Physiologia Plantarum 171: 66–76.

2021 © 2020 Scandinavian Plant Physiology Society, ISSN 0031-9317

Meta-analysis of drought and heat stress combination impact

on crop yield and yield components
Itay Cohen, Sara I. Zandalinas, Clayton Huck, Felix B. Fritschi and Ron Mittler*
Division of Plant Sciences and Interdisciplinary Plant Group, College of Agriculture Food and Natural Resources, Christopher S. Bond Life Sciences Center,
University of Missouri, 1201 Rollins Street, Columbia, Missouri, 65201, USA

Correspondence Episodes of prolonged drought coupled with heat waves (i.e. drought and
*Corresponding author,
heat combination) can have a devastating impact on agricultural produc-
e-mail: mittlerr@missouri.edu
tion and crop yield. It is therefore not surprising that improving tolerance
Received 15 June 2020; to drought and heat combination has been a major goal for breeders and
revised 26 August 2020 biotech companies. Although much is known about the physiological
and molecular responses of vegetative tissues to a combination of drought
doi:10.1111/ppl.13203
and heat stress, less is known about the impact of this stress combination
on yield and different yield components. Here, we used a meta-analysis
approach to synthesize results from over 120 published case studies of
crop responses to combined drought and heat stress. Our findings reveal
that drought and heat stress combination significantly impacts yield by
decreasing harvest index, shortening the life cycle of crops, and altering
seed number, size and composition. Furthermore, these impacts are more
severe when the stress combination is applied during the reproductive
stage of plants. We further identify differences in how legumes and cereals
respond to the stress combination and reveal that utilizing C3 or C4 metab-
olism may not provide an advantage to plants during stress combinations.
Taken together our study highlights a need to focus future studies, as well
as breeding efforts, on crop responses to drought and heat combination
at the reproductive stage of different crop species.

Introduction grain production worldwide (Ciais et al. 2005, Mit-

Cereals and legumes are grown on more than 160 million
hectares of non-irrigated (rain-fed) land worldwide, sup-
porting millions of lives in many different countries
(Dwivedi et al. 2018). While growing on non-irrigated
lands, these crops are potentially subjected to different
environmental stress conditions such as drought, heat
stress and their combination. Heat waves combined with
acute and prolonged drought stress can have a devastat-
ing outcome for agriculture, as well as economic and
social stability, primarily impacting drylands used for
tler 2006, Chen et al. 2019, Zandalinas et al. 2020). The
2003 drought and heat episode across Europe, for exam-
ple, caused a 30% reduction in agricultural production
(Ciais et al. 2005). Combined instances of drought and
heat wave have considerably increased in the United
States during the period of 1990–2010 compared to
1960–1980 (Mazdiyasni and AghaKouchak 2015), with
climate models predicting that these episodes will further
intensify (Lobell and Gourdji 2012, Lawas et al. 2018b);
with an average increase of 2 C already recorded for pro-
duction regions of major crops such as wheat (Triticum

Abbreviations – DS, drought stress; HI, harvest index; HS + DS, combination of heat and drought stresses; HS, heat stress; SNPs,
single nucleotide polymorphisms.

