature are presented.
Wheat Yield Components Temperature (T)
Preanthesis Growth stage
Grain number was affected by the combination of prean- water (pre-θ) (GS) Ambient 38°C
thesis water supply, heat treatment, and timing (Table 5). For Grain number
wheat under high water supply in the preanthesis phase, there –––––––– No. plant–1 ––––––––
was no significant effect of high temperature applied at either Low –5 DAA 49 43
−5 or 15 DAA, on grain number. In contrast, where wheat was 15 DAA 49 51
grown under a low water supply in the preanthesis period, high High –5 DAA 55 55
temperatures applied at −5 DAA caused a significant reduc- 15 DAA 56 55
tion in grain number, whereas heat applied 15 DAA did not LSD(0.05) pre-θ × GS × T = 3.1
affect grain number. Under ambient temperature, high-water Individual grain weight
treatments in the preanthesis phase produced crops with 13% ––––––––––– mg –––––––––––
higher grain number compared with the low water treatment. Pooled –5 DAA 49.9 51.9
Individual grain weight was affected by the temperature 15 DAA 48.9 47.4
and the timing; however, there were no significant interactive LSD(0.05) GS × T = 1.45
effects of water availability either in the preanthesis or post- Grain yield
anthesis period. When wheat was exposed to heat −5 DAA, ––––––––– g plant–1 ––––––––
individual grain weight significantly increased (4.0%) com- Low –5 DAA 2.4 2.2
pared to the wheat under ambient temperatures, whereas when 15 DAA 2.4 2.4
heat occurred at 15 DAA, there was the reverse trend where High –5 DAA 2.7 2.8
individual grain weight was significantly reduced by 3.2%. 15 DAA 2.8 2.7
Yield was affected by the combination of preanthesis water
LSD(0.05) pre-θ × GS × T = 0.06
supply, heat treatment and timing. There was no significant
effect of postanthesis water supply. For wheat under high water
supply in the preanthesis phase, there was no significant effect of 14% lower yield compared with the high water treatment. The
high temperature applied at −5 DAA, whereas for heat occurring average harvest index in this experiment was 0.40 with no sig-
at 15 DAA there was a significant reduction in yield of 5%. In nificant main or interactive effects linked with heat treatment.
contrast, where wheat was grown under a low water supply in the
preanthesis period, high temperature applied at −5 DAA caused Grain Nitrogen
a significant reduction (8%) in yield, whereas heat occurring at For grain nitrogen concentration, there were no interactive
15 DAA did not affect yield. Under ambient temperature, low effects of water availability or timing of high temperature linked
water treatments in the preanthesis phase produced crops with with heat treatment, although the main effect of heat was to

1302 Agronomy Journal   •  Volume 110, Issue 4  •  2018


Fig. 1. Preanthesis high temperature and wheat response.
Percentage of change in wheat (‘Yitpi’) yield components, grain
number (GN) and individual grain weight (GW), and grain
nitrogen concentration (GNC) due to increasing heat sum (°C∙h,
>32°C) associated with a range of short term high-temperature
treatments applied 5 d prior to anthesis. For experiment three
(Exp. 3), two preanthesis crop water availabilities, low water
(LW) and high water (HW) are presented. One treatment (6) is
excluded from the grain number linear regression analysis (dashed
line) and exponential models (solid lines) are for Experiment 1.
increase grain nitrogen concentration by 3% from 1.53 to 1.60%.
There was, however, a significant effect of water availability where
for the preanthesis and postanthesis treatments, low water supply
produced a significant increase in nitrogen concentration of 12 and
3% respectively compared with the high-water equivalents.
Heat Load and Crop Response
The factorial structure of these experiments was aimed at
developing relationships which define the impact of timing,
duration, temperature and water content on wheat yield com-
ponents. In this section the relationships between crop response
and an applied heat load are presented. By using heat sum, the
interactions between temperature and duration are captured in a
single variable. Two sets of relationships were developed through
a separate analysis of the preanthesis and postanthesis response
due to the different yield component effects before and after
anthesis. Pooling of data across these two periods did not provide
useful descriptive models due to a departure in response charac-
teristics of wheat across the preanthesis and postanthesis periods.
