Journal of Plant Growth Regulation (2020) 39:456–480

https://doi.org/10.1007/s00344-019-09994-x

Approaches in Enhancing Thermotolerance in Plants: An Updated

Review
Shafaqat Ali1   · Muhammad Rizwan1 · Muhammad Saleem Arif1 · Rehan Ahmad1 · Mirza Hasanuzzaman2 ·
Basharat Ali3 · Afzal Hussain1

Received: 16 November 2018 / Accepted: 6 June 2019 / Published online: 18 June 2019
© Springer Science+Business Media, LLC, part of Springer Nature 2019

Abstract
Global warming has been increasing manifold in recent times, and this may cause tremendous economic losses in the near
future. Recently, heat stress is considered one of the major constraints affecting crop growth and yield at world level. Heat
stress reduced the plant growth, photosynthesis, mineral nutrients, and yield attributes. Heat stress caused both ultrastructural
alterations and oxidative stress in different parts of plants. Plants can tolerate certain levels of heat stress by maintaining
membrane stability, adjusting antioxidants and compatible solutes, and scavenging reactive oxygen species. Heat tolerance
in plants can be improved by selecting heat-tolerant cultivars, genetic engineering, and exogenous application of osmolytes,
microbes, mineral nutrients, soil amendments, and proper agricultural practices. This review is devoted to discuss the plants’
physiological and biochemical responses to heat stress and various integrated approaches to improve heat stress tolerance
in plants.

Keywords  Heat stress · Plants · Thermotolerance

Introduction The increase in the mean temperature coupled with climatic

Heat stress is a major ecological constraint that threatens
world food security as global warming progressed manifold
in recent times (Abbas et al. 2018). Global climatic variabil-
ity is further expected to intensify as global climatic projec-
tions suggest an increase in mean temperature by 2–4 °C
over the next half of this century (IPCC 2007). Globally,
agriculture is widely considered as one of the sectors likely
to be imperiled by changing climate (Abbas 2013). Tem-
perature is a primary factor affecting the rate of plant growth
and development. Each plant species represents a certain
temperature regime of growth and productivity which is
characterized by minimum, maximum, and optimal range.
* Shafaqat Ali
shafaqataligill@yahoo.com; shafaqataligill@gcuf.edu.pk
1
Department of Environmental Sciences and Engineering,
Government College University, Allama Iqbal Road,
Faisalabad 38000, Pakistan
2
Department of Agronomy, Sher-e-Bangla Agricultural
University, Dhaka, Bangladesh
3
Department of Agronomy, University of Agriculture
Faisalabad, Faisalabad 38040, Pakistan
variability often exacerbates heat stress in crop plants. Heat
stress adversely affects plant growth and productivity, and
leads to a wide range of morphological, physiological, bio-
chemical, and molecular responses (Zandalinas et al. 2018).
In recent times, frequent extreme heat events have caused
phenological disruptions among various plant species across
the world (Ibáñez et al. 2010; Li et al. 2014a, b, c, d). In
2003, severe heat events inflicted a loss of approximately 5
million tons of rice grain in China (Tian et al. 2009). In addi-
tion, the European heat wave of 2003 also reduced the crop
yields (Ciais et al. 2005). Based on projected climatic mod-
els, heat stress-associated yield loss in crop plants is likely
to increase up to 40% in coming decades (Lobell and Tebaldi
2014). The extent of plant damages caused by heat stress is
not restricted to plant growth stage. Heat stress-triggered
plant vulnerabilities are based on plant sensitivity, dura-
tion, and intensity of prevalent extreme heat events (Prasad
et al. 2017). Heat stress at an early growth stage of crop
plants arrests seed germination and delays seedling emer-
gence (Deng et al. 2015). Heat stress at vegetative growth
can impair photosynthetic pigments, light perception, carbon
metabolism, and translocation of organic solutes (Asseng
et al. 2015; Sgobba et al. 2015; Balal et al. 2016). Impact of