66 Physiol. Plant. 171, 2021


aestivum), rice (Oryza sativa) and maize (Zea mays).
Models further predict that more significant yield
decreases in the second half of this century will take
place in tropical areas compared to temperate regions
(Challinor et al. 2014). Field studies with soybean
(Glycine max) demonstrated that episodes of drought
and heat negate the boost C3 plants receive from growing
in a CO2 enriched environment (Gray et al. 2016). This
recent insight from field experimentation imposing com-
bined heat and drought demonstrates the likelihood of
negative impacts from interacting global change factors
on other key global commodity crops such as wheat
and maize in their primary production regions.
Combined heat and drought stresses were found to
negatively impact the yield of major crop plants includ-
ing legumes such as soybean, chickpea (Cicer arietinum),
and lentil (Lens culinaris) (Dornbos Jr and Mullen 1991,
Awasthi et al. 2014, Sehgal et al. 2017), as well as cereals
such as wheat, maize and rice (Prasad et al. 2011, Cairns
et al. 2013, Obata et al. 2015, Lawas et al. 2018a), which
are the mainstay of global food and feed supply in terms
of both calorie and protein intake. A recent study in
India showed that supplying field crops such as wheat
with irrigation can offset some of the yield reductions
associated with water-limited, heat-stressed plants
(Zaveri and Lobell 2019). Nonetheless, the use of fresh
water to irrigate wheat is unsustainable and aggravates
conditions of water scarcity similar to the ones faced by
India during the summer of 2019 (Shah and
Narain 2019).
Most studies in both model and crop plants have
focused on the effects of drought or heat on yield as
single-stress factors, or focused on the effects of com-
bined stresses during the vegetative stages without
emphasizing how grain yields are impacted (Prasad
et al. 2011, Obata et al. 2015, Lawas et al. 2018b). This
is despite the prevalence of combined heat and drought
periods in field-grown plants during reproductive growth,
and the fact that we cannot extrapolate plant responses to
stress combinations simply by the addition of responses
to the two single stresses that comprise the stress combi-
nation (Rizhsky et al. 2004, Mittler 2006, Suzuki
et al. 2014). In vegetative tissues, combined heat and
drought negatively impact vital physiological plant pro-
cesses such as stomatal conductance, photosynthesis
and respiration (Rizhsky et al. 2002, 2004, Zandalinas
et al. 2020). Furthermore, carbon balance is disturbed
under drought and heat combination due to increased
carbohydrate demand for cellular respiration taking
place simultaneously with the decrease in photosynthesis
(Foyer et al. 2009, Yu et al. 2012). Indeed, heat stress can
cause a negative whole plant carbon balance even under
relatively mild water deficit conditions (Zhao et al. 2013).
Physiol. Plant. 171, 2021
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Drought and heat combination during the reproduc-
tive stages are more detrimental by far to crop yields
because flower, ovary or seed abortion are irreversible
processes, while the photosynthesis machinery can
recover once the stress is removed (Balfagón et al. 2019,
Mahalingam and Bregitzer 2019). Drought and heat
combination can also shorten the life cycle, overall car-
bon assimilation and grain filling period in crops
(Awasthi et al. 2014). Additionally, this stress combina-
tion negatively impacts a variety of yield components
such as harvest index (HI), seed number and single seed
size (Rollins et al. 2013, Sehgal et al. 2017).
Due to the complexities of properly controlling four
different environments (control, heat, drought, and
drought and heat), large scale phenotyping of crop plants
subjected to drought and heat combination are rare, and
until now reported only for maize (Cairns et al. 2013;
stress was applied during anthesis), groundnut (Arachis
hypogea; Hamidou et al. 2013; Stress was applied at
the onset of flowering) and wheat (Li et al. 2019; stress
was applied 1 week after anthesis). Drought and heat
combination studies performed on large populations of
crop plants (maize and wheat) suggest that genotypes
with tolerance to heat or drought as a single stress do
not necessarily exhibit tolerance to the combination of
these stresses (Cairns et al. 2013, Qaseem et al. 2019).
These findings are consistent with previous evidence that
transcripts upregulated in response to stress combination
do not necessarily increase in response to the two single-
stress conditions that comprise the stress combination
(Mittler 2006). Furthermore, single nucleotide polymor-