Short term high temperature effects have been observed to influ-
ence grain number (Tashiro and Wardlaw, 1990), therefore we
tested grain number response combining the −5 and 5 DAA
treatments. We observed a flat response to high-temperature
treatments at 5 DAA, thus restricted further analysis of grain
number to −5 DAA treatments.
Agronomy Journal   •   Volume 110, Issue 4  •  2018 1303
Grain Number
High-temperature treatments in the preanthesis period
(−5 DAA) applied in Exp. 1 and 3 caused an overall reduction
in grain number of 0.16% per °C∙h (>32οC; R2 = 0.60) (Fig. 1).
In comparison to this simple linear model, for Exp. 1 alone, an
exponentially decreasing function effectively described the asymp-
totic nature of decreasing grain number with increasing heat sum
(Table 6). For postanthesis treatments (5 and 15 DAA) of high
temperature, there was no significant effect on grain number.
Individual Grain Weight
High-temperature treatments in the preanthesis period
(−5 DAA) applied in Exp. 1 and 3 caused an overall increase in
individual grain weight of 0.034% per °C∙h (>32°C; R2 = 0.49)
(Model not shown). An exponential function more effectively
described (R2 = 0.66) the asymptotic nature of increasing
individual grain weight with heat sum (Fig. 1; Table 6), indicat-
ing diminishing compensation in response to reduced grain
number (sink size).
In contrast, the effect of postanthesis heat, applied from 1
to 28 DAA (Exp. 2) resulted in a progressive decrease in indi-
vidual grain weight of 0.049% per °C∙h (>32οC; R2 = 0.49)
(Fig. 2). Again, an exponential function more effectively
described decreasing individual grain weight with postanthesis
heat sum (R2 = 0.71) (Table 6) and may reflect the biological
response of diminishing impact of high temperature on indi-
vidual grain weight with increasing time from anthesis.
Grain Nitrogen
High-temperature treatments before anthesis (−5 DAA)
applied in Exp. 1 and 3 caused an overall increase in grain
nitrogen concentration of 0.059% per °C∙h (>32°C; R2 = 0.36)
(Model not shown). An exponential function more effectively
described the asymptotic nature of increasing grain nitrogen
concentration with heat sum (R2 = 0.80) (Fig. 1; Table 6).
For high-temperature treatments applied before anthesis, the
increase in individual grain weight was accompanied by a pro-
portionate increase in grain nitrogen concentration.
The effect of postanthesis high-temperature treatments,
applied from 1 to 28 DAA resulted in progressive average
increase in nitrogen concentration of 0.032% per °C∙h (>32°C;
R2 = 0.64) for Exp. 1, 2, and 3 (Fig. 2). Restricting the response
to Exp. 2, which assessed cumulative effects of short term high
temperature events, grain nitrogen response followed an expo-
nential function (R2 = 0.84) (Table 6). In contrast with the
effects of preanthesis heat on individual grain weight and grain
nitrogen concentration, for postanthesis high temperature,
there was an inverse relationship between these two variables.
Grain Yield
High-temperature treatments before anthesis (−5 DAA)
applied in Exp. 1 caused an overall decrease in grain yield of
0.15% per °C∙h (>32°C; R2 = 0.54) (Fig. 3). An exponential
function more effectively described the asymptotic nature of
decreasing grain yield with heat sum (R2 = 0.83) (Table 6).
For high-temperature treatments applied in the postanthesis
phase (Exp. 1 used for model development), yield response was
less sensitive, where there was a decrease of 0.065% per °C∙h
(>32°C; R2 = 0.60) (Fig. 3; Table 6). An exponential function
Table 6. Summary of linear and exponential functions on the percentage of change in wheat (‘Yitpi) yield and components (y), grain num-
ber (GN) and individual grain weight (GW) and grain nitrogen concentration (GNC) due to increasing heat sum (°C∙h, >32°C) associated
with a range of short term high-temperature treatments (x). Domain for the preanthesis and postanthesis functions is 0 to 350 and 0 to
600°C∙h (>32°C), respectively. Linear function is described by y = ax and exponential function by y = a + brx. Standard errors of estimate
are presented in parentheses.
