fpls-13-886541 May 10, 2022 Time: 16:52 # 1
ORIGINAL RESEARCH
published: 16 May 2022
doi: 10.3389/fpls.2022.886541
The Effects of Brief Heat During Early
Booting on Reproductive,
Developmental, and Chlorophyll
Physiological Performance in
Common Wheat (Triticum
aestivum L.)
Jiemeng Xu1, Claudia Lowe1, Sergio G. Hernandez-Leon2, Susanne Dreisigacker3,
Matthew P. Reynolds3, Elisa M. Valenzuela-Soto2, Matthew J. Paul1 and Sigrid Heuer1,4*
1 Plant Science Department, Rothamsted Research, Harpenden, United Kingdom, 2 Centro de Investigación en Alimentación
Edited by: y Desarrollo A.C., Carretera Gustavo Enrique Aztiazarán Rosas, Hermosillo, Mexico, 3 International Maize and Wheat
Pasala Ratnakumar, Improvement Center (CIMMYT), Texcoco, Mexico, 4 Pre-Breeding Department, National Institute of Agricultual Botany
Indian Institute of Oilseeds Research (NIAB), Cambridge, United Kingdom
(ICAR), India
Reviewed by: Rising temperatures due to climate change threaten agricultural crop productivity. As
Renu Munjal,
Chaudhary Charan Singh Haryana a cool-season crop, wheat is heat-sensitive, but often exposed to high temperatures
Agricultural University, India during the cultivation period. In the current study, a bread wheat panel of spring
Ashok Singamsetti,
Banaras Hindu University, India wheat genotypes, including putatively heat-tolerant Australian and CIMMYT genotypes,
*Correspondence: was exposed to a 5-day mild (34◦C/28◦C, day/night) or extreme (37◦C/27◦C) heat
Sigrid Heuer stress during the sensitive pollen developmental stage. Worsening effects on anther
sigrid.heuer@niab.com morphology were observed, as heat stress increased from mild to extreme. Even under
Specialty section: mild heat, a significant decrease in pollen viability and number of grains per spike
This article was submitted to from primary spike was observed compared with the control (21◦C/15◦C), with Sunstar
Plant Abiotic Stress, and two CIMMYT breeding lines performing well. A heat-specific positive correlation
a section of the journal
Frontiers in Plant Science between the two traits indicates the important role of pollen fertility for grain setting.
Received: 28 February 2022 Interestingly, both mild and extreme heat induced development of new tillers after
Accepted: 04 April 2022 the heat stress, providing an alternative sink for accumulated photosynthates and
Published: 16 May 2022
significantly contributing to the final yield. Measurements of flag leaf maximum potential
Citation:
Xu J, Lowe C, quantum efficiency of photosystem II (Fv/Fm) showed an initial inhibition after the heat
Hernandez-Leon SG, Dreisigacker S, treatment, followed by a full recovery within a few days. Despite this, model fitting using
Reynolds MP, Valenzuela-Soto EM, chlorophyll soil plant analysis development (SPAD) measurements showed an earlier
Paul MJ and Heuer S (2022) The
Effects of Brief Heat During Early onset or faster senescence rate under heat stress. The data presented here provide
Booting on Reproductive, interesting entry points for further research into pollen fertility, tillering dynamics, and leaf
Developmental, and Chlorophyll
Physiological Performance senescence under heat. The identified heat-tolerant wheat genotypes can be used to
in Common Wheat (Triticum aestivum dissect the underlying mechanisms and breed climate-resilient wheat.
L.). Front. Plant Sci. 13:886541.
doi: 10.3389/fpls.2022.886541 Keywords: heat stress, booting, pollen viability, tillering, SPAD and Fv/Fm, wheat
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Xu et al. Novel Sources & Traits for Heat-Tolerant Wheat
INTRODUCTION underlying tillering dynamics and impact on final yield have
not been discussed.
Wheat is one of the most important crops for human In addition to the effects on pollen fertility and spike number,
consumption, grown on 220 million hectares with a total heat-induced yield loss has also been ascribed to accelerated
production of 760 million tons in 2020 (FAOSTAT). In scenarios leaf senescence, shortening the duration of grain filling (Cossani
of climate change, wheat plants are prone to be exposed to and Reynolds, 2012; Pinto et al., 2016; Shirdelmoghanloo et al.,
warmer and more variable temperatures (Trnka et al., 2014). 2016; Bergkamp et al., 2018; Sade et al., 2018). As indicators of
Beyond a physiological threshold, high temperatures cause stress senescence, chlorophyll soil plant analysis development (SPAD)
and impair plant growth and development. Both historical data (chlorophyll content index) (Richardson et al., 2002) and
and future predictions have revealed the negative effects of heat Fv/Fm (the maximum potential quantum yield of photosystem
on wheat productivity at the global and regional scale (Liu et al., II) (Murchie and Lawson, 2013) have been widely used to
2016; Zampieri et al., 2017; Pequeno et al., 2021). Therefore, it evaluate this trait. Under terminal heat, SPAD and Fv/Fm
is crucial to identify and breed heat-adapted varieties to sustain were often reduced in leaf tissue during senescence and were
wheat production and ensure food security. closely related to yield-contributing traits, such as thousand
In nature, the adverse effects of heat stress on plants can be grain weight (Talukder et al., 2014; Hassan et al., 2018;
variable depending on the intensity, duration, and developmental Mirosavljević et al., 2021; Touzy et al., 2022). Studies for the
stage (Stone and Nicolas, 1995; Yeh et al., 2012). Most of the genetic analysis of these leaf senescence related traits are also
heat-related studies in wheat have been field-based and used available (Azam et al., 2015; Bhusal et al., 2018; Touzy et al.,
late sowing to expose plants to high temperatures during the 2022). Nevertheless, time course measurements of SPAD and
flowering and grain filling stages; however, short episodes of Fv/Fm, which enable model fitting and senescence parameter
heat during earlier reproductive stages can also cause significant prediction, have rarely been captured in wheat under heat stress
damage (Zampieri et al., 2017). Indeed, anther and pollen (Pinto et al., 2016; Šebela et al., 2020; Touzy et al., 2022),
development are considered to be the stages most vulnerable to especially after brief heat during the early reproductive stage.
heat stress (Zinn et al., 2010; Rieu et al., 2017). Stage-specific In the present study, a wheat heat panel, including putatively
treatments have found that wheat is particularly sensitive to heat-tolerant Australian and CIMMYT-nominated spring wheat
heat around 8 days before anthesis, which coincides with the genotypes, was exposed to a 5-day extreme (37◦C/27◦C) (Erena,
early meiosis to tetrad stage of pollen development (Saini and 2018) or mild (34◦C/28◦C) heat stress during the early pollen
Aspinall, 1982; Prasad and Djanaguiraman, 2014). Because pollen developmental stage and analyzed for the effects on (i) pollen
development occurs during the booting stage, while spikes are viability and seed set; (ii) spike formation and underlying tillering
still inside the developing pseudostem in wheat, the length dynamics; (iii) leaf senescence measured with SPAD and Fv/Fm;
of the auricles between the flag leaf and the penultimate leaf and (iv) relationships among the reproductive, developmental,
(referred as auricle interval length, AIL) has been used as a physiological, and yield-related traits.