phisms (SNPs) found to be significantly associated with
grain yield during a single stress do not overlap with the
ones observed under combined stress conditions (Yuan
et al. 2019). These results further emphasize the original
findings of Rizhsky et al. (2002, 2004), that we cannot
extrapolate the plants’ responses to stress combination
from its responses to each of the two different stresses that
comprise the stress combination. Though previous stud-
ies suggested that a transgenic approach can mitigate
the effects of drought or heat stress applied individually
(e.g. Ambavaram et al. 2014), published work that dem-
onstrates mitigation of the impact of combined heat and
drought stress, to the best of our knowledge, is limited
to a single study in cotton (Gossypuim hirsutum) by
Mishra et al. (2017).
Although previous reviews summarized the effects of
drought and heat combination on different model and
crop plants (Mittler 2006, Barnabás et al. 2008, Prasad
et al. 2008, Suzuki et al. 2014, Sehgal et al. 2018, Lawas
et al. 2018b), a comprehensive meta-analysis of crop
responses to combined drought and heat stresses has
not been conducted. Here we synthesized results from
67
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126 different case studies (Table S1) obtained from 49 dif- and water potential; however, we primarily focused on
ferent publications (Table S2) reporting the impacts of studies that presented data on yield and yield compo-
drought, heat and their combination on yield, yield com- nents. To be included in the analyses, studies had to
ponents and seed composition. report on all four conditions: control, heat stress, drought
and drought and heat stress combination. Short term or
small-scale experiments were excluded. Moreover,
Materials and methods results from the model plant Arabidopsis were also
excluded. When data was presented in a bar graph, the
In the winter of 2019, a variety of key word searches were
image was digitized and WebPlotDigitizer 4.2 software
performed using different scientific bibliographic tools
(http://arohatgi.info/WebPlotDigitizer/) was used to
such as Google Scholar, Web of Science, Pubmed and
extract values. In some cases, the HI parameter was not
AGRICOLA, focused on the effects of drought and heat
explicitly reported, therefore we calculated it from the
combination on plants. In addition, lists of cited refer-
data on yield and overall biomass (Erice et al. 2014).
ences in relevant reviews were surveyed (Mittler 2006,
Parameters subjected to the meta-analysis included:
Barnabás et al. 2008, Prasad et al. 2008, Suzuki
yield, HI, single seed size, seed protein content, seed
et al. 2014, Sehgal et al. 2018, Lawas et al. 2018b). Over-
starch content, and time needed to complete life cycle.
all, we extracted and analyzed 126 different case studies
Data is presented as the mean of all relevant cases. Since
taken from 49 different peer-reviewed publications
comparing yield and yield parameters from field and
(Tables S1 and S2).
greenhouse experiments is not entirely valid, and as crop
Several factors were taken into consideration when
species varied greatly in their yield, we normalized
analyzing the published data. These included: Plant spe-
results from all studies to percentage (%) of the results of
cies, type of photosynthetic pathway used (C3 or C4; no
the control group for all parameters. Since some publica-
reports on CAM or C3-C4 or C3-CAM intermediates were
tions reported on more than one genotype, we included
found), rooting environment (pots or field environment),
these genotypes as separate case studies. To determine
plant family (most plants were either in the cereals or
statistical significance, combined case studies were sub-
legumes families; however, few studies included crops
jected to a one- or two-way ANOVA followed by
in the Brassicaceae or Solanum families), and the devel-
Tukey’s test.
opmental stage of studied plants at the time stress was
applied (vegetative or reproductive). In addition, experi-
ments that used a short (less than 12 h) heat treatment Results
or used fewer than four replications per treatment were
Impact of drought and heat stress combination on
omitted.
yield and yield components
Meta-analysis was only performed on data acquired
from published, peer-reviewed studies that met several Comparing the impact of drought and heat stress combi-
specific criteria. Many publications displayed results nation to that of drought or heat stresses applied individ-
from physiological measurements such as gas exchange ually for all cases studied, revealed that the combination