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Journal of Plant Growth Regulation (2020) 39:456–480 457
heat stress on reproductive stages of crop plants often results
in imbalance in mineral nutrition, inactivation of defense
system (antioxidant enzymes), and subsequent production
of reactive oxygen species (ROS) damaging membranes
(Huang et al. 2015; Zhang et al. 2016a, b). Therefore, this
focused review highlighted the impacts of heat events on
plant growth and productivity at morphological, physiologi-
cal, and biochemical scales. In addition, various adaptive
interventions to improve heat stress tolerance in crop plants
have been highlighted and discussed.
Effect of Heat Stress on Plants
Effects on Growth and Yield
Heat stress can have devastating impacts on plant growth
and yield (Fig. 1, Table 1). Recent studies indicate signifi-
cant negative impacts of extreme heat event on plant height,
root length, biomass production, and grain quality among
field crops (Nayyar et al. 2014; Cao et al. 2015; Waqas et al.
2015; Bahuguna et al. 2017). Temperature variation during
different growth stages affects the crop yield and quality
(Deng et al. 2015). Plant growth is significantly reduced
by heat stress at initial stages of plant growth in most field
crops. Seedling mortality due to heat is one of the most
common stress responses and is related to meristem injury
and subsequent stem collapse in crop plants. Recently, El-
Daim et al. (2014) found that extreme heat events of 45 °C
caused 80%–95% seedling mortality in two cultivars of
wheat. Heat stress decreased the growth and grain yield of
wheat depending upon genotypes (Ihsan et al. 2016). Fahad
Fig. 1  Possible effects of heat
stress on different parts of plants
Reduction in
• Shoot growth and biomass
• Yield and quality
• Chlorophyll contents
• Photosynthetic rate
• Stomatal conductance
• Water use efficiency
• Antioxidant enzyme activities
• Regulation of heat shock
proteins
• Ultrastructure alterations
Reduction in
• Root growth and biomass
• Mineral uptake by plants
• Antioxidant enzyme
ti iti
et al. (2016a) reported that heat stress decreased the leaf
area, panicle length, the relative water content of spikes, and
relative water content of the leaf of rice plants. Heat stress
did not affect the length of primary panicle branches while
it reduced the length of secondary panicle branches. High
nighttime temperature reduced the rice grain yield and qual-
ity compared to the control (Shi et al. 2016). Maya and Mat-
subara (2013) observed that heat stress (30 °C) significantly
decreased the shoot and root dry weights in cyclamen plant
compared to control (22 °C). Shah et al. (2014) observed
that heat stress decreased the individual rice grain weight
significantly under higher night temperature. Heat stress dur-
ing early reproductive phase reduced the rice yield and yield
components (Wu et al. 2016). Heat stress reduced the root
biomass, root vigor, root traits, and RWC of B. campestris
compared to the control (Yuan et al. 2016). Heat and water-
logging co-stress reduced the cotton fiber qualities and yield
compared to the control (Chen et al. 2017b).
Effect on Photosynthesis
Photosynthesis is susceptible to heat stress and negatively
affected by high-temperature stress (Table 1). Heat stress-
induced reduction in photosynthetic activity has been
attributed to the inhibition of PSII, which also mediates the
decrease in variable chlorophyll fluorescence (Cao et al.
2015; Feng et al. 2014; Guo et al. 2016; Chen et al. 2017a).
Fahad et al. (2016c) observed that heat stress (35 °C and
32 °C day and night temperature) reduced the photosynthesis
rate (day temperature), stomatal conductance, and transpira-
tion rate in two cultivars of rice compared to control temper-
ature (28 °C). Heat stress decreases the water use efficiency
Heat stress
Reduction in
• Carbohydrate metabolism
• Floral bud number
• Pollen performance
• Seed development
Increase in
• Electrolyte leakage
• Hydrogen peroxide
production
• Production of
phytohormones
Shoot
Root
Increase in
• Oxidative stress
• Ultrastructure alterations
13


Table 1  Effects of heat stress in plants

458

Plant species Experiment type Heat stress and duration (day/night) Effects References

13
Wheat Pot containing a mixture of soil and sand in At 4th–5th stage, plants were placed in a Heat stress decreased the chlorophyll Bouchemal et al. (2017)
a 2:1 ratio phytotron at 45 °C for 6 h contents and increased the MDA, EL, and
­H2O2 accumulation. Heat stress increased
POD and CAT activities depending upon
genotypes
Wheat Pot containing a soil Day/night temperatures of 37 °C/27 °C for Heat stressed, reduced growth and chloro- Shirdelmoghanloo et al. (2016)
3-days ina growth chamber, at 10 days phyll contents compared to the control
after anthesis.
Wheat Sand with ½ Hoagland’s solution 2-week-old seedlings were subjected to Heat and light co-stress decreased chloro- Chen et al. (2017a)
high light and heat co-stress (1,800 μmolof phyll contents, relative water contents,
photon ­m−2 ­s−1; 38 ± 2 °C) for 1 and 3 h and and photochemical activity of PSII. Heat
recovered and light co-stress increased the MDA,
EL and H ­ 2O2 contents, and affected the
activities of antioxidant enzymes
Wheat Hydroponic culture Heat stress for 1 h and for 24 h at 40 °C in Heat stress decreased the chlorophyll Demirevska-Kepova et al. (2005)
darkness or in light content, soluble protein content, and elec-
trolyte leakage compared to the control
Wheat Pot containing soil Heat shocked for 5 h at 40 °C during the Heat or drought stress or combined both Grigorova et al. (2011)
sampling day (18-day-old plants) stresses decreased the relative water
contents and increased the electrolyte
leakage, and altered the heat shock pro-
tein expression.
Wheat Plants were grown in one-fourth MS liquid 7-day-old seedlings exposed to 45 °C for Heat stress significantly decreased the root Gupta et al. (2013)
Media 2 h and then plants grown for 3 days and shoot lengths and their dry biomasses
in all genotypes. Heat stress decreased
the chlorophyll contents and membrane
stability index, while it increased the
proline and activities of CAT, POD, and
SOD in plants.
Tomato Plant were grown in growth chambers At 5–6 leaves, Heat stress and high light Heat stress decreased chlorophyll contents Faik et al. (2016)
intensity were applied for 6 days and then and exhibited more negative impact on
for 5 days under control PSII activity than PSI.
Rice Pots containing a mixture of 17 kg soil Four temperature treatments (control, HNT, Heat stress reduced the rice yield and yield Wu et al. (2016)
(loam:sand, 2:1) HDT, and high whole day) were given in components including spikelet fertility,
individual greenhouses number of spikelets per panicle. Heat
stress affected the degradation of floret
and branches and also affected the phyto-
hormones production
Rice Field High night temp. (29 °C) starting from Heat stress decreased growth, head rice Shi et al. (2016a)
panicle initiation until maturity yield, increased chalkiness, and reduced
grain width. However, response varied
among studied genotypes
Journal of Plant Growth Regulation (2020) 39:456–480
 Table 1  (continued)
Plant species Experiment type Heat stress and duration (day/night) Effects References

Rice 15-day-old seedlings were transplanted into Six different day/night temperature regimes Heat stress reduced the pollen tube length, Das et al. (2014)
pots containing clay loam soil (25/15, 30/20, 35/25, 40/30, 45/35 and pollen grain diameter, number of pollens
50/40 °C) during panicle initiation. on stigma, pollen germination, and anther
dehiscence, and reduced the moisture and
protein contents of rice pollens
Maize Seeds were grown on a cotton gauze, lying high- (40 °C), moderate- (30 °C), and low- Germination rate and antioxidant enzymes Deng et al. (2015)
on quartz stones, in a plastic box, contain- (15 °C) temperature stress in germinating seeds varied with the color
ing about 30 ml tap water of the seeds under heat stress
Maize Field Artificial warming (about 2 °C) with heater Heat stress decreased leaf width and thick- Zhang et al. (2013)
at about 2.25 m above the ground ness, mesophyll thickness, and mesophyll
while increased the soluble sugars and
C:N ratio. Heat stress increased the gas
exchange traits compared to the control
Journal of Plant Growth Regulation (2020) 39:456–480