proxy for pollen development. AIL between 3 and 6 cm has
been associated with this sensitive stage (Bokshi et al., 2021;
Erena et al., 2021). Brief heat exposure during this sensitive MATERIALS AND METHODS
period resulted in abnormal meiosis behavior (Omidi et al., 2014;
Draeger and Moore, 2017) and a significant reduction in pollen Plant Material
fertility (Prasad and Djanaguiraman, 2014; Begcy et al., 2018; In this study, three greenhouse experiments (i.e., Exp1, Exp2,
Browne et al., 2021). A few studies have examined the natural and Exp3) were conducted during 2020–2021 at the controlled
variation in pollen viability under heat stress and its association environment and glasshouse facilities at Rothamsted Research,
with yield, as booting usually occurs during the cooler time of Harpenden, United Kingdom (51.8094◦N, 0.3561◦W). For Exp1
the cropping season and it is difficult to apply precise stage- and Exp2, the same set of 14 wheat genotypes was used, and
specific heat stress (Bheemanahalli et al., 2019; Bokshi et al., 22 lines (seven overlapping with Exp1 and Exp2) were grown
2021). However, considering a warmer and increasingly erratic in Exp3 (refer to Supplementary Table 1 for genotype details).
climate, this area warrants further investigation. These lines are putatively heat-tolerant elite spring varieties
Spike number is one of the main components in determining (Sunstar, Sokoll, and Waagaan), parental lines and their pre-
wheat yield; it is highly variable and responsive to the breeding materials (Cossani and Reynolds, 2015; Erena, 2018), as
environmental factors (Slafer et al., 2014). Interestingly, well as two lines from the United Kingdom included as controls.
contrasting responses of spike number under heat stress have
been reported. When exposed to continuous high temperatures Experimental Design and Heat Stress
during the terminal flowering and grain filling stages, spike Treatment
formation and tillering were always reduced (Cai et al., 2016; Exp1
Sharma et al., 2016; Dwivedi et al., 2017; Kumar et al., 2021). This experiment was conducted between June and September
In contrast, after a short episode of heat stress during earlier of 2020 and followed a split randomized complete block design
developmental stages, spike numbers increased (Bányai et al., (split RCBD) with four blocks/biological replicates. Fourteen
2014; Chavan et al., 2019; Hütsch et al., 2019). Enhanced genotypes (Supplementary Table 1) were randomly assigned to
spike formation after early heat stress is surprising, but the the whole plot within each block, and temperature treatments
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(control/CT and heat/HT) were assigned to the subplots within sequentially moved into the growth chamber with a mild
each whole plot. Two seeds were sown in separate pots filled temperature of 34.00 ± 0.02/28.00 ± 0.01◦C (day/night)
with Rothamsted Standard compost (75% medium grade peat; (Supplementary Figure 1F). Plants for CT treatment were also
12% screened sterilized loam; 3% medium grade vermiculite; 10% moved into a similar growth chamber with the temperature of
5 mm screened lime-free grit) and fertilized with Osmocote Exact 21.01 ± 0.02/15.01 ± 0.01◦C (Supplementary Figure 1F). The
for 3–4 months at the rate of 3.5 kg/m3. One week after sowing, light period, intensity, and RH were similar between CT and HT
seedlings were thinned down to one per pot and grown under treatments with settings of 16 h, 600 µmol/m/s, and 70–75%
natural light glasshouse conditions with a 16-h light period; they respectively. After 5 days in the growth chambers, plants were
were supplemented with artificial light (230W LED; Kroptek Ltd., moved back to the glasshouse until final harvest.
London, United Kingdom) if natural light intensity fell below
175 µmol/m2/s1. The temperature in the glasshouse was set at Morphological, Phenological, and
21◦C/15◦C (day/night, actual value: 21.5 ± 0.4/16.3 ± 0.5◦C)
and the relative humidity (RH) was around 60/75% (day/night) Physiological Measurements
(Supplementary Figure 1A). At the booting stage, plants with On the day before (day 0) and after (day 6) HT treatment,
the primary tiller reached the targeted AIL (Supplementary the primary tiller of each plant was tagged and measured
Figure 2A) of 6 cm (actual value for each genotype in for AIL. Plant height (PH) was also recorded at these two
Supplementary Figure 2B) and were sequentially moved into time points in Exp2 and Exp3 (Supplementary Figure 1G).
Fitotron Modular Plant Growth Chambers (HGC1514; Weiss Chlorophyll SPAD and Fv/Fm (maximum potential quantum
Technik UK Ltd., Loughborough, United Kingdom) for HT efficiency of Photosystem II) were measured at the same time
treatment (36.97 ± 0.03/26.95 ± 0.17◦C, day/night). The light as AIL and weekly thereafter (Supplementary Figure 1G). The
period was 16 h and the intensity was maintained around SPAD measurement was performed with an MC-100 Chlorophyll
600 µmol/m2/s1 at the plant level. The RH was maintained Concentration Meter (Apogee Instruments, Inc., Logan, UT,
between 70 and 75% (Supplementary Figure 1D). Plants for United States). Fv/Fm was measured with a Pocket PEA
CT treatment were kept in the glasshouse. After 5 days of (Hansatech Instruments Ltd., Norfolk, United Kingdom) after
HT treatment, heat-stressed plants were moved back to the 15–20 min dark adaptation. For each plant, the mean SPAD
glasshouse until final harvest. value of measurements at the tip, middle, and bottom of flag
leaf was obtained and one measurement of Fv/Fm was made in
Exp2 the middle of flag leaf. After the HT treatment, the heading date
This experiment was conducted between August and December of each plant was recorded to calculate days to heading in Exp2
of 2020 and with the same set of 14 genotypes (Supplementary and Exp3. Physiological maturity of the spike on the tagged tiller
Table 1). The experiment design and plant cultivation was recorded as days to maturation. These measurements were
conditions were similar as in Exp1. The temperature in the conducted with four biological replicates of each genotype and
glasshouse was also set at 21◦C/15◦C (day/night, actual value: treatment combination.