A B C
140 140 100
b
Relative days to maturity (% of control)

a n = 126 a n = 36 a n = 20
120 c
120
a b 90
Relative yield (% of control)

100 a
b 100
80
HI (% of control)

80
80
60 70
60
40
60
40
20
50
0 20

-20 0 40
HS DS HS + DS HS DS HS + DS HS DS HS + DS

Fig 1. The impact of drought and heat stress combination on relative yield, harvest index, and days to maturity. (A) Relative yield of all crops surveyed
under heat stress (HS) drought stress (DS) and their combination (HS + DS). (B) Relative harvest index (HI) of all crops under HS, DS and HS + DS. (C)
Relative days needed to reach maturity under HS, DS and HS + DS. Results are expressed as percentage of control conditions. Boxplots with different
letters within each panel are significantly different at P > 0.05 according to one way ANOVA followed by Tukey’s test (n = 126 cases in A, n = 36 cases
in B, and n = 20 cases in C).

68 Physiol. Plant. 171, 2021


of drought and heat stress had a more severe impact on
yield compared to drought or heat alone (Figs 1 and
S1). Compared to controls, crops subjected to heat or
drought stresses applied as single-stress factor displayed
a 33 and 48% yield reduction, respectively, whereas
the average yield reduction in response to a combination
of drought and heat stress was 65% (Fig. 1A). This impact
of stress combination on yield could manifest itself in a
number of different ways. We therefore compared the
impact of stress combination on different yield compo-
nents to that of each of the stresses applied individually.
HI is a key indicator of biomass partitioning between
vegetative and reproductive organs in crop plants. It is
defined as the total weight of grain divided by the total
weight of above ground biomass. As highlighted in
Figs. 1B and S2, when different crops were exposed to
heat or drought, their HI decreased by 28 and 27%,
respectively. Interestingly, the combination of drought
and heat further impacted HI and reduced it by 53%. This
result suggests that the drought and heat stress combina-
tion may shorten the life cycle of annual crops and drive
them to produce seeds earlier, and most likely in reduced
numbers and/or size, with less vegetative tissues pro-
duced in the process. Indeed, as shown in Fig. 1C (calcu-
lated for all studies that measured the length of life cycle
of crops), the combination of drought and heat stress
shortened the life cycle of most crops by an average of
more than 40%. Interestingly, the impact of drought on
life cycle (a decrease of about 20%) was significantly dif-
ferent than that of heat (a decrease of about 30%) reveal-
ing that drought had the least impact on shortening the
life cycle of crops compared to heat or drought and heat
combination (with drought and heat combination having
the maximal effect).
The impact of drought and heat stress combination
on seed number, as well as seed starch and protein
content
Plants that display a shortened life cycle often also exhibit
a reduced number of seeds per reproductive unit
(e.g. pod, spike, panicle, ear). Heat and drought as single
stresses reduced seed numbers in each reproductive unit,
and their combination further magnified the impact,
resulting in a 32% decrease in seed number per repro-
ductive unit (Fig. 2A).
Seed composition is determined by many factors,
including the environmental conditions during the seed
filling processes, as well as the overall biomass of the
plant, accumulated during the vegetative stage. Thus,
we reviewed the impacts of drought, heat and drought
and heat combinations on seed starch and protein con-
tents. As shown in Fig. 2B, the reduction in starch content
Physiol. Plant. 171, 2021
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by the stress combination (60%) was about double that
observed in response to heat or drought individually
(30%). In contrast, seed protein content was elevated
compared to control in all three stress treatments
(Fig. 2C). However, while drought or heat caused a mod-
erate increase in protein content of about 10–15%, the
combination of drought and heat increased seed protein
content by more than 30%. Although the reason for the
increase in seed protein content during stress combina-
tion is unknown at present, it is possible that this increase
reflects a decrease in overall seed water content and/or a
compensatory mechanism to the decrease in starch con-
tent. Overall, the findings presented in Fig. 2B,C demon-
strate that, in addition to the more pronounced decrease
in yield and number of seeds per reproductive unit
(Figs 1A and 2A), the drought and heat stress combination
also amplified the impact on seed composition compared
to the effect of heat or drought individually (Fig. 2B,C).
The negative impact of stress combination is greater
during the reproductive stage
The impact of stress combination on yield, HI, life cycle
and seed composition (Figs 1 and 2) could result from
the stress combination impact on overall biomass
through suppression of photosynthesis, from its effects
on plant reproductive processes such as fertilization
and/or abortion, and/or from its effects on seed filling.
To explore the effects of stress combination relative to
developmental stage, we divided the data set into exper-
iments that subjected crops to stress during the vegetative
or the reproductive stages. Not surprisingly, the highest
yield penalty resulted when the stress combination was
applied during the reproductive stage (Fig. 3).
Legumes and cereals display differential sensitivity
to drought and heat stress combination
To develop crops with enhanced tolerance to drought
and heat stress combination, a better understanding of
various strategies displayed by different crops subjected
to stress combination is needed. We therefore divided
the data set into experiments that subjected cereals or
legumes to a combination of drought and heat stress
(Fig. 4). Compared to drought or heat stress applied indi-
vidually, both cereals and legumes were more sensitive
to the combination of drought and heat (Fig. 4A); with
legumes showing a higher sensitivity (in yield) to drought
than heat, whereas the impact of the individual stresses
was not different in cereals. To further dissect the
responses of these different crop types to the stress combi-
nation, we compared relative HI (Fig. 4B) and individual
seed weight (Fig. 4C) between them. Compared to
legumes, cereals had a higher HI penalty in response to
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A B C
110 160
a a a n= 16
Relative seed number in reproductive

Relative seed protein (% of control)

a n= 19 a n= 20

Relative seed starch (% of control)

100 100
b 150
90
140
unit (% of control)

80
80
b b
b
70 130
60
60
120
50
40 110
40
100
20 30

20 90
HS DS HS + DS HS DS HS + DS HS DS HS + DS

Fig 2. The impact of drought and heat stress combination on relative seed number and composition. (A) Relative seed number in a reproductive unit (pot,
spike, and ear) under heat stress (HS) drought stress (DS) and their combination (HS + DS). (B) Relative seed starch, under HS, DS and HS + DS. (C) Relative
seed protein, under HS, DS and HS + DS. Results are expressed as percentage of control conditions, boxplots with different letters within each panel are
significantly different at P > 0.05 according to one-way ANOVA followed by Tukey’s test (n = 19 cases in A, n = 20 cases in B, and n = 16 cases in C).