Brassica campestris Sown in sand, and then moved into a
phytotron
Brassica campestris Sown in sand, and then moved into a
phytotron
Grapevine pots containing a mixture of garden earth,
sand, and matrix soil (2:1:1)
After 3 weeks, heat stress (40/30 °C) for
5 days
After 3 weeks, heat stress (40/30 °C) for
5 days
At 10 leaves, leaf disks were treated
with 25, 30, 35, 40, 42.5 °C for 1 h in
600 µmol m−2S−1 light
Heat stress reduced the root biomass, root Yuan et al. (2016)
vigor, root length, total root volume,
surface area, number of tips, and aver-
age diameter. Heat stress increased the
oxidative stress and reduced antioxidant
enzyme activities, and caused root ultras-
tructural alterations.
Heat stress decreased plant height, stem Zou et al. (2017)
diameter, and plant weight, chlorophyll
contents and photosynthetic parameters,
and caused chloroplast ultrastructural
alterations.
Heat stress (> 35 °C) decreased the photo- Sun et al. (2016)
synthetic ­O2 evolution rate and efficiency
of PSII (Fv/Fm) in leaves, and increased
­H2O2 accumulation compared to the
control

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460
of the plant (Zhu et al. 2011a, b). Due to heat stress, transpi-
ration rate of the plant increases which highly influences the
water use efficiency (Topbjerg et al. 2015). High temperature
decreases the net photosynthetic rate which affects the both
transpiration rate and stomatal conductance or mesophyll
photosynthetic capacity (Von Caemmerer and Farquhar
1981). Reduction in stomatal conductance and high intercel-
lular ­CO2 assimilation due to heat stress suggest that reduc-
tion in net photosynthetic rate is attributable to stomatal
closure due to high temperature. However, at medium-high
temperature, decreases in intercellular C­ O2 assimilation and
stomatal conductance show that the net photosynthetic rate
is not only dependent on stomatal closure but also asso-
ciates to inhibition of mesophyll capacity which is further
related to the inactivation of Rubisco, and the limitation of
the capacity of photosynthetic electron transport to regen-
erate Rubisco. Heat stress triggers the overproduction of
ROS which reduces the synthesis of nicotinamide adenine
dinucleotide phosphate hydrogen (NADPH) and adenosine
triphosphate (ATP) resulting in decreased photosynthesis
(Schrader et al. 2004). Overproduction of ROS also disrupts
the thylakoid membrane, resulting in loss of chlorophyll
and finally decreases the photosynthesis (Ristic et al. 2008;
Krause and Weis 1984). Heat stress reduced the chlorophyll
contents in wheat leaves, but the response varied among
studied genotypes (Bouchemal et al. 2017). Similarly, heat
stress decreased the chlorophyll contents and PSII activ-
ity in tomato seedling (Faik et al. 2016). Damage to PSII
is considered to be linked with structural modification of
proteins such as D1 protein, and dissociation of oxygen-
evolving complex and manganese-stabilizing 33 kDa protein
at the PSII reaction center (Wahid et al. 2007). In grapevine
leaves, heat stress (> 35 °C) decreased the photosynthetic ­O2
evolution rate, and efficiency of PSII (Fv/Fm) compared to
the control (Sun et al. 2016).
Effect on Mineral Nutrient Uptake
Heat stress also caused a significant disturbance in plant
mineral nutrition and severely affected the translocation and
accumulation of mineral nutrients in heat-stressed plants.
Cabral et al. (2016) reported that nitrogen (N) at an earlier
point is allocated more in grains compared to tillers in wheat
plants under heat stress, while the phosphorus (P) concentra-
tion was decreased in wheat plant due to heat stress. Moreo-
ver, heat stress caused an influence in ion mobility with the
increasing K/Ca ratio in plants. Heat stress (2 °C higher than
the control) increased the C:N ratio and reduced the mineral
nutrients in leaves of maize (Zhang et al. 2013). Overall, few
studies are available related to the effects of heat stress on
the uptake of mineral nutrients in plants, and more in-depth
studies will help to highlight the mechanisms of nutrient
uptake in heat-stressed plants.
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Journal of Plant Growth Regulation (2020) 39:456–480
Effect on Plant Reproductive System
Heat stress badly affects the germination, anther dehiscence,
and pollination in different plants which resulted in poor and
less grain production and low germination rate of harvested
seeds. The most significant consequences of heat stress in
plant-reproductive phase are shortening of developmental
phases. Pollens’ development and functions are the most
sensitive to heat stress. Heat stress at reproductive stage
disrupts carbohydrate metabolism and impairs reproductive
function that eventually affects seed development (Wu et al.
2016; Bhandari et al. 2016). During reproduction, heat stress
event reduces floral bud number and increases flower abor-
tion with varied degree of sensitivity in various crop plants
(Folsom et al. 2014; Lin et al. 2014; Nguyen et al. 2014).
High temperature also decreases pollen performance in
higher trees, e.g., olive tree (Koubouris et al. 2015). Spikelet
sterility is one of the most potent threats to rice productivity
from global warming.
Jagadish et al. (2009) observed a high level of spikelet
sterility during the process of anthesis in rice plant when
the temperature has risen to higher than 35 °C over the
duration of 1 h. Due to high temperature, spikelet steril-
ity is caused by a disturbance in pollination pairing, poor
anther dehiscence, and germination of pollen (Jagadish et al.
2009; Matsui and Omasa 2002; Das et al. 2014). Fahad et al.
(2015a, b) observed that heat stress reduced the rate of pol-
len germination and pollen count per stigma, and decreased
the pollen and spike fertility, and anther dehiscence in rice,
depending upon the rice genotypes. The low germination
rate of pollen is controlled by several reproductive upheav-
als such as reduced pollen swelling, decreased size of anther
pore, anther dehiscence, and poor pollen reception (Prasad
et al. 2016). Heat stress decreases spike and pollen fertil-
ity mainly due to tight coupling with locules, which causes
low pollen dispersal and eventually poor spikelet fertility in
plants (Zinn et al. 2010).
Ultrastructural Alterations in Plants
Heat stress caused an ultrastructural alteration in roots of B.
campestris as was observed by thickened cell wall, slightly
concentrated cytoplasm, and mild plasmolysis of cells, and
damage to mitochondria (Yuan et al. 2016). In addition,
heat stress (5 days of exposure to 40 °C) severally dam-
aged the chloroplast ultrastructures of B. campestris (Zou
et al. 2006). Artificial warming (2 °C higher than control)
altered the stomatal aperture, the thickness of the cell wall,
chloroplast, and mitochondria of maize leaves (Zhang et al.
2013). Similarly, heat stress damaged the chloroplasts and
mitochondria in leaves of pear cultivars compared to the
control (Liu et al. 2017).
Journal of Plant Growth Regulation (2020) 39:456–480 461
Oxidative Stress in Plants
Heat stress often accompanies oxidative stress and develops
as a result of ROS accumulation in plants (Pucciariello et al.
2012). ROS are partially toxic byproducts of different cel-
lular oxygen-consuming redox processes in plant cells, e.g.,
respiratory electron transport or photosynthesis. Oxidative
stress triggered the build-up of these toxicants which dam-
ages protein, lipids, carbohydrates, and DNA, resulting in
membrane damage and cell death (Gill and Tuteja 2010).
Sharma et al. (2012) reported that ROS accumulation causes
lipid peroxidation and disturbs the membrane permeability
of plant cell. Reactive oxygen species such as hydrogen per-
oxide ­(H2O2), superoxide radical ­(O−), and hydroxyl radical
­(OH−) are produced due to the transfer of an electron to
oxygen. These ROS are toxic and cause damage to chloro-
phyll, lipids, DNA, protein, and almost every other organic
constituent in the cell (Vranova et al. 2002). Several studies
reported that heat stress increased the H ­ 2O2 concentration
in leaves of grape (Yuan et al. 2016; Sun et al. 2016). Heat
stress increased the H
­ 2O2, MDA, and O ­ 2− formation rates but
decreased the SOD, POD, and CAT activities in B. camp-
estris roots (Sun et al. 2016). Heat stress increased H ­ 2O 2,
MDA, and ­O2− formation rates in B. campestris, while SOD,
POD, and CAT activities first increased and then decreased
with the increasing heat stress (Zou et al. 2017).
Heat Tolerance in Plants
The plants can tolerate certain heat levels by modifying the
production of osmolytes and antioxidants and regulating the
heat shock proteins. Under heat stress, plants can regulate
the production of some phytohormones such as abscisic acid
(ABA), gibberellins (GAs), jasmonic acid (JA), and indole
acetic acid (IAA) to enhance the heat resistance (Bita and
Gerats 2013; Hasanuzzaman et al. 2014). IAA and GAs
contribute in the development of processes while JA and
ABA alleviate the effects of environmental stresses such as
drought, cold, heat, and pathogens (Bita and Gerats 2013;
Claeys et al. 2014). Under abiotic stress, plants upregulate
the biosynthesis of ABA to shrink the stomatal opening
and minimize the transpiration to enhance the water use
efficiency (Hasanuzzaman et al. 2014; Khan et al. 2012).
Hydrogen sulfide is a signaling molecular and, as a part of
the defense system, its concentration increases with the heat
stress and enhances the heat tolerance in plants Chen et al.
2016). Heat stress reduced the cytokinins, GA, IAA while
increasing ABA and bound cytokinins in panicles of rice
(Wu et al. 2016).
The plants have well-developed an antioxidant defense sys-
tem to combat with abiotic stresses (Table 1). This antioxidant
system comprises of both enzymatic and nonenzymatic antiox-
idants. When a plant exposes to heat stress, the plant increased
the activity of antioxidant enzymes to recover from oxidative