20.6 ± 0.8/15.4 ± 0.7◦C) and the RH was around 57/69%
(day/night) (Supplementary Figure 1B). When the AIL of the Measurement With Tagged Tillers/Spikes
primary tiller reached 2–3 cm (actual value for each genotype for Pollen Fertility and the Number of
in Supplementary Figure 2C), plants for HT treatment were
sequentially moved into the same growth chamber as Exp1 with Grains Per Spike
the temperature of 37.02 ± 0.01/27.00 ± 0.01◦C (day/night) During anthesis in Exp2 and Exp3, the fourth or fifth spikelet
(Supplementary Figure 1E). Plants for CT treatment were also (counted from the bottom) was sampled from the tagged tiller.
moved into a similar growth chamber with the temperature of One anther from two florets at the bottom was photographed for
21.01 ± 0.01/15.01 ± 0.01◦C (Supplementary Figure 1E). The a representative image and length of the anther was measured.
light period, intensity, and RH were similar between CT and HT In Exp3, the remaining five anthers from two florets at the
treatments with settings of 16 h, 600 µmol/m2/s1, and 70–75% bottom were pooled together for pollen viability analysis using
respectively. After 5 days in the growth chambers, plants were staining with Lugol’s solution. Fully stained pollen was scored as
moved back to the glasshouse until final harvest. viable, whereas partially stained or aberrant shaped pollen was
scored as non-viable. At maturity, the number of filled grains
Exp3 of the tagged spike was counted and recorded as the number
This experiment was conducted between January and May of of grains per spike, and also, spike length (cm) and number of
2021 and with 22 genotypes (Supplementary Table 1). The spikelets were measured. Four biological replicates were used for
experiment design and plant cultivation conditions were the these measurements.
same as the previous two experiments. The temperature in
the glasshouse was also set at 21◦C/15◦C (day/night, actual Measurement of Tillering Dynamics
value: 21.7 ± 0.4/15.4 ± 0.3◦C) and the RH was around In Exp1, development of extra young spikes after heat stress
42/49% (day/night) (Supplementary Figure 1C). When the was observed. In Exp2 and Exp3, tiller number was therefore
AIL of the primary tiller reached 2–3 cm (actual value in continuously counted for four biological replicates of CT and HT-
Supplementary Figure 2D), plants for HT treatment were treated plants of each genotype on the day (day 0) before and
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after (day 6) the 5-day HT treatment, and on weekly intervals RESULTS
thereafter until maximum tillering (Supplementary Figure 1G).
Heat-Impaired Pollen Fertility and
Yield-Related Measurements at Number of Grains Per Spike
Maturation To understand the effects of heat on pollen development and
At maturity, the spikes per plant were distinguished into “old” grain setting, the primary tiller of each plant was tagged and
spikes (labeled just before starting the HT treatment in Exp2 measured. In Exp1 and Exp2, the imposed severe heat treatment
and Exp3) and “new” spikes, harvested separately, and then of 37◦C/27◦C caused nearly complete loss of grain setting for
dried in oven at 40◦C for 7 days prior to mechanical threshing all genotypes, except for Paragon and Cadenza (Supplementary
and cleaning. The weight, number, length, and width were Figure 4). The anther morphology was also severely changed by
then determined for grain samples from old and new spikes the HT treatments indicating complete absence of viable pollen
separately with a scale and a MARViN digital seed analyzer (Figures 1A,B). In Exp3, relatively mild heat stress (34◦C/28◦C)
(MARViTECH GmbH., Wittenburg, Germany). Grain yield per also significantly reduced anther length; however, this was less
plant was calculated as the sum of grains from old and new severe compared with Exp2 (Figures 1A,B) and pollen viability
spikes. The aboveground biomass for each plant was determined was therefore analyzed by staining with Lugol’s solution. The
as the weight of all straw materials dried in an oven at 80◦C for results showed considerable variation among genotypes, ranging
48 h. The yield-related measurements were analyzed with four from 0 to 60%. One line (SWBL1.1, a progeny between the
biological replicates. cross of Sokoll and Weebill1) had the highest pollen viability
(relative to control value), followed by SWES, SUN (Sunstar),
Statistical Analysis and WBL1.2 (Weebill1) (Figure 1C). The number of grains
The data from the time course SPAD measurements were fitted of the tagged primary spike was also variable among the
using a generalized additive model (GAM) for each of the genotypes, with SUN showing the highest value relative to control
three experiments to estimate maximum SPAD (SPADmax), value (Figure 1D). Further analysis found a positive correlation
senescence onset (SenOnset), and senescence rate (SenRate) between pollen viability and the number of grains per spike under
(Supplementary Figure 3). SPAD was predicted by a smooth HT (Figure 1F), but not under CT treatment (Figure 1E).
function of time (days counted from stress initiation), with a
separate smooth function fitted for each combination of genotype Heat-Stimulated Tillering/Spike
and treatment. The Exp1 model used eight basis functions,
whereas Exp2 and Exp3 used seven basis functions. SPADmax Formation and Its Association With Yield
was estimated from the fitted predicted model. SenOnset was During the ripening stage of Exp1, the senescence status of
calculated as the day that SPAD fell to 95% of the maximum tillers/spikes was clearly separated into two groups (Figure 2A)
SPAD. Senescence period was defined over 14 days from the onset and tillers were therefore distinguished into old (pre-heat) and
or until the end of the measurement, whichever was shorter. new (post-heat) spikes for each plant. About 1 week after heat
SenRate was then calculated as the daily reduction of SPAD over treatment, new tiller outgrowth was noticed from the bottom of
the senescence period. GAMs were fitted in R package (version HT-stressed plants (Figures 2B,C). A final count of spikes found
3.6.1) using the “mgcv” package (version 1.8-35) (Wood, 2011). significantly more new spikes in the HT-treated plants compared
All trait measurements and calculated parameters with the CT plants in Exp1 (p < 0.001), Exp2 (p < 0.001), and
(Supplementary Table 2) were used for statistical analysis Exp3 (p < 0.001) (Figures 2D–F), while the number of old spikes
in R 4.0.3.1. First, descriptive statistics were summarized with was similar between HT and CT conditions (Supplementary
the “describeBy” from the “psych” package (Revelle, 2020). Figure 5). In addition, there was no significant interaction
The effects of genotype treatment and the interaction were between treatment and genotype (Figures 2D–F), indicating that
obtained from ANOVA with the model fitted with “lmer” from all genotypes responded similarly to the HT treatment in terms
the R package “lmerTest” (Kuznetsova et al., 2017); genotype, of new spike formation. The analysis of tillering dynamics in
treatment, and their interaction were treated as fixed factors, Exp2 and Exp3 showed that onset of new tiller development
while block and genotype nested in block were treated as commenced at 2–3 weeks after the HT treatment, with a
random effects. Later, Tukey’s post hoc test was carried out stronger effect observed in Exp2 (Figures 2G,H). Moreover, the
for multiple test comparisons to identify genotypic variation. more severe heat stress in Exp2 (37◦C/27◦C) also caused tiller
Estimated marginal means were calculated for each combination retardation on day 6, 1 day after the end of the HT treatment
of genotype and treatment. Subsequently, for either CT or HT (Figure 2G), but this was not observed under the milder heat
treatment, Pearson correlation coefficient table was calculated stress condition in Exp3 (34◦C/28◦C) (Figure 2H).
by using “tab_corr” from “sjPlot” package (Lüdecke, 2021) As new tillers developed after the HT treatment and
among measurements and pairwise-deletion method was used to extended the days to maturity of the plants, the aboveground
account for missing data. For each experiment and temperature biomass per plant (including both old and new tillers) was
treatment, correlations among different traits were visualized as very similar between HT and CT treatments (Figures 3A–C).
networks with the “qgraph” package (Epskamp et al., 2012). Nevertheless, the overall grain yield per plant was significantly
reduced after the HT treatment in all three experiments
1https://www.R-project.org/ (p < 0.001 for all) (Figures 3D–F). This was primarily due
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FIGURE 1 | The heat effects on wheat reproductive traits. Anther morphology after heat treatments in two representative genotypes is shown in (A, bar = 1 mm).