the drought and heat combination (Fig. 4B). In addition,
as shown in Figs 4C and S3, individual seed mass of
cereals was further reduced compared to legumes by
the stress combination.
Impact of heat and drought stress combination on
C3 and C4 crops
To investigate whether the magnified yield penalty asso-
ciated with exposure to combined, as opposed to individ-
ual, heat and drought stress is associated with C3 or C4
metabolism, we also divided the data set based on C3
Reproductive
n= 119
Relative yield (% of control)
or C4 plants (Fig. 5). The vegetative tissues of C3 and
C4 plants differ in responses to heat or drought stresses,
mostly due to the near abolishment of photorespiration
in plants utilizing the C4 photosynthetic pathway
(Crafts-Brandner and Salvucci 2002, Ripley et al. 2010,
Killi et al. 2017). Although compared to C4 plants the
yield of C3 plants displayed higher sensitivity to heat,
the yield of both C3 and C4 plants was similarly impacted
by the stress combination (Fig. 5).
Discussion
Global food security is influenced by many local and
global factors, such as demand for food and feed,
Vegetative changes in input prices (especially that of fertilizers in
a developing countries), soil losses due to erosion, and
n= 11
water availability. Furthermore, managing the balance

150
between conservation of farmland and natural habitats,
as urbanization increases, puts more pressure on land
a a
b
resources (St Clair and Lynch 2010, Seck et al. 2012,
b Challinor et al. 2014). The overall economic losses and
100 c
hardships resulting from episodes of combined drought
and heat wave highlight the need to study how crops
respond to these events (Fischer et al. 2005, Mittler 2006,
50 Lobell and Gourdji 2012, Xie et al. 2018). Because the
vast majority of our food and feed are generated from
field-grown crops, drought and heat stress combination
poses a major risk to local and even global food security.
0 In crops, drought and heat combinations have a syner-
HS DS HS + DS HS DS HS + DS gistic impact on life cycle, such as shortening the number
of days to anthesis and overall period required to reach
Fig 3. Comparison of the effects of heat stress (HS) drought stress maturity (Fig. 1C; Awasthi et al. 2014, Qaseem
(DS) and their combination (HS + DS) on relative yield when the stress
et al. 2019). From an evolutionary stand-point, shorten-
was imposed during the reproductive (n = 119) or vegetative (n = 11)
growth stages. Boxplots with different letters within each panel are
ing the life cycle of a plant enables it to escape drought
significantly different at P > 0.05 according to two-way ANOVA followed by reaching maturity before its occurrence becomes
by Tukey’s test. lethal (Prasad et al. 2008). Nevertheless, reduced life

70 Physiol. Plant. 171, 2021

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A Cereal Legume
Legume
B Legume
C Legume
Cereal Cereal
Cereal Legume Cereal
120 140
a n= 92 n= 33 n= 26 n= 20 n= 27 a n= 20
a a
a A 100

Individual seed weight (% of control)

120
100 a a a a E bC c a
Relative yield (% of control)

Relative HI (% of control)
c 80 b
c b 100
80 a
c 80
60
60
60
40
40
40

20 20
20

0 0 0
HS DS HS + DS HS DS HS + DS HS DS HS + DS HS DS HS + DS HS DS HS + DS HS DS HS + DS

Fig 4. Comparison of the effects of heat stress (HS) drought stress (DS) and their combination (HS + DS) on relative yield (A), harvest index (HI) (B) and
relative seed weight (C) in crop plants that belong to the cereal (n = 92 in A, n = 26 in B and n = 27 in C) and legume (n = 33 in A, n = 20 in B and
n = 20 in C) families. Boxplots with different letters within each panel are significantly different at P > 0.05 according to two-way ANOVA followed by
Tukey’s test.