Response
variate Function Source data a b r p R2
Preanthesis
GN Linear Experiments 1 and 3 (low-water treatments) –0.16 (0.02) – – <0.001 0.60
GN Exponential Experiment 1 –59.0 (27.9) 60.4 (24.0) 0.995 (0.005) 0.015 0.67
GW Exponential Experiment 1 9.7 (2.8) –13.6 (3.5) 0.987 (0.009) 0.029 0.66
GNC Exponential Experiment 1 17.5 (2.9) –19.8 (3.4) 0.988 (0.006) 0.004 0.80
Yield Linear Experiment 1 –0.15 (0.02) – – <0.001 0.54
Yield Exponential Experiment 1 –48.3 (12.3) 45.8 (10.5) 0.994 (0.004) 0.002 0.83
Postanthesis
GW Linear Experiments 1, 2, and 3 –0.049 (0.005) – – <0.001 0.49
GW Exponential Experiment 2 –30.5 (8.2) 29.7 (6.9) 0.996 (0.002) <0.001 0.71
GNC Linear Experiments 1, 2, and 3 0.032 (0.002) – – <0.001 0.64
GNC Exponential Experiment 2 25.4 (10.7) –24.7 (9.9) 0.998 (0.001) <0.001 0.84
Yield Linear Experiment 1 –0.065 (0.008) – – <0.001 0.60

did little to improve the descriptive capability. Experiment 2
was used for validation of the linear function describing post-
anthesis temperature on percent change in yield. There was
good agreement between observed (y) and predicted (x) values
where the slope was unbiased: y = 0.96 (±0.15) x + 2.0 (±2.5)
(R2 = 0.71); standard error is in parentheses. The Root Mean
Squared Error (RMSE) was 6% change in yield.
Discussion
For short-term high-temperature effects in wheat, the tim-
ing, cumulative duration, and magnitude of high temperature
all impacted the nature and severity of response. Of the yield
components, grain number was most sensitive to high tempera-
ture occurring just prior to anthesis (−5 DAA), with an average
reduction of 0.16% per °C∙h above 32°C, although this sensitiv-
ity was not evident when stress occurred at or beyond 5 d after
anthesis. This preanthesis response is consistent with Tashiro
and Wardlaw (1990) where heat-induced grain sterility was
greatest 2 to 3 d prior to anthesis, which approximated 0.86%
per °C∙h above 32°C, for floret basal grains from the 5th and
11th spikelets, with the temperature response rapidly dropping
off hereafter. Wollenweber et al. (2003) determined that high
temperature for 8 d at anthesis caused a reduction in grain
number, on a whole-plant basis equivalent to the rate of 0.18%
per °C∙h above 32°C demonstrating the sensitivity of grain-set
to high temperature in the early stages after anthesis.
Limiting grain-set due to acute high temperature just before
anthesis is linked to the sensitivity of microsporogenesis (pollen
development) occurring at this time and loss of pollen viability,
disrupted fertilization process and resultant grain sterility and
also the formation of parthenocarpic grains when high tempera-
ture occurs at anthesis (Djanaguiraman et al., 2017; Tashiro and
Wardlaw, 1990). Similarly for other crops such as grain sorghum
and legumes (peanut), grain-set is also highly sensitive to high
temperature in the period just prior to flowering (Prasad et al.,
2008; Singh et al., 2011). For example, sorghum grain-set was
reduced by 0.07% per °C∙h above 32°C for a high-temperature
treatment of 40:30°C for ten consecutive days leading up to
flowering (Prasad et al., 2008). With regard to crop models, the
sensitivity of grain number response, particularly in the period of
10 d centering on anthesis for wheat, supports the need for a vari-
able step response based on growth stage in models consistent
with that proposed by Barlow et al. (2015).
The reduction in grain-set associated with preanthesis high
temperature corresponded with an increase in individual grain
weight and grain nitrogen concentration of 0.03 and 0.06% per
°C∙h above 32°C, respectively. In this case, reduction in grain
number of up to 48%, translated to both (i) greater assimilate
available on a per kernel basis, and (ii) capacity to maintain
grain nitrogen concentration without dilution compared with
carbohydrate supply, although the net effect of preanthesis high
temperature was a reduction in yield. In contrast Calderini et
al. (1999) observed that short-term high temperature, immedi-
ately before anthesis, caused a reduction in grain weight, linked
with reduced carpel weight where the proximal florets of the
four central spikelets of the main stem were assessed. Similarly
Ugarte et al. (2007) found for wheat growing under irrigated
field conditions, high temperature in the period between
heading and anthesis induced an 8 and 7% reduction in grain
number and individual grain weight, respectively. Within the
current study, the almost halving of grain number due to pre-
anthesis high temperature resulted in individual grain weight
increasing. These different observations across studies indicate
that grain size is more an emergent property of source and sink
relationships that should be adequately modeled.