Average anther length across all analyzed genotypes in Exp2 (37/27◦C) and Exp3 (34/28◦C) is shown in (B). Genotypic variation of pollen viability (C) and the
number of grains per spike (D) under heat in Exp3. Representative pollen images for CT, HT-tolerant, and HT-sensitive were inserted (C, bar = 100 µm). The data
were obtained from the primary tiller and calculated as relative to control values, which are shown on the top of each bar. Pearson correlation between pollen viability
and number of grains per spike under control (E) and heat (F). Significance level: ∗∗∗p < 0.001; ∗∗p < 0.01; ∗p < 0.05; ∗p < 0.05.
to heat-induced sterility in the old spikes (Figures 3G–I). reduced by limited seed setting of old spikes under HT
However, heat-induced formation of new spikes gave rise to condition, source supply became more than sufficient for the
similar (Exp2, Figure 3K) or even significantly higher grain survived developing grains, and their width and length were
yield from new spikes in Exp1 and Exp3 (Figures 3J,L). significantly higher than grains of old spikes from control plants
The proportion of yield from new spikes after the HT (Supplementary Table 2). By contrast, the grains from new
treatment was therefore significantly higher than under CT spikes showed variable responses in terms of width and length
conditions (Supplementary Figure 6). As sink size was (Supplementary Table 2).
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FIGURE 2 | The effects of heat treatments on tillering/spike formation. After heat (HT) treatment, new tillers/spikes (in yellow ellipse) were vigorously stimulated, while
controls were not (CT, A). Tiller outgrowth from CT (B) and HT (C) around 1 week after stress treatment. A comparison of the number of new spikes between CT and
HT in Exp1 (D), Exp2 (E), and Exp3 (F). The effects of genotype/G, treatment/T, interaction/G × T were indicated for each panel. Dynamic change of tillering before
(day 0), after (day 6) the 5-day HT treatment (days 1–5), and weekly intervals in Exp2 (G) and Exp3 (H). Significance level: ***p < 0.001; **p < 0.01.
Heat Effects on Plant Morphology, compared with the CT of 21◦C/15◦C (Figures 4A,B,D). In
Phenology, and Chlorophyll Dynamics contrast, the AIL (p = 0.065) and PH (p = 0.279) were
When wheat plants were exposed to heat stress during the marginally affected under the milder HT of 34◦C/28◦C in Exp3
early booting stage, the increase in AIL (p < 0.001 for (Figures 4C,E). HT treatments also changed plant phenology
Exp1 and Exp2) and PH (p < 0.001 Exp2) during the 5-day as indicated by the significantly reduced number of days to
treatments was significantly reduced by the HT of 37◦C/27◦C heading (DTH) (p < 0.001 for Exp2 and Exp3) (Figures 4F,G)
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between CT and HT treatments. On day 6 (1 day after treatment),
in comparison to the corresponding CT conditions, SPAD value
was significantly reduced by the severe heat (37◦C/27◦C) in
Exp1 (Figure 5A) and Exp2 (Figure 5B), but surprisingly
increased slightly after the mild heat (34◦C/28◦C) in Exp3 and
maintained a higher maximum SPAD value (Figures 5E,F).
At later stages, however, an accelerated decrease in SPAD
was observed under HT conditions in all three experiments,
irrespective of heat stress intensity (Figures 5A,B,E). Based
on the time course of SPAD measurements, GAMs were fitted
to estimate maximum SPAD (SPADmax), senescence onset
(SenOnset), and senescence rate (SenRate) for each combination
of genotype and treatment. In Exp1 and Exp3, SenOnset from
HT treatment was reproducibly and significantly advanced
in comparison with CT conditions, whereas SenRate was
similar between treatments (Figures 5C,F). By contrast, Exp2
showed an opposite response with similar SenOnset between
treatments, but an increased SenRate under HT (Figure 5D).
This variation between the three experiments may be due
to variable intensities of natural sunlight. Even within the
same experiment, some genotypes showed earlier SenOnset,
while others showed faster SenRate under HT treatment
(Supplementary Figures 7–9). In addition, the Fv/Fm value at
day 6 was always significantly reduced by HT treatment in all
three experiments indicating a negative effect of the HT on PSII
(Supplementary Figure 10).
Analysis of Trait Correlations From
Different Experiments and Temperature
Conditions
To understand the relationships among different traits across
genotypes, correlations were calculated (Supplementary Table 3)
and visualized as networks (Figure 6). Number of grain per
spike (GpS) showed different correlations under control and HT
conditions; In Exp1 and Exp2, there was no correlation between
GpS and any other trait under HT, but under CT, it was strongly
and positively correlated with the number of spikelets (SpikeletN)
(r = 0.98∗∗∗ for Exp1 and 0.81∗∗ for Exp2) and length (SpikeL)
(r = 0.94∗∗∗ for Exp1 and 0.79∗∗ for Exp2) of the tagged spike, as
well as with biomass (r = 0.88∗∗∗) and yield (r = 0.88∗∗∗) in Exp1.
In Exp3, GpS was also associated with different traits between CT
and HT. The importance of induced new tillers and spikes after
heat stress was corroborated by the reproducible strong positive
correlations (r = 0.98∗∗∗, 0.92∗∗∗, 0.80∗∗∗ for Exp1, Exp2, and
Exp3, respectively) between grain yield of new tillers (GY.NT)
FIGURE 3 | Average values of wheat genotypes grown under high and total grain yield (GY), observed in all three experiments
temperature (HT) or control (CT) across the three experiments are shown for (Figure 6 and Supplementary Table 3). This suggests a critical
biomass (A–C), grain yield per plant (D–F), grain yield from old spikes (G–I), role of new spikes in mitigating heat-induced yield reduction.
and grain yield from new spikes (J–L). The effects of genotype (G), treatment In addition, the morphological traits, increase in AIL and PH,
(T), and interaction (G × T) are indicated for each panel. were generally positively correlated with yield or biomass-related
traits, regardless of temperature treatments. Ultimately, SPAD
and Fv/Fm parameters were not consistently correlated with
and days to maturation (DTM) (p < 0.001 for Exp1, Exp2, and other traits from different experiments and treatments. In Exp1,
Exp3) (Figure 4H). SenOnset showed HT-specific weak positive correlations with a
To understand the physiological basis of changes in grain yield of old tillers (GY.OT) (r = 0.62∗) and a spike number
phenology, dynamic changes in SPAD and Fv/Fm were compared of new tillers (SpikeN.NT) (r = 0.69∗); SenRate was closely related
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FIGURE 4 | The heat effects on plant morphology and phenology. Comparison of the effect of heat (HT) and control (CT) treatments on the increase of auricle
interval length (AIL, A–C), the increase in plant height (D,E), days to heading (F,G), and days to maturation (H).