cycle length has a profound impact on overall assimilate of seeds in each reproductive unit (Fig. 2A), the overall
accumulation, overall biomass and the length of the number of reproductive units per plant (Barnabás
effective grain filling period resulting in an overall loss et al. 2008, Lawas et al. 2018a, Li et al. 2019, Qaseem
in seed mass in many crop species (Fig. 4C). Because bio- et al. 2019), and when expressed on an area basis, the
mass accumulation is an integrator of photosynthesis rate number of plants per unit area. While both heat and
over the growth period, and because drought and heat drought as single stresses can negatively impact each
combination negatively impacts both, the overall bio- yield component, the examined literature indicates a
mass of plants and the amount of assimilates available shared trend among crop plants which display a synergis-
to allocate into the grains decreases accordingly. tic negative response to drought and heat combination
Yield (Figs 1A, 3, 4A and 5) can be quantified by the (Figs 1–5). When comparing the effects of heat, drought
integration of individual seed weight (Fig. 4C), number and their combination between C3 and C4 crop plants
for example, heat stress alone decreased yields of C3
crops more than of C4 crops. However, when exposed
C3 C4 to a combination of drought and heat, both C3 and C4
140 crops displayed similar decreases in yield (Fig. 5). This
b n= 99 n= 21 result is somewhat surprising given that C4 plants are
a
120 considered, at least in their vegetative stages, as more
Relative yield (% of control)

b
drought tolerant (Lopes et al. 2011).
100 While vegetative tissues are sensitive to drought and
b heat, especially under high light conditions, they may
c c
80 recover from the impacts of stress (Balfagón et al. 2019,
Ruehr et al. 2019). In contrast, seed abortion is irrevers-
60 ible. Although, plants can display a considerable com-
pensation potential and may produce fewer but larger
40 seeds under different stress conditions (Vonhof and
Harder 1995, Griffiths et al. 2015), examples of drought
20 and heat stress combination resulting in partial or com-
plete yield loss due to male sterility have been recorded.
HS DS HS + DS HS DS HS + DS In wheat, a crop with very short growth period, combined
heat and drought during the early reproductive stage
Fig 5. Comparison of the effects of heat stress (HS) drought stress (anthesis) can lead to male sterility (Nicolas et al. 1984).
(DS) and their combination (HS + DS) on relative yield of crops
Unfortunately, only a few studies attempted to compare
belonging to the C3 (n = 93) or C4 (n = 21) photosynthetic pathway
families. Boxplots with different letters within each panel are
the effects of similar drought and heat intensities between
significantly different at P > 0.05 according to two-way ANOVA followed the reproductive and vegetative stages (Fig. 3). An excel-
by Tukey’s test. lent example in barley (Hordeum vulgare) demonstrated