The dominant postanthesis response to short term high tem-
perature was a reduction in individual grain weight, which is
consistent with a range of studies (Jenner et al., 1991; Pradhan
et al., 2012; Ugarte et al., 2007). This response is driven by
shortened duration of starch deposition and accelerated senes-
cence (Lobell et al., 2012; Stone and Nicolas, 1995a) as well as
reduced activity of enzymes catalyzing starch synthesis limit-
ing the rate of starch deposition (Jenner, 1994). The increase
in grain filling rate under high temperature is insufficient to
compensate these negative effects. For the current study, average
reduction in individual grain weight due to high temperature
was 0.05% per °C∙h above 32°C, accounting for both single
high temperature events staged at 5 and 15 DAA and also

1304 Agronomy Journal   •  Volume 110, Issue 4  •  2018

Fig. 2. Postanthesis high temperature and wheat response.
Percentage of change in wheat (‘Yitpi’) individual grain weight
(GW) and grain nitrogen concentration (GNC) due to
increasing heat sum (°C∙h, >32°C) associated with a range of
short term high-temperature treatments applied postanthesis.
For Experiment 3, two preanthesis crop water availabilities,
low water (LW) and high water (HW) are presented. Linear
models (dashed lines) describe the pooled response of the three
experiments and the exponential models (solid lines) describes
the response for Experiment 2 only.
cumulative effects of high temperature from anthesis to 28
DAA. For short-term high temperature (40°C for 5 d) applied
at a range of stages between 15 and 50 DAA (Stone and Nicolas,
1995b), a reduction in individual grain weight of 9 to 15% in
the period of 15 to 30 DAA was recorded, which equated to a
reduction of 0.03 to 0.05% per °C∙h above 32°C for this period,
respectively. With regard to the cumulative effects of high tem-
perature, Pradhan et al (2012) imposed 16 d of cumulative high
temperature (18 h per day) at 36:30°C commencing at anthesis
with individual grain weight of wheat reduced by 0.06% per
°C∙h above 32°C, where the total cumulative heat load was
estimated to be 1152°C∙h above 32°C which compares with
579°C∙h above 32°C in the current study. For crop models, such
as APSIM-N wheat senescence is accelerated at temperatures
greater than 34°C (Asseng et al., 2011) with simulated yield and
individual grain weight reduction comparable in magnitude to
what we observed, that is, 5 to 10% for 3 to 5 d exposure.
For individual grain weight, the timing at which high
temperature occurs during the postanthesis period is also
important, where we observed that high temperature (42°C)
5 d after anthesis significantly reduced individual grain weight,
although not at 15 DAA, indicating a declining sensitivity to
high temperature as the grain filling phase advances. Similarly,
Tashiro and Wardlaw (1990) observed that the incidence of
shrunken grain was greatest for high temperature (36:31°C,
2 d) at 2 to 6 DAA, whereas from 6 to 10 DAA damage to
Agronomy Journal   •   Volume 110, Issue 4  •  2018 1305
Fig. 3. High temperature and yield response of wheat.
Percentage of change in wheat (‘Yitpi) yield due to increasing
heat sum (°C∙h, >32°C) associated with a range of short-term
high-temperature treatments applied in the preanthesis and
postanthesis periods. Linear (dashed lines) and exponential
models (solid line) describe the response where models
are derived from Experiment 1 data only. Plotted data for
Experiment 2 postanthesis (8) is for model validation.
grain was restricted to notching, or being split and opaque. For
3-d exposure to high temperature, Randall and Moss (1990)
observed a 19, 14, and 1% reduction in individual grain weight
for high temperature applied at 20, 36, and 50 DAA, respec-
tively. Moreover Stone and Nicolas (1995b) demonstrated a
progressive reduction in sensitivity of the grain filling process
to short periods of high temperature, where at 40°C for 5 d
(300°C∙h above 32°C) the average reduction in individual
grain weight across two genotypes was 15, 9, and 1% for 15, 30,
and 40 DAA respectively for grain from the a and b florets of
the two central spikelets of the main stem ear.