to yield traits in both Exp2 (r = 0.62∗ with GY.NT under CT; temperature (34◦C/28◦C) treatment, suggesting that both stress
r = 0.79∗∗ with GY.NT and 0.69∗ with GY under HT) and Exp3 intensity and duration are critical to screening reproductive
(r = 0.47∗ with GY and 0.53∗ with SpikeL under CT; r = 0.45∗ heat tolerance. Under the 34◦C/28◦C condition, pollen viability
with GpS and 0.49∗ with SpikeL under HT), but not heat-specific; was considerably variable among genotypes. Two of the lines
in Exp2, SPADmax was important, as it was strongly correlated (SWB1.1 and SWES) with high pollen viability share one
with Spikelet (r = 0.66∗ under CT, 0.75∗∗ under HT) and SpikeL common parent, Sokoll, in their pedigree. Sokoll is an advanced
(r = 0.70∗ under CT, 0.74∗∗ under HT) of tagged spike (Figure 6 wheat line derived from synthetic hexaploid wheat and has
and Supplementary Table 3). shown a yield advantage under terminal heat stress in other
reports (Cossani and Reynolds, 2015; Thistlethwaite et al., 2020),
although it did not show particularly high pollen viability
DISCUSSION after early booting-stage heat stress in this study. These results
suggest stage-specific heat tolerance; therefore, it is necessary
Importance and Limitation of Pollen to pyramid tolerant traits across different developmental stages.
Another parental line included in this study, Weebill1 (WBL1.1
Viability as a Target Trait for Wheat Heat and WBL1.2), has previously been reported to be tolerant
Research to a wide range of variable environmental conditions (Singh
In the present study, anther morphology was gradually affected et al., 2007). One of the most tolerant genotypes identified
under two levels of heat stress, 34◦C/28◦C (day/night) and in this study was Sunstar, in agreement with data reported
37◦C/27◦C, applied for 5 days during early booting stage by Erena (2018) who also demonstrated the reproductive heat
coinciding with pollen development. The more severe heat tolerance of Sunstar. These identified genotypes with heat
stress condition in this study led to a complete loss of pollen tolerance during pollen development may be suitable donors
viability, while results from a parallel study, in which the for breeding and warrant further studies to understand the
same 37◦C/27◦C heat treatment was applied that lasted for underlying genetic and molecular-physiological mechanisms.
only 3 days (Erena, 2018), were similar to the 5-day, milder The importance of pollen viability is supported by its positive
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Xu et al. Novel Sources & Traits for Heat-Tolerant Wheat
FIGURE 5 | The effects of heat on SPAD (chlorophyll content index) and leaf senescence parameters. Comparison of the effect of heat (HT) and control (CT)
treatments on the dynamic change of SPAD measured before (day 0) and 1 day after (day 6) a 5-day HT treatment, and in weekly intervals thereafter in Exp1 (A),
Exp2 (B), and Exp3 (E). Senescence-related parameters, SPADmax (maximum SPAD value), SenOnset (Senescence onset day), and SenRate (Senescence rate),
were compared between CT and HT for Exp 1 (C), Exp2 (D), and Exp3 (F). Significance level: ∗∗∗p < 0.001; ∗∗p < 0.01; ∗p < 0.05.
correlation with the number of grains per spike under heat thus important to consider genotypic differences and carefully
stress. Interestingly, similar relationships have been reported target meiosis to microspore stage when applying heat stress to
in other crops (Xu et al., 2017; Shi et al., 2018) and abiotic exclude confounding effects. Currently, the most widely used
stresses (Ji et al., 2010), indicating that pollen fertility is a morphological marker for pollen developmental stage is AIL,
general limiting factor for final grain number under suboptimal which is also known as auricle distance (Ji et al., 2010; Erena,
growth conditions. Therefore, it should be an important target 2018; Bokshi et al., 2021). However, AIL corresponding to
trait for heat-related research and breeding. Nevertheless, the a specific pollen developmental stage varies among different
response of pollen viability to heat stress is highly dependent genotypes (Erena, 2018) and must be determined for each
on the developmental stage when stress is applied (Saini and genotype, which is laborious. Fortunately, progress has been
Aspinall, 1982; Prasad and Djanaguiraman, 2014) and it is made by non-destructive X-ray micro-computed tomography
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Xu et al. Novel Sources & Traits for Heat-Tolerant Wheat
FIGURE 6 | The effects of heat on trait relationships across different experiments. Correlation networks for Exp1 (A,B), Exp2 (C,D), and Exp3 (E,F). Only significant
correlations are shown and the width of the edges indicated correlation r-value. Orange solid edges represent positive correlations, while blue dashed edges
represent negative correlations. Trait abbreviations: SPADres: (SPAD at day 6—SPAD at day 0)/SPAD at day 0; Fv/Fmres: (Fv/Fm at day 6 -Fv/Fm at day 0)/(Fv/Fm at
day 0); SPADmax, maximum value of SPAD; SenOnset, senescence onset time; SenRate, senescence rate; AILincrease, auricle interval length increase during the
5-day treatment; PHincrease, plant height increase during the 5-day treatment; PS, observed frequency of paired spikelet from all spikes; SR, observed frequency of
sham ramification from all spikes; DTH, days to heading; DTM, days to maturation; SpikeL, spike length (tagged primary spike); SpikeletN, number of spikelets
(tagged primary spike); GpS, number of grains per spike (tagged primary spike); SpikeN.OT, number of spikes from old tillers; SpikeN.NT, number of spikes from
new tillers; GY.OT, grain yield of old tillers; GY.NT, grain yield of new tillers; GY, grain yield per plant (sum of old and new tillers); Biomass, the dry weight of all straw
per plant; PV, pollen viability from the middle spikelet of tagged spike.
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Xu et al. Novel Sources & Traits for Heat-Tolerant Wheat
scanning (Fernández-Gómez et al., 2020), and integrating fast nutrient remobilization in high-yielding lines. Finally,
this with modeling could be a promising way to overcome both SPAD and Fv/Fm were reduced by heat immediately
difficulties with accurate identification of developmental stages after the treatment (day6) in Exp1 and Exp2, but the mild
of wheat pollen. temperature of 34◦C/28◦C only decreased Fv/Fm, not SPAD.