Physiol. Plant. 171, 2021 71


that under 1 week of combined stress conditions in either
the vegetative or heading stages, photosynthesis rates
were similarly affected whereas a dramatic difference in
the effect on yield was observed. While yield decrease
was limited when the stress was applied during vegeta-
tive stages, yield loss of plants exposed to combined
stress during the heading stage was almost complete
(Mahalingam and Bregitzer 2019).
Seed yields of all crops in this study displayed synergis-
tic negative responses to combined drought and heat
(Figs 1A, 3, 4A and 5). Across the many studies examined
here, both individual drought and heat stress generally
caused a decrease in seed numbers and seed weight,
and the impact on these traits was magnified by the com-
bination of heat and drought stress (Figs 2A and 4C). Sep-
arating the overall results into cereals and legumes,
revealed a more dramatic reduction in seed weight in
cereals (70%) than in legumes (50%) in response to the
stress combination (Fig. 4C). In contrast, the effect of
the stress combination on HI and individual seed weight
of legumes was lower. The results presented in Fig. 4,
suggest that, compared to legumes, cereals attempt to
compensate for their yield loss during drought and heat
stress combination by reducing vegetative growth and
seed size.
Compare to legumes, cereals have a high starch and
low protein content. Our results suggest that at least in
part, cereals display a greater decrease in HI in response
to combined drought and heat then legumes (Fig. 4B).
Because drought and heat combination results in low
starch coupled with high protein seed content (Fig. 2C),
it is possible that seed carbohydrates to protein ratio plays
a role in the response to heat and drought combination,
giving an advantage to legumes over cereals, at least
when it comes to HI (Fig. 4B).
General tradeoffs between seed number and weight of
individual seeds have been well documented for a num-
ber of crop species (Vonhof and Harder 1995, Griffiths
et al. 2015). In addition, the impact of stress on seed num-
ber and seed weight is strongly influenced by the timing
of the stress relative to reproductive stages that are associ-
ated with the primary processes influencing these two
parameters (Stone and Nicolas 1995). For example, seed
size in wheat is most sensitive to heat during the early
grain filling period and becomes progressively more resil-
ient throughout grain filling (Nicolas et al. 1984). More-
over, lower seed set under combined drought and heat
makes sense from a sink-source standpoint, as fewer
seeds means less sink competition during the grain filling
stages. Likewise, seeds cannot just shrink indefinitely in
size and stay viable, and therefore, as resources (assimi-
lates) are limited under combined stress, the decreasing
seed-set is a trade-off and an adjustment mechanism to
72
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ensure the survival of few, but viable seeds (Figs 2
and 4C).
Clearly, the timing of the stress during different devel-
opmental stages is critical (Fig. 3). For example, during
flowering, pollen is particularly sensitive to high temper-
atures, especially when combined with drought (Ruan
et al. 2010, Jiang et al. 2019). A recent study also sug-
gested that stigma functionality and fertility are also sen-
sitive under combined drought and heat in wheat
plants, leading to flower abortion (Fábián et al. 2019).
Earlier work proposed that heat stress during anthesis
can cause smaller or complete absence of the embryo-
sac (Sainiab et al. 1983), which can later result in a
decrease in pod set and seed size (Sainiab et al. 1983,
Gross and Kigel 1994). The number of seeds per plant is
a function of availability of viable pollen that germinates,
grows and leads to successful fertilization (Ruan
et al. 2010). Thus, stress during flowering can have a
dominant effect on seed numbers. For example, Ji
et al. (2010) as well as others (Vonhof and Harder 1995,
Yu et al. 2019) found that drought episodes early during
the reproductive stage cause pollen sterility. Addition-
ally, heat stress is well-known to negatively impact pollen
viability and germination of pollen in different crops such
as wheat, pea (Pisum sativum) and soybean (Sainiab
et al. 1983, Salem et al. 2007, Jiang et al. 2019). Besides
resource (carbohydrates) availability during the grain fill-
ing stage, the final size of an individual seed is governed
by the number of cell divisions and cell expansion.
Drought is known to negatively impact mitotic activity
(Schuppler et al. 1998), and heat stress was found to
decrease the number of cells in soybean seeds
(Tacarindua et al. 2012), suggesting that stress-induced
decrease in cell division can negatively impact overall
seed size (Fig. 4C).
A number of mechanisms including carbohydrate
availability and metabolism have been explored and
documented to be associated with impaired reproductive
success in response to heat or drought stress. For
instance, impaired sucrose metabolism has been sug-
gested to underpin reduced pollen function and fertiliza-
tion under heat stress in chickpea (Kaushal et al. 2013).
Consistent with the importance of sucrose availability
during flowering, sucrose infusion into stems of water-
limited maize can mitigate the effects of stress on seed
set (Boyer and Westgate 2004). The combination of
drought and heat stress may magnify the impact of each
individual stress on the plant carbohydrate balance
(Zhao et al. 2013). Indeed, recent studies in rice suggest
that sugar starvation in the floral organs is the underlying
factor in reproductive failure of a rice cultivar sensitive to
the combination of drought and heat (Li et al. 2015,
Lawas et al. 2018a, 2019). Additionally, other
Physiol. Plant. 171, 2021