For the current work, despite a linear model being presented
as a simplified expression between reduction in individual grain
weight and heat sum, our data (Exp. 2) did show a tendency to an
asymptotic response where greatest sensitivity of individual grain
weight reduction was observed for heat loads up to 150 °C∙h
above 32°C, which constituted treatments of either 35°C (1 to
16 DAA) or 38°C (1 to 8 DAA). Hereafter, additional heat load
had less impact reflecting increasing tolerance to high tempera-
ture later in the grain filling phase. This is consistent with Porter
and Gawith (1999) who, in a review on high temperature effects
on wheat, concluded that during the reproductive period, 31°C
was the upper limit (Tmax) wheat could tolerate during anthesis
whereas Tmax increased to between 33 and 37°C during the
grain filling phase, although critical thresholds can shift given
cultivar (Stone and Nicolas, 1994). Accounting for this variable
response with time from anthesis is of importance in modeling
acute high temperature response in the postanthesis period.
 We observed that grain nitrogen concentration increased by
0.03% per °C∙h above 32°C for the range of high-temperature
treatments during the grain-filling phase. Moreover, the ten-
dency to an asymptotic response of grain nitrogen concentration
to increasing heat sum highlighted the utility of an exponential
type model. Typically, acute high temperature increases grain
nitrogen concentrations, where temperatures above 30°C dur-
ing grain filling decrease the rate at which starch accumulates,
while the rate of nitrogen accumulation is largely unaffected
(Altenbach et al., 2003; Jenner, 1994; Panozzo and Eagles,
2000; Randall and Moss, 1990). Additionally, an increase in
grain nitrogen concentration due to a reduction in grain filling
period and a reduction in individual grain weight is a contribut-
ing factor; however, we were unable to resolve these high tem-
perature effects in our study.
Abiotic factors such as water availability also affect crop
response to acute high temperature. The effects of water supply
on high temperature response appear variable across a range of
studies. We observed that adequate water supply attenuated high
temperature effects where for limited water in the preanthesis
period, high temperature 5 d prior to anthesis caused a signifi-
cant reduction in grain-set; however, when water was non-lim-
iting up to anthesis, there was little effect of high temperature.
Similarly, for crops that were heat stressed, adequate water supply
helped maintain grain filling rate, duration and size (Altenbach
et al., 2003). In another case, despite adequate water, a reduction
in grain weight was observed to fall up to 4% for every 1°C rise in
temperature above 18°C (McDonald et al., 1983). Pradhan et al.
(2012) determined that for postanthesis water supply and tem-
perature effects across six wheat genotypes, that a decrease in leaf
chlorophyll, individual grain weight, and grain yield occurred
in an increasing magnitude of drought < high temperature <
combined stress. In contrast for a controlled environment study,
Mahrookashani et al. (2017) found the order of severity to be
high temperature < drought < combined stress on wheat growth.
For field crops factors such as canopy cooling through transpira-
tion are also likely to attenuate the effects of high temperature,
although this will depend on plant available water. Overall, the
link between water supply and acute high temperature response
of crop infers that a modifying parameter related to these factors
may provide utility within crop models. Given the many poten-
tial combinations of water supply and high temperature, the
challenge is defining a useful range of response surfaces.
Wheat genotypes vary significantly in their sensitivity to high
temperature (Farooq et al., 2011; Pradhan et al., 2012; Slafer and
Rawson, 1994; Stone and Nicolas, 1995a). To highlight this point,
Stone and Nicolas (1998) demonstrated significant differences in
the response of two wheat genotypes, differing in heat tolerance,
linked primarily with duration of the grain filling phase and also
rate of deposition during the period of high temperature. Across
genotypes, tolerance to heat was inferred by (i) the reduction in
sensitivity of response from anthesis curtailing earlier than the
sensitive genotype (30 vs. 40 DAA) which translates to a longer
grain filling phase, and (ii) the rate of grain filling in the early
period after anthesis (5 to 25 DAA) not declining so sharply in
response to high temperature and more rapid recovery, compared
with the intolerant genotypes. Moreover, the reduction in dura-
tion of the grain filling phase is not entirely attributable to more
rapid accumulation of thermal time, where differences in duration
1306 Agronomy Journal   •  Volume 110, Issue 4  •  2018
varied based on the postanthesis growth stage at which the high
temperature event occurs (Stone and Nicolas, 1995a). For example
from 15 DAA onward, a delay in exposure to heat of 3 d translated
to lessening the reduction of duration of grain filling by 1 d. These
findings provide important insights into how genotypic response,
differing in heat tolerance may be modeled. Such advances will
also support the development of crop ideotypes, (Sylvester-Bradley
et al., 2012) optimized for targeted agroecological zones and future
seasonal growing conditions as the climate changes.