damages caused by heat stress (El-Daim et al. 2014). Antioxi-
dant enzymes in plants mainly include lower molecular sub-
stances, e.g., α-tocopherol, glutathione, and ascorbate (AsA),
other enzymes such as catalase (CAT), superoxide dismutase
(SOD), ascorbate peroxidase (APX), peroxidase (POD), glu-
tathione reductase (GR) and glutathione peroxidase (GPX)
(Asada 2006). Heat stress increased CAT and POD activities
in wheat plants depending upon genotypes (Bouchemal et al.
2017).
Almost all types of stresses induce the production of heat
shock proteins (HSPs). The HSPs are molecular chaperones,
which improves the thermotolerance of the plant by protecting
the native proteins from denaturing conditions and improves
the protein stability under high temperature stress (Schöffl
et al. 1999). Studies showed that HSPs accumulation has a
strong correlation with heat stress (Liu et al. 2013) such as
maize plant synthesized ZmHSP17.2 (Jorgensen and Nguyen
1994) rice plant synthesized OsHSP26 in leaves (Lee et al.
2007) under heat stress. Asada (2006) observed that sHSP26,
sHSP17.4, and sHSP17.2 were regulated under the heat stress
which showed its important role in heat tolerance of maize
plant. Momčilović et al. (2016) identified a eEF1A (eukary-
otic elongation factor 1A), a cytosolic multifunctional protein
which is considered responsible for developing the thermo-
tolerance in tomato plant under heat stress. Moreover, eEF1A
genes’ isolation and utilization might be beneficial in improv-
ing heat tolerance in plants. Expression of tomato heat shock
proteins improved the tobacco tolerance by increasing the anti-
oxidant capacity (Zhang et al. 2016a, b). It is suggested that
heat tolerance in wheat and other crops may be improved by
modulating expression of plastidial protein synthesis elonga-
tion factor and/or by selecting genotypes having the ability to
produce this protein endogenously (Fu et al. 2008).
The negative effects of heat stress on photosynthesis may be
further increased in the presence of other stresses. For exam-
ple, Chen et al. (2017a) reported that heat and light co-stress
had a synergistic effect on reducing the wheat chlorophyll con-
tents, net photosynthetic rate, stomatal conductance, relative
water contents, and photochemical activity of PSII. Heat stress
increased the accumulation of toxic compounds, i.e., reactive
oxidative species (ROS), in plants which disturbed the syn-
thesis of ATP and NADPH and also affected the permeability
of thylakoid membrane, which could ultimately disturb the
functioning of photosynthetic apparatus (Schrader et al. 2004;
Ristic et al. 2008).
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462
Management of Heat Stress in Plants
Selection of Heat‑Tolerant Cultivars
Selection and breeding of thermotolerant cultivars might
be a useful practice to mitigate the harmful effect of heat
on plants (Chauhan et al. 2009; Khan et al. 2017). Many
studies well documented such cultivars that showed a better
resistance against heat stress compared to sensitive cultivars
(Gupta et al. 2013; Frey et al. 2015; Zhang and Du 2016).
Bita et al. (2011) compared the two cultivars of tomato under
the heat stress (25 to 32 °C) and found that, at moderate heat
stress, heat-tolerant genotype showed the medium transcrip-
tional changes and exhibited upregulated of gene expression
compared to heat-sensitive genotype where downregulation
was observed in gene expression. Huang et al. (2015) iden-
tified the heat-sensitive and heat-tolerant wheat cultivars
under field conditions and found lesser grain yield reduc-
tions in tolerant cultivars than sensitive ones and suggested
that tolerant cultivars might be used in breeding programs
aiming to develop tolerant cultivars of wheat.
Khanna-Chopra and Chauhan (2015) observed the behav-
ior of two genotypes of wheat under heat stress. Results
showed that tolerant genotype showed lower membrane
damage and oxidative stress compared to a sensitive one.
Shi et al. (2017) reported that there were significant dif-
ferences among rice cultivars in rate and duration of grain
filling exposed to high night temperature and those authors
suggested that breeders should also select source–sink
traits to enhance rice, probably other crops, and tolerance
to high night temperature. Tesfaye et al. (2017) suggested
that severe yield losses of maize crop due to heat stress may
be minimized by cultivating heat-tolerant maize varieties.
In B. campestris, genotypes, reduction in root growth and
Fig. 2  Possible management
strategies to reduce heat stress
in plants
Soil
Inorganic Organic
amendments amendments
Fertilizer
management
Other inorganic
amendments
Proper crop
rotation
13
Journal of Plant Growth Regulation (2020) 39:456–480
antioxidant enzymes was lower in heat-tolerant genotypes
than heat-sensitive genotype (Yuan et al. 2016). Pettigrew
(2016) reported a genetic variation in photosynthesis and
heat tolerance in cotton genotypes.
Exogenous Application of Growth Regulators
Osmolytes such as ABA, JA, AsA are also a part of plant
defense system. When plants undergo the oxidative stress,
production of osmolytes also increases. These osmolytes
can protect plants from stressful conditions to some extent.
However, these osmolytes become insufficient to protect
the plant against higher stressful conditions (Fahad et al.
2016c, d). Many studies showed that exogenous applica-
tion of osmolytes played a beneficial role in protecting the
defense system and enhanced the plant tolerance to heat
stress (Figs. 2, 3; Table 2).
Ascorbic Acid
Ascorbic Acid (AsA) is considered as a powerful antioxi-
dant which resists the oxidative damage in plant cells due to
aerobic metabolism and photosynthetic damage under abi-
otic stress (Upadhyaya et al. 2010). Ascorbic acid showed
the positive effect under different abiotic stresses such as
drought stress (Dolatabadian et al. 2009) and salt stress
(Shalata and Neumann 2001; Dolatabadian et al. 2008).
Kumar et al. (2011) observed that AsA (50 µM) improved
the defense system by decreasing the production of MDA
and hydrogen peroxide, and enhanced the germination and
growth of mungbean under different levels of heat stress
(day/night; 30/20, 35/25, 40/30, 40/30 and 45/35 °C).
Management of heat stress in plants
Plant
Selection of heat
Other agricultural
tolerant cultivars
practices
Grafting
Mulching
Biochar
Tillage Genetic engineering
Compost
management
Exogenous Exogenous application
application of of osmolytes
microbes
Journal of Plant Growth Regulation (2020) 39:456–480 463
Fig. 3  Mechanism behind
oxidative stress regulation under
heat stress
Abscisic Acid
Abscisic acid is an important plant hormone which contrib-
utes in plant defense system against different environmental
stresses such as heat, drought, and cold (Zou et al. 2017;
Ding et al. 2010; Kumar et al. 2012). ABA contributes to
the induction of biochemical pathways which are essential
to protect plant under heat stress (Maestri et al. 2002). Many
studies reported that ABA enhances the thermotolerance in
different plant species (Claeys et al. 2014; Ding et al. 2010;
Talanova et al. 2006; Song et al. 2013). Kumar et al. (2012)
observed the effect of ABA (2.5 µM) on chickpea plant at
different levels of heat stress (day/night; 30/20, 35/25, 40/30,
40/30, and 45/35 °C) and reported that ABA improved the
plant growth and defense system at higher heat stress; more-
over, ABA decreased the MDA and H ­ 2O2 contents at the
highest temperature (45/40 °C) compared to that without
ABA treatment. In another study, ABA also upregulated the
different HSPs which play a significant role in heat tolerance
of plant (Zou et al. 2017).
γ‑Aminobutyric Acid
Amino acids (nonprotein) are reported to play a benefi-
cial role in plant functioning under different environmen-
tal stresses due to their involvement in metal binding,
osmoregulation, signaling, and antioxidant defense systems
(Sharma and Dietz 2006). γ-Aminobutyric acid (GABA)
contains free amino acid in a significant fraction in plant
cells and also plays a role in the animal system as a neu-
rotransmitter (Bouche and Fromm 2004). It was observed
that GABA concentration was elevated due to the abiotic
stress including the heat stress (Bartyzel et al. 2003; Bor
et al. 2009). In plants, GABA is involved in different mecha-
nisms such as cytosolic pH regulation, buffering in carbon
and nitrogen metabolism, defending against oxidative stress
and osmoregulation, and defending against herbivorous pests
and signal transduction (Bouche and Fromm 2004; Kinner-
sley and Turano 2000). Due to the calcium-induced activa-
tion of glutamate decarboxylase, GABA accumulates in a
plant cell under heat stress (Locy et al. 2000). Nayyar et al.
(2014) observed the effect of exogenous GABA (1 mM) on
rice plant under heat stress and reported that GABA con-
tent was increased in early days of heat stress (light/dark
42/37 °C), while after two days, its concentration decreased
significantly; moreover, the exogenous application of GABA
increased the endogenous GABA content sevenfold in severe
heat-stressed condition compared to that without GABA-
treated plants. Physiological, morphological, and biochemi-
cal parameters were also improved with the application of
GABA under heat stress.
Brassinosteroids
Brassinosteroids (BRs) are steroidal hormones of plants
which are essential for development and growth. These are
widely distributed in different parts of plants, e.g., vegeta-
tive and reproductive tissues, and generally accumulates in
reproductive organs such as fruits and pollen (Symons et al.
2007). Brassinosteroids are involved in many physiological
processes and responses, e.g., functioning of stomata, respi-
ration, photosynthesis (Thussagunpanit et al. 2015a; Cao and
Hua 2008), ­CO2 assimilation (Xia et al. 2009) ion transport
and cell division (Wu et al. 2014; Vriet et al. 2012). At low
13