These results indicate that Fv/Fm may be more sensitive and
Utilizing Developmental Plasticity to therefore a better parameter for heat tolerance evaluation (Cao
Mitigate Heat Effects on Yield et al., 2019). Therefore, these senescence-related parameters
The number of spikes per plant, interacting with spikelet are useful for crop phenotyping, and integrating modeling
number and floret fertility, determines grain number and with high-throughput imaging measurements will enable large-
thereby final yield. Our data show that a short episode of scale analysis.
heat stress during early booting stage induced the development
of new tillers and spikes, which is in agreement with other
studies (Bányai et al., 2014; Chavan et al., 2019; Hütsch CONCLUSION
et al., 2019). Although tillering was initially inhibited under
severe heat stress, new tillers started emerging at 2 weeks In this study, a spring wheat panel, including heat-tolerant
after recovery, corresponding to about 1 week after anthesis. elite varieties and their pre-breeding lines, was dissected for
This timing suggests that available photosynthates stored in reproductive, developmental, physiological, and yield responses
vegetative tissue that cannot be translocated into grain due to along with their inter-relationships after a 5-day heat stress
spikelet sterility can be reallocated into the development of application during the early booting stage. In comparison with
new tillers and spikes. Additional photo-assimilates for new the control treatment, pollen viability from the tagged primary
tillers and spikes would be produced during recovery and spike was significantly decreased by heat and subsequently
this is reflected by its positive correlation with delayed onset reduced number of grains per spike. The heat stress, however,
of senescence (Figure 6C). The observed formation of new resulted in late tillering after the disruption of sink strength.
spikes after heat stress compensating for heat-induced biomass Consequently, more new spikes were formed contributing
and yield losses under controlled environment conditions now to final yield and biomass, though an additional week was
needs to be corroborated under field conditions to ensure that needed for the maturation of the late tillers. Flag leaf SPAD
it is a valid target trait for breeding. In addition, a higher (Chlorophyll content index) and Fv/Fm (maximum potential
frequency of paired spikelets (Boden et al., 2015) and sham quantum efficiency of Photosystem II) were reduced by heat
ramification (Amagai et al., 2017) was observed in heat-treated stress. Model fitting with time course SPAD measurements
plants and this may also be related to excessive source supply. showed accelerated leaf senescence by either earlier onset or
Although these traits were not correlated with yield, they faster senescence rate, and these parameters were associated
could contribute to understand mechanisms underlying such with yield traits. Ongoing genomic and genetic studies will
developmental abnormalities. subsequently be used to dissect the mechanism of identified heat-
tolerant genotypes (Sunstar, SWBL1.1). Taken together, these
Accelerated Leaf Senescence After Brief reproductive, developmental, and physiological traits could be
Heat Stress During Early Booting Stage further used as targets for understanding basic mechanisms and
breeding heat-tolerant wheat.
Screening wheat for heat tolerance in the field is generally
implemented by late-sowing to impose continuous terminal
heat stress during grain filling, often resulting in accelerated
leaf senescence (Bergkamp et al., 2018). In the present DATA AVAILABILITY STATEMENT
study, a similar stimulation of flag leaf senescence was
observed after a brief episode of heat stress was applied The original contributions presented in the study are included
during early booting. It is possible that plants are able to in the article/Supplementary Material, further inquiries can be
measure and memorize phenology or leaf age to program directed to the corresponding author/s.
the senescence process (Woo et al., 2019). In our study,
model fitting using SPAD time course data proved to be
successful in identifying senescence parameters. Both earlier AUTHOR CONTRIBUTIONS
onset and faster senescence rate were identified and were
closely related to accelerated leaf senescence, in agreement with SH conceived and supervised the project, together with EV-S and
similar results reported by Šebela et al. (2020). Heat-specific MP. JX designed and implemented the experiments and analyzed
positive correlations between senescence onset (SenOnset), the data, with support from CL. MR and SD advised on the
new spike formation (SpikeN.NT), and yield of old tillers selection of genotypes included in this study and provided the
(GY.OT) in Exp1 support the important role of late senescence. seeds. SH, EV-S, SH-L, and MP held regular project planning
The observed positive associations between senescence rate discussions. JX wrote the manuscript, which was reviewed and
(SenRate) and yield traits (grain yield/GY, number of grains edited by SH, CL, MR, SD, EV-S, SH-L, and MP. All authors
per spike/GpS, spike length/SpikeL) in Exp2 and Exp3 suggest contributed to the article and approved the submitted version.
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Xu et al. Novel Sources & Traits for Heat-Tolerant Wheat
FUNDING Dale for advice on the experimental setup. We would also like
to thank Fiona Gilzean, Jill Maple, and Jack Turner for taking
This project was funded by the BBSRC UK-Mexico Newton excellent care of the plants and for their technical support,
Fund (BB/S012885/1 “Safeguarding Sonora’s Wheat from as well as Chris Hall for helping with the sample processing.
Climate Change”). SH and MP were supported by the Seeds were kindly provided by the CIMMYT and Nick Collins,
Designing Future Wheat (DFW) Institute Strategic Programme University of Adelaide.
(BB/P016855/1) and SH by NIAB.
SUPPLEMENTARY MATERIAL
ACKNOWLEDGMENTS
The Supplementary Material for this article can be found
We would like to thank Tess Rose and Maria Oszvald for their online at: https://www.frontiersin.org/articles/10.3389/fpls.2022.
support and suggestions on the manuscript, as well as Matthew 886541/full#supplementary-material
REFERENCES Cossani, C. M., and Reynolds, M. P. (2015). Heat stress adaptation in elite lines
derived from synthetic hexaploid wheat. Crop Sci. 55, 2719–2735. doi: 10.2135/
Amagai, Y., Gowayed, S., Martinek, P., and Watanabe, N. (2017). The third glume cropsci2015.02.0092
phenotype is associated with rachilla branching in the spikes of tetraploid wheat Draeger, T., and Moore, G. (2017). Short periods of high temperature during
(Triticum L.). Genet. Resour. Crop Evol. 64, 835–842. doi: 10.1007/s10722-017- meiosis prevent normal meiotic progression and reduce grain number in
0503-7 hexaploid wheat (Triticum aestivum L.). Theor. Appl. Genet. 130, 1785–1800.
Azam, F. I, Chang, X., and Jing, R. (2015). Mapping QTL for chlorophyll doi: 10.1007/s00122-017-2925-1
fluorescence kinetics parameters at seedling stage as indicators of heat tolerance Dwivedi, S. K., Basu, S., Kumar, S., Kumari, S., Kumar, A., Jha, S., et al. (2017). Heat
in wheat. Euphytica 202, 245–258. doi: 10.1007/s10681-014-1283-1 stress induced impairment of starch mobilisation regulates pollen viability and
Bányai, J., Karsai, I., Balla, K., Kiss, T., Bedö, Z., and Láng, L. (2014). Heat stress grain yield in wheat: study in Eastern Indo-Gangetic Plains. Field Crop Res. 206,
response of wheat cultivars with different ecological adaptation. Cereal Res. 106–114. doi: 10.1016/J.FCR.2017.03.006
Commun. 42, 413–425. doi: 10.1556/CRC.42.2014.3.5 Epskamp, S., Cramer, A. O. J., Waldorp, L. J., Schmittmann, V. D., and Borboom,
Begcy, K., Weigert, A., Egesa, A. O., and Dresselhaus, T. (2018). Compared to D. (2012). {qgraph}: network visualizations of relationships in psychometric
australian cultivars, european summer wheat (Triticum aestivum) overreacts data. J. Stat. Softw. 48, 1–18.
when moderate heat stress is applied at the pollen development stage.Agronomy Erena, M. F. (2018). Genetic and Physiological Bases of Heat-Induced Floret Sterility
8:99. doi: 10.3390/agronomy8070099 in Wheat. Adelaide: University of Adelaide.