researchers have shown an interactive negative effect of
these stresses on the activity of key sucrose metabolism
enzymes such as sucrose synthase and invertase
(Awasthi et al. 2014, Sehgal et al. 2017). Together with
the decline in photosynthesis, the decrease in sucrose
metabolism under combined stress conditions may limit
sucrose availability for pollen, resulting in lower pollen
viability and germination, and ultimately seed set
(Figs 2 and 4C). During the seed-filling stage, the above-
mentioned reduction in photosynthesis and leaf sucrose
metabolism in response to the stress combination results
in lower carbohydrate availability for import into devel-
oping seeds (Fig. 2B). As starch is the key component
(by weight) in seeds of the major global staple crops
(maize, rice and wheat; Sehgal et al. 2018), reduction in
source strength and carbon availability for starch biosyn-
thesis during the grain filling stage will inevitably lead to
decrease in seed size and weight (Thitisaksakul
et al. 2012). Recent findings suggest that in the endo-
sperm of developing wheat grains, drought or heat, and
especially their combination decrease the activity of
key enzymes in the starch biosynthesis pathway such as
starch synthase and starch branching enzyme
(Tetlow 2011, Thitisaksakul et al. 2012).
HI describes the ratio between grain yield and the
aboveground biomass (Erice et al. 2014). It is a key trait
tightly associated with significant yield increases of rice
and wheat during the second half of the 20th century.
Both drought and heat stress are well known to negatively
impact HI (e.g. Edmeades et al. 1999, Prasad et al. 2006),
and were documented in the majority of studies exam-
ined here (Figs 1B and 4B). As expected, based on the
impact of stress combination on seed yield and yield
components (Figs 1–5), combined heat and drought stress
caused a further decline in HI (Figs 1B and 4B), empha-
sizing that combined stress conditions impact the repro-
ductive outcome of crops more severely than their
vegetative growth. Interestingly, a striking contrast in HI
under combined drought and heat conditions was found
between different crops (Figs 1B and 4B) and the model
plant Arabidopsis (Vile et al. 2012). A careful study of
biomass allocation in 10 Arabidopsis genotypes sug-
gested that HI increases under combined drought and
heat (Vile et al. 2012). These results, which are in contrast
to our findings, could suggest that Arabidopsis may not
be a suitable model plant for studies of biomass alloca-
tion during drought and heat combination. In contrast,
the model plant of C3 cereals, Brachypodium dysta-
chion, demonstrated a similar alteration in HI to what
we observed among a diverse group of crop plants
(Shaar-Moshe et al. 2017). Ruan et al. (2010) suggested
a very straightforward explanation as to why, under
severe stress, the vegetative organs stay alive while HI is
Physiol. Plant. 171, 2021
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altered. If the parent plant dies, no seeds will be pro-
duced, therefore, even slight seed reproduction is better
for ensuring the next generation. This is potentially why
HI suffers a significant reduction when plants are
exposed to combined drought and heat (Figs 1B and 4B).
Heat, drought, and their combination influence many
developmental and physiological processes in crop
plants. Whether occurring individually or in combina-
tion, the impact of these different stresses depends on
many factors, including the crop type and its growth
habits (Figs 4 and 5), as well as the stress intensity, dura-
tion, and timing with respect to crop developmental stage
(Fig. 3). Thus, it is not surprising that the examination of
studies that include control, heat, drought, and combined
heat and drought stress treatments revealed a wide range
in relative impacts of all stress treatments and for all
parameters explored in this study. Nonetheless, the rela-
tive effect of the combined heat and drought stress treat-
ment was consistently more dramatic than the impact of
drought or heat applied individually. This finding high-
lights the importance of studies that specifically address
heat and drought stress combination (Mittler 2006, Chen
et al. 2019, Zandalinas et al. 2017, 2020, Mazdiyasni
and AghaKouchak 2015, Lobell and Gourdji 2012,
Lawas et al. 2018b). Importantly, the results presented
here underscore the need to focus on stress combinations
occurring during the reproductive growth stages, as the
impact on yield is more severe than when stress combi-
nation occurs during vegetative development (Fig. 3).
This is especially important as to date most studies exam-
ining molecular level mechanisms focused on vegetative
tissues (e.g. Rizhsky et al. 2002, 2004, Zandalinas
et al. 2017, 2020, Balfagón et al. 2019), while only lim-
ited knowledge is available on the molecular events
occurring in reproductive tissues in response to drought
and heat stress (Li et al. 2015, Lawas et al. 2018b). A par-
ticular focus on the molecular responses of reproductive
tissues to the combination of drought and heat stress is
warranted to identify mechanisms and avenues that can
be targeted to improve tolerance and thus alleviate the
impact of stress combination on overall yield and grain
quality.
Author contributions
I.C. and C.H. collected, analyzed the data, and generated
the figures. I.C., S.I.Z., F.B.F. and R.M. wrote the manu-
script. S.I.Z., F.B.F. and R.M. supervised the project.
Acknowledgements – This work was supported
by funding from the National Science Foundation
(IOS-1353886, MCB-1936590, IOS-1932639) and the
University of Missouri.
73

Data availability statement
All data is available online through public websites.
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Supporting information
Additional supporting information may be found online
in the Supporting Information section at the end of the
article.
Fig. S1. Relative yield of different crops under heat stress
(HS) drought stress (DS) and their combination
(HS + DS).
Fig. S2. Relative harvest index (HI) of different crops
under heat stress (HS) drought stress (DS) and their com-
bination (HS + DS).
Fig. S3. Relative individual seed weight of different crops
under heat stress (HS) drought stress (DS) and their com-
bination (HS + DS).
Table S1. List of case studies and their corresponding ref-
erences used in the meta-analysis.
Table S2. List of publications used for meta-analysis.
Physiol. Plant. 171, 2021