Table 2  Effects of different plant growth regulators (PGR) on reducing heat stress in plants
PGR and doses applied
13
Ascorbic acid (50 µM)
Ascorbic acid (70 ppm)
Abscisic acid (2.5 µM)
Abscisic acid (100 µM)
Abscisic acid (0.05, 0.1 mM)
γ-Aminobutyric acid (1 mM)
Brassinoloid (0.1 mgL-1)
Brassinolide (10 µM)
24-epibrassinolide (0.005,
0.25 mg dm−3)
464
Experiment and plant type Heat stress (day/night) Treatment stage Effects References
Hydroponic 30/20, 35/25, 40/30, 40/30 and From start Seeds germination AsA increased the seeds Kumar et al.(2011)
Mungbean 45/35 °C) germination; and SOD, CAT,
APX, GSH activities; and
decreased the MDA and
­H2O2 contents under higher
stress
Greenhouse pots and Field 45/30 °C, 38/24 °C, 32/20 °C Sowing stage, reproductive Improved the leaf SOD, CAT Sarwar et al. (2018)
experiment stage activity, chlorophyll contents,
Cotton net photosynthetic rate, num-
ber of sympodial branches,
boll weight, and fiber quality.
Hydroponic 30/20, 35/25, 40/30, 40/30 and 4 days seedling ABA increased the osmolyte Kumar et al. (2012)
Chickpea 45/35 °C contents (Proline, GB,
Trehalose), survival rate of
seedlings; and mitigated the
oxidative damage
Hydroponic From 28 to 42 °C After ­2nd leave ABA upregulated the heat Liu et al. (2013)
Maize 2 °C interval shock protein and enhanced
the tolerance against heat
stress
Knop’s solution 38 °C One week seedling ABA increased the heat resist- Talanova et al. (2006)
cucumber For 2-24 h ance in cucumber plant
Hydroponic 42/37 °C 4 days seedlings Increased endogenous GABA, Nayyar et al. (2014)
Rice improved the growth, sur-
vival rate, and antioxidant
defense system
Sand 38/25 °C At 16-18 cm seedlings BRs improved the growth, Niu et al. (2016)
L. chinensis chlorophyll content, and
thermotolerance
Soil 45 °C For 4 and 8 h 3 weeks old seedlings Brassinolide spray increased Kurepin et al. (2008)
Brassica napus L. the endogenous ABA content
and enhanced the plant toler-
ance against heat stress
Soil 42 °C for 3 h in darkness 2 leaves stage EBR leaves infiltration Janeczko et al. (2011)
Barley improved the PSII efficiency
of barley
Journal of Plant Growth Regulation (2020) 39:456–480
 Table 2  (continued)
PGR and doses applied
24-epibrassinolide (0.01, 0.1,
1 mg ­L−1)
Citric acid (0, 0.2, 2, 20 mM)
Glycine betaine (100 mM)
Glycine betaine (20 mM)
Sodium hydrosulfide (0.5 mM) Hydroponic
Maize
Sodium hydrosulfide (0.3, 0.6,
0.9, 1.2 mM)
13
Experiment and plant type Heat stress (day/night) Treatment stage Effects References
Vermiculite 40/30 °C 6 weeks after germination EBR increased the heat Ogweno et al. 2008
Tomato tolerance by activating
antioxidant enzymes and
reducing ­H2O2 and MDA
contents. Furthermore, it also
improved the photosynthesis
under heat stress
(Peat + soil + sand) 35/30 °C 50 days plants Citric acid improved the plant Hu et al. (2016)
Tall Fescue growth, membrane stability,
root activity, and antioxidant
defense system and mitigated
physiological damage
Quartzite 39 °C (for 1 & 2 h) 18 days after anthesis Glycine betaine enhanced Wang et al. (2014)
Journal of Plant Growth Regulation (2020) 39:456–480
Wheat tolerance by increasing GB
accumulation, and regulated
the stomatal conductance
and PSII
Soil 40/32 °C Presowing seeds treatment GB application increased Wahid and Shabbir (2005)
Barley For 10 days biomass and yield. It also
enhanced the heat tolerance
by improving photosynthetic
rate, leaf water potentia–sink
relative membrane perme-
ability.
47 °C for 15 h 2.5 days seedlings H2S improved thermotolerance Li and Zhu (2015)
and increased the seedling
survival. Increased activity
of BADH
6-layers wet filter paper 47 °C in dark for 15 h After germination H2S increased the survival rate Li et al. (2014a, b, c, d)
Maize of seedling and improved the
heat tolerance by increas-
ing activity of trehalose-
6-phosphate phosphatase and
trehalose contents in maize
plant
465