Heat sums were used in this study to express and compare
the high temperature response of wheat, which simplified the
prediction of grain number, weight and nitrogen concentration
in response to the interactions of temperature and duration.
Contemporary process-based crop models use readily available
climate data as key inputs into models, including daily maxi-
mum and minimum temperatures, which typically operate at
a daily time step, consequently the difference between time
resolution between heat sums on an hourly basis and daily time
step accentuates the approximation of the daily time step mod-
els. Such approximation can be minimized by measured hourly
climate data, hourly data derived from models that predict the
diurnal temperatures based on daily minimum and/or maxi-
mum data (Cesaraccio et al., 2001), or a relationship which
allowed the estimation of heat load from maximum daily
temperatures. To the latter point, an analysis of hourly (or sub-
hourly) climate data from 20 climate stations across Victoria,
Australia found a strong relationship between the maximum
temperature and heat load (R2 = 0.95) (K. Barlow, pers. comm.,
2016), pointing to likely improvements with such approaches.
While we used air temperature as the primary measure of heat
load further improvements should also be possible if the canopy
temperatures are used so that the effects of canopy cooling and
heating from varying water status is more fully expressed. The
majority of high temperature studies on crop are conducted in
controlled environment facilities, which carry limitations such as
the measured response being on a per plant response and cannot
account for process peculiar to that which occur within a crop
canopy such as buffering through cooling linked with transpira-
tion and potential heating through water stress. Clearly, the cur-
rent results need to be field validated to determine whether the
magnitude of response reflects field conditions. Previous research
also suggests that pot trials often show a greater response to heat
wave treatment than is observed under field conditions (Asseng
et al., 2011), potentially due to cooler root temperatures in the
field compared to pot trials (Kuroyanagi and Paulsen, 1988; van
Herwaarden et al., 1998). Despite these limitations controlled
environment experiment provide a valuable source of informa-
tion for understanding the response to targeted treatments where
other confounding factors, which may exist under field condi-
tions can be controlled.
From a next-users perspective, it is anticipated that these
data will assist in the evolution of expanded crop models with
improved high temperature response functions. Such model
improvements are particularly important in the evaluation of
the impact of global climate change in various agro ecological
zones of the world to wheat production and to identify pos-
sible agronomic management and genetic solutions to limit the
impact of a changing climate.
 Conclusion
For the three high temperature studies presented, which tar-
geted response of wheat to heat wave-like scenarios, coinciding
with the reproductive and grain filling phase, high temperature
shortly prior to anthesis caused a significant reduction in grain
set, with a corresponding increase in individual grain weight
and grain nitrogen concentration, but an overall reduction in
yield. These responses could be defined in terms of heat load,
which combined the effects of intensity and duration of high
temperature. These observation provide further insight into
the step change response of wheat yield potential to acute high
temperature and a requirement for a reset mechanism within
crop models. For high temperatures commencing 5 d after
anthesis, this induced an initial rapid reduction in individual
grain weight with a corresponding increase in grain nitrogen
concentration, where greatest sensitivity of crops to high tem-
perature occurred early in the grain filling phase. Collectively,
these results contribute to the broader knowledge base used
for developing acute high temperature response algorithms for
wheat within contemporary crop models. Such advances will
provide increasingly robust methods for analyzing the impact
of abiotic constraints to wheat production, using a modeling
approach. In particular such analyses will become increasingly
important in the context of climate change impacts and devel-
oping crop adaptation strategies which maintain production
and yield stability of arable cropping systems.
Acknowledgments
The authors would like to thank the Australian Grains Research
and Development Corporation and Agriculture Victoria, Dep. of
Economic Development, Jobs, Transport and Resources for their
financial support of this research.
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