Bergkamp, B., Impa, S. M., Asebedo, A. R., Fritz, A. K., and Jagadish, S. V. K. (2018). Erena, M. F., Lohraseb, I., Munoz-Santa, I., Taylor, J. D., Emebiri, L. C., and Collins,
Prominent winter wheat varieties response to post-flowering heat stress under N. C. (2021). The WtmsDW locus on wheat chromosome 2B controls major
controlled chambers and field based heat tents. Field Crop Res. 222, 143–152. natural variation for floret sterility responses to heat stress at booting stage.
doi: 10.1016/j.fcr.2018.03.009 Front. Plant Sci. 12:376. doi: 10.3389/FPLS.2021.635397/BIBTEX
Bheemanahalli, R., Sunoj, V. S. J., Saripalli, G., Prasad, P. V. Vara, Balyan, H. S., Fernández-Gómez, J., Talle, B., Tidy, A. C., and Wilson, Z. A. (2020).
Gupta, P. K., et al. (2019). Quantifying the impact of heat stress on pollen Accurate staging of reproduction development in Cadenza wheat by non-
germination, seed set, and grain filling in spring wheat. Crop Sci. 59, 684–696. destructive spike analysis. J. Exp. Bot. 71, 3475–3484. doi: 10.1093/jxb/era
doi: 10.2135/CROPSCI2018.05.0292 a156
Bhusal, N., Sharma, P., Sareen, S., and Sarial, A. K. (2018). Mapping QTLs for Hassan, F. S. C., Solouki, M., Fakheri, B. A., Nezhad, N. M., and Masoudi, B. (2018).
chlorophyll content and chlorophyll fluorescence in wheat under heat stress. Mapping QTLs for physiological and biochemical traits related to grain yield
Biol. Plant 62, 721–731. doi: 10.1007/s10535-018-0811-6 under control and terminal heat stress conditions in bread wheat (Triticum
Boden, S. A., Cavanagh, C., Cullis, B. R., Ramm, K., Greenwood, J., Jean Finnegan, aestivum L.). Physiol. Mol. Biol. Plants 24:1231. doi: 10.1007/S12298-018-0
E., et al. (2015). Ppd-1 is a key regulator of inflorescence architecture and paired 590-8
spikelet development in wheat. Nat. Plants 1, 1–6. doi: 10.1038/nplants.2014.16 Hütsch, B. W., Jahn, D., and Schubert, S. (2019). Grain yield of wheat (Triticum
Bokshi, A. I., Tan, D. K. Y., Thistlethwaite, R. J., Trethowan, R., and Kunz, K. aestivum L.) under long-term heat stress is sink-limited with stronger inhibition
(2021). Impact of elevated CO2and heat stress on wheat pollen viability and of kernel setting than grain filling. J. Agron. Crop Sci. 205, 22–32. doi: 10.1111/
grain production. Funct. Plant Biol. 48, 503–514. doi: 10.1071/FP20187 JAC.12298
Browne, R. G., Li, S. F., Iacuone, S., Dolferus, R., and Parish, R. W. (2021). Ji, X., Shiran, B., Wan, J., Lewis, D. C., Jenkins, C. L., Condon, A. G., et al. (2010).
Differential responses of anthers of stress tolerant and sensitive wheat cultivars Importance of pre-anthesis anther sink strength for maintenance of grain
to high temperature stress. Planta 254:4. doi: 10.1007/s00425-021-03656-7 number during reproductive stage water stress in wheat. Plant Cell Environ. 33,
Cai, C., Yin, X., He, S., Jiang, W., Si, C., Struik, P. C., et al. (2016). Responses 926–942. doi: 10.1111/j.1365-3040.2010.02130.x
of wheat and rice to factorial combinations of ambient and elevated CO2 Kumar, P., Gupta, V., Singh, G., Dhakar, R., and Ramakrishnan, R. S. (2021).
and temperature in FACE experiments. Glob. Change Biol. 22, 856–874. doi: Assessment of terminal heat tolerance based on agro-morphological and stress
10.1111/gcb.13065 selection indices in wheat. Cereal Res. Commun. 49, 217–226. doi: 10.1007/
Cao, Z., Yao, X., Liu, H., Liu, B., Cheng, T., Tian, Y., et al. (2019). Comparison s42976-020-00112-2
of the abilities of vegetation indices and photosynthetic parameters to detect Kuznetsova, A., Brockhoff, P. B., and Christensen, R. H. B. (2017). {lmerTest}
heat stress in wheat. Agric. For. Meteorol. 265, 121–136. doi: 10.1016/J. package: tests in linear mixed effects models. J. Stat. Softw. 82, 1–26. doi: 10.
AGRFORMET.2018.11.009 18637/jss.v082.i13
Chavan, S. G., Duursma, R. A., Tausz, M., and Ghannoum, O. (2019). Elevated Liu, B., Asseng, S., Müller, C., Ewert, F., Elliott, J., Lobell, D. B., et al. (2016). Similar
CO2 alleviates the negative impact of heat stress on wheat physiology but not estimates of temperature impacts on global wheat yield by three independent
on grain yield. J. Exp. Bot. 70, 6447–6459. doi: 10.1093/JXB/ERZ386 methods. Nat. Clim. Change 6, 1130–1136. doi: 10.1038/nclimate3115
Cossani, C. M., and Reynolds, M. P. (2012). Physiological traits for improving heat Lüdecke, D. (2021). sjPlot: Data Visualization for Statistics in Social Science Version
tolerance in wheat. Plant Physiol. 160, 1710–1718. doi: 10.1104/pp.112.207753 2.8.10.
Frontiers in Plant Science | www.frontiersin.org 12 May 2022 | Volume 13 | Article 886541
fpls-13-886541 May 10, 2022 Time: 16:52 # 13
Xu et al. Novel Sources & Traits for Heat-Tolerant Wheat
Mirosavljević, M., Mikić, S., Župunski, V., Špika, A. K., Trkulja, D., Ottosen, C. O., environment. Field Crop Res. 157, 71–83. doi: 10.1016/j.fcr.2013.
et al. (2021). Effects of high temperature during anthesis and grain filling on 12.004
physiological characteristics of winter wheat cultivars. J. Agron. Crop Sci. 207, Stone, P. J., and Nicolas, M. E. (1995). Effect of timing of heat stress during grain
823–832. doi: 10.1111/jac.12546 filling on two wheat varieties differing in heat tolerance. I. Grain growth. Aust.
Murchie, E. H., and Lawson, T. (2013). Chlorophyll fluorescence analysis: a guide J. Plant Physiol. 22, 927–934. doi: 10.1071/PP9950927
to good practice and understanding some new applications. J. Exp. Bot. 64, Talukder, A. S. M. H. M., McDonald, G. K., and Gill, G. S. (2014). Effect of short-
3983–3998. doi: 10.1093/jxb/ert208 term heat stress prior to flowering and early grain set on the grain yield of wheat.