Table 2  (continued)
PGR and doses applied
13
Sodium hydrosulfide (0.1, 0.5,
1.0, 1.5 mM)
Sodium nitroprusside (10 µM)
Sodium nitroprusside (200 µM) Soil
Chrysanthemum
Salicylic acid (100 µL 1 mM)
Salicylic acid (10 mM)
Salicylic acid (0.1, 1 and
10 mM)
Salicylic acid (0.1, 0.3 and
0.5 mM)
466
Experiment and plant type Heat stress (day/night) Treatment stage Effects References
6-layers wet filter paper 48 °C for 18 h 3 days seedlings H2S increased the seedlings Li et al. (2013)
Maize survival rate and germina-
tion rate of maize plant. H
­ 2S
treatment decreased level of
electrolyte leakage in roots,
and MDA in coleoptiles.
It improved the pyrroline-
5-carboxylate synthetase and
lowered the proline dehydro-
genase activity
Soil 40, 45, 50 °C for 4 h in dark Four leaves stage SNP (NO donor) improved the Song et al. (2013)
Rice photosynthesis and zeaxan-
thin, and decreased the ­H2O2
accumulation and electrolyte
leakage
45 °C for 3,6 and 12 h 8-10 leaves stage SNP slowed down the decreas- Yang et al. (2011)
ing photosynthetic rate and
lowered the production of
MDA and maintained the
higher performance of SOD,
POD, CAT, and APX
Peat moss + perlite + Vermicu- 28/24 °C for 16 h 1 week old seedlings SA treatment increased net Martel and Qaderi (2016)
lite ­CO2 assimilation and chlo-
Pea rophyll content significantly.
SA improved the plant
growth parameters under heat
stress.
Vermiculite + Sand 38 °C for 2 h 10 days old seedlings SA improved accumulation Kumar et al. (2015)
Wheat of SAGs, total antioxidant
capacity, and osmolytes
under heat stress
Petri dishes 45 °C for 0, 30, 60, 120, Incubation of seeds for 2 days SA application increased the Górnik et al. (2014)
Sunflower 240 min root length and dehydro-
genases activity while it
decreased the electrolyte
leakage.
Quartzite 39 ± 2 °C for 2 h 15 days after anthesis SA increased psbA gene Wang et al. (2014)
Wheat transcription and maintained
the activity of antioxidants.
It also protected the PSII
complex from photo-damage
under heat stress
Journal of Plant Growth Regulation (2020) 39:456–480
 Table 2  (continued)
PGR and doses applied Experiment and plant type Heat stress (day/night) Treatment stage Effects References