Omidi, M., Siahpoosh, M. R., Mamghani, R., and Modarresi, M. (2014). The Field Crop Res. 160, 54–63. doi: 10.1016/J.FCR.2014.01.013
influence of terminal heat stress on meiosis abnormalities in pollen mother cells Thistlethwaite, R. J., Tan, D. K. Y., Bokshi, A. I., Ullah, S., and Trethowan, R. M.
of wheat. Cytologia 79, 49–58. doi: 10.1508/cytologia.79.49 (2020). A phenotyping strategy for evaluating the high-temperature tolerance
Pequeno, D. N. L., Hernández-Ochoa, I. M., Reynolds, M., Sonder, K., Molero- of wheat. Field Crop Res 255:107905. doi: 10.1016/j.fcr.2020.107905
Milan, A., and Robertson, R. (2021). Climate impact and adaptation to heat Touzy, G., Lafarge, S., Redondo, E., Lievin, V., Decoopman, X., Le Gouis, J., et al.
and drought stress of regional and global wheat production. Environ. Res. Lett. (2022). Identification of QTLs affecting post-anthesis heat stress responses in
16:54070. doi: 10.1088/1748-9326/abd970 European bread wheat. Theor. Appl. Genet. 135, 947–964. doi: 10.1007/S00122-
Pinto, R. S., Lopes, M. S., Collins, N. C., and Reynolds, M. P. (2016). Modelling 021-04008-5
and genetic dissection of staygreen under heat stress. Theor. Appl. Genet. 129, Trnka, M., Rötter, R. P., Ruiz-Ramos, M., Kersebaum, K. C., Olesen, J. E., Žalud,
2055–2074. doi: 10.1007/s00122-016-2757-4 Z., et al. (2014). Adverse weather conditions for European wheat production
Prasad, P. V. V., and Djanaguiraman, M. (2014). Response of floret fertility and will become more frequent with climate change. Nat. Clim. Change 4, 637–643.
individual grain weight of wheat to high temperature stress: sensitive stages doi: 10.1038/nclimate2242
and thresholds for temperature and duration. Funct. Plant Biol. 41, 1261–1269. Woo, H. R., Kim, H. J., Lim, P. O., and Nam, H. G. (2019). Leaf senescence:
doi: 10.1071/FP14061 systems and dynamics aspects. Annu. Rev. Plant Biol. 70, 347–376. doi: 10.1146/
Revelle, W. (2020). psych: Procedures for Psychological, Psychometric, and annurev-arplant-050718-095859
Personality Research Version 2.2.3. Wood, S. N. (2011). Fast stable restricted maximum likelihood and marginal
Richardson, A. D., Duigan, S. P., and Berlyn, G. P. (2002). An evaluation of likelihood estimation of semiparametric generalized linear models. J. R. Stat.
noninvasive methods to estimate foliar chlorophyll content. New Phytol. 153, Soc. Series B 73, 3–36. doi: 10.1111/j.1467-9868.2010.00749.x
185–194. doi: 10.1046/j.0028-646X.2001.00289.x Xu, J., Wolters-Arts, M., Mariani, C., Huber, H., and Rieu, I. (2017). Heat stress
Rieu, I., Twell, D., and Firon, N. (2017). Pollen development at high temperature: affects vegetative and reproductive performance and trait correlations in tomato
from acclimation to collapse. Plant Physiol. 173, 1967–1976. doi: 10.1104/pp.16. (Solanum lycopersicum). Euphytica 213:156. doi: 10.1007/s10681-017-1949-6
01644 Yeh, C. H., Kaplinsky, N. J., Hu, C., and Charng, Y. Y. (2012). Some like it hot,
Sade, N., Del Mar Rubio-Wilhelmi, M., Umnajkitikorn, K., and Blumwald, E. some like it warm: phenotyping to explore thermotolerance diversity. Plant Sci.
(2018). Stress-induced senescence and plant tolerance to abiotic stress. J. Exp. 195, 10–23. doi: 10.1016/j.plantsci.2012.06.004
Bot. 69, 845–853. doi: 10.1093/jxb/erx235 Zampieri, M., Ceglar, A., Dentener, F., and Toreti, A. (2017). Wheat yield loss
Saini, H. S., and Aspinall, D. (1982). Abnormal sporogenesis in wheat (Triticum attributable to heat waves, drought and water excess at the global, national
aestivum L.) induced by short periods of high temperature. Ann. Bot. 49, and subnational scales. Environ. Res. Lett. 12:064008. doi: 10.1088/1748-9326/
835–846. doi: 10.1093/OXFORDJOURNALS.AOB.A086310 aa723b
Šebela, D., Bergkamp, B., Somayanda, I. M., Fritz, A. K., and Krishna Jagadish, S. V. Zinn, K. E., Tunc-Ozdemir, M., and Harper, J. F. (2010). Temperature stress
(2020). Impact of post-flowering heat stress in winter wheat tracked through and plant sexual reproduction: uncovering the weakest links. J. Exp. Bot. 61,
optical signals. Agron. J. 112, 3993–4006. doi: 10.1002/AGJ2.20360 1959–1968. doi: 10.1093/jxb/erq053
Sharma, D., Singh, R., Rane, J., Gupta, V. K., Mamrutha, H. M., and Tiwari, R.
(2016). Mapping quantitative trait loci associated with grain filling duration and Conflict of Interest: The authors declare that the research was conducted in the
grain number under terminal heat stress in bread wheat (Triticum aestivum L.). absence of any commercial or financial relationships that could be construed as a
Plant Breed. 135, 538–545. doi: 10.1111/pbr.12405 potential conflict of interest.
Shi, W., Li, X., Schmidt, R. C., Struik, P. C., Yin, X., and Jagadish, S. V. K. (2018).
Pollen germination and in vivo fertilization in response to high-temperature Publisher’s Note: All claims expressed in this article are solely those of the authors
during flowering in hybrid and inbred rice. Plant Cell Environ. 41, 1287–1297. and do not necessarily represent those of their affiliated organizations, or those of
doi: 10.1111/pce.13146 the publisher, the editors and the reviewers. Any product that may be evaluated in
Shirdelmoghanloo, H., Cozzolino, D., Lohraseb, I., and Collins, N. C. (2016). this article, or claim that may be made by its manufacturer, is not guaranteed or
Truncation of grain filling in wheat (Triticum aestivum) triggered by brief endorsed by the publisher.
heat stress during early grain filling: association with senescence responses
and reductions in stem reserves. Funct. Plant Biol. 43, 919–930. doi: 10.1071/ Copyright © 2022 Xu, Lowe, Hernandez-Leon, Dreisigacker, Reynolds, Valenzuela-
FP15384 Soto, Paul and Heuer. This is an open-access article distributed under the terms
Singh, R. P., Huerta-Espino, J., Sharma, R., Joshi, A. K., and Trethowan, R. (2007). of the Creative Commons Attribution License (CC BY). The use, distribution or
High yielding spring bread wheat germplasm for global irrigated and rainfed reproduction in other forums is permitted, provided the original author(s) and the
production systems. Euphytica 157, 351–363. doi: 10.1007/s10681-006-9346-6 copyright owner(s) are credited and that the original publication in this journal
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