Salicylic acid (50 ppm) Greenhouse pots and Field 45/30 °C, 38/24 °C, 32/20 °C Sowing stage, reproductive Improved the leaf SOD, CAT Sarwar et al. (2018)
experiment stage activity, chlorophyll contents,
Cotton net photosynthetic rate, num-
ber of sympodial branches,
boll weight, and fiber quality
Salicylic acid (1 mM) Peat + vermiculate 42 °C for 36 h 5th leaf stage Improved the gas exchange Jahan et al. (2019)
Tomato parameters and antioxi-
dant enzymes activity, and
reduced the oxidative dam-
age due to heat stress
Proline (10 µM) Hydroponic 30/20, 35/25, 40/30, 45/35 °C From seed germination Proline increased osmolytes Kaushal et al. (2011)
Chickpea content (proline, ascor-
bic acid, glutathione) and
Journal of Plant Growth Regulation (2020) 39:456–480

improved antioxidant defense

system
Trehalose (1.5 mM) Hydroponic 40 °C for 24 h 15 days seedling for 3 days Trehalose decreased the pro- Luo et al. (2010)
Wheat duction of ROS and protected
the protein in thylakoid mem-
brane and photosynthetic
capacity
Trehalose (30 mM) Soil 40 °C for 3 days 6 years old plants Trehalose decreased the Zhao et al. (2019)
Herbaceous peony fluorescence signal intensity,
­H2O2 content, MDA and
Relative Electric Conductiv-
ity in heat-stressed plants.
Also improved the photo-
synthetic and antioxidant
enzymes parameters
Sperimidine (1 mM) Hydroponic 42 °C for 48 h 14 days old seedlings Sperimidine enhanced the Mostofa et al. (2014)
Rice antioxidant and decreased the
oxidative damage by decreas-
ing the production of MDA
and ­H2O2
Sperimidine (1 mM) Pot, cucumber 42/32 °C for 9 days 2 days of preculture Sperimidine increased the Zhou et al. (2016)
plant growth and photo-
synthesis compared to the
control

13
467

Table 2  (continued)
PGR and doses applied
13
Sperimidine (1.5 mM)
Glutathione (0.5 mM)
5-aminolevulenic acid (3 µM)
Hydrogen peroxide (30 ppm)
2,3-Butanediol
468
Experiment and plant type Heat stress (day/night) Treatment stage Effects References
Soil 40 °C for 5 days Grains filling stage Sperimidine improved the Fu et al. (2019)
Rice seeds germination percent-
age, germination index, grain
quality vigor index, seedling
shoot height and dry weight
of seeds harvested. It also
improved the antioxidant
enzymes activity
Hydroponic 42 °C for 24 and 48 h 6 days old seedling GSH enhanced the heat toler- Nahar et al. (2015)
Mungbean ance in plants by improving
the antioxidant and glyoxa-
lase system while decreasing
the production of ROS
Hydroponic 42/38 °C 2-leaf stage ALA improved the antioxidant Zhang et al. (2012)
Cucumber defense system and decreased
the ROS production under
heat stress
Greenhouse pots and Field 45/30 °C, 38/24 °C, 32/20 °C Sowing stage, reproductive Improved the leaf SOD, CAT Sarwar et al. (2018)
experiment stage activity, chlorophyll contents,
Cotton net photosynthetic rate, num-
ber of sympodial branches,
boll weight, and fiber quality
Fritted clay 35/30 °C day/night, 20/15 °C 10 days interval Butanediol improved the heat Shi et al. (2018)
Agrostis stolonifera day/night tolerance of plant by upregu-
lation of gene related to cell
elongation and metabolism.
It also enhanced the accu-
mulation of organic acids,
sugars, and sugars’ acid in
plant
Journal of Plant Growth Regulation (2020) 39:456–480
Journal of Plant Growth Regulation (2020) 39:456–480 469
concentration, it improves the growth parameters and also
improves the thermotolerance of the plant (Ogweno et al.
2008; Thussagunpanit et al. 2015b; Kurepin et al. 2008).
Many studies have proven that BRs enhances the heat toler-
ance in plants which might be due to the synthesis of HSPs
in plants (Dhaubhadel et al. 1999). Moreover, BRs enhance
the activity of antioxidant enzymes and reduce the peroxida-
tion of membrane lipid by scavenging the ROS which are
produced due to heat stress (Janeczko et al. 2011; Niu et al.
2016; Yun-Ying et al. 2009).
Citric Acid
Citric Acid (CA) is an important organic acid which has
been closely related to different environmental stresses in
plants (Gao et al. 2010). Citrate complex is the mobile that
formed iron, which assists in iron transportation inside the
plant system (Hell and Stephan 2003). It has been reported
that this complex increases the chlorophyll content and vase
life of Lilium and tuberose (2012). Moreover, it acts as anti-
oxidant respiratory metabolism intermediate participating in
the defense pathways under heat stress (Zhao et al. 2015).
Hu et al. (2016) observed the effects of different levels of
CA (0, 0.2, 2, 20 mM) on Tall fescue under heat stress (day/
night 35/30 °C while control 25/20 °C) and reported that
CA mediates the heat stress by decreasing MDA and elec-
trolyte leakage, and improved the root activity, Fv/Fm ratio,
antioxidant enzymes, and HSP gene family expression under
heat stress condition.
Glycinebetaine
Glycinebetaine (GB) is biosynthesized naturally under dif-
ferent stresses in plants (Jagendorf and Takabe 2001). It is
nontoxic, water soluble, and absorbable in various plant
tissues (Diaz-Zorita et al. 2001). Exogenous application
of GB showed beneficial effects on plants (Rahman et al.
2002; Chen and Murata 2002; Ahmad et al. 2013). Many
studies also reported its beneficial role in plants under high
temperature stress (Yang et al. 2007; Zhang et al. 2012; Li
et al. 2014a, b, c, d). Glycinebetaine (GB) protects the plant
by maintaining the membrane integrity, stabilizing activi-
ties, and maintaining the structure of protein and enzymes
complex in stressed plants (Sakamoto and Murata 2002).
Moreover, GB reduces the leakage of ions by improving cell
membrane structure in the plant under heat stress (Wahid
and Shabbir 2005). Wang et al. (2014) reported that foliar
application of GB (100 mM) improved the heat tolerance of
wheat by increasing chlorophyll content, and GB content
under heat stress (39 ± 2 °C). Stomatal conductance was also
improved due to the GB application.
Hydrogen Sulfide
Hydrogen sulfide ­(H2S) is reactive water-soluble gas. In
plants, it is involved in different physiological processes in
the defensive system against different environmental toler-
ance impacts (Li et al. 2012; Shen et al. 2013; Li and Gu
2016; Li and Zhu 2015). It is also involved in guard cell
signaling in plant Garcia-Mata, and Lamattina (2010) [133]
reported that pretreatment of ­H2S donor sodium hydrosulfide
(NaHS) (0.5  mM) enhanced accumulation of betaine in
maize plant under heat stress (47 °C) by improving the activ-
ity of betaine aldehyde dehydrogenase (BADH) which is a
key enzyme in betaine biosynthesis which finally increased
the survival percentage of seedlings. Many other studies
also showed the positive effect of H ­ 2S in seed germination
under different environmental stresses (Li and Zhu 2015;
Fang et al. 2014; Shan et al. 2014). Li et al. (2014a, b, c,
d) concluded that ­H2S (0.7 mM) application improved the
tolerance and antioxidant defense system of maize plant by
increasing the activities of SOD, CAT, GR, GPX, and GSH
under normal condition, and increased the plant resistance
when exposed to heat stress (47 °C in the dark).
Nitric Oxide
Nitric oxide (NO) is a short-lived free radical and found
in plant cells and organs (Stöhr and Stremlau 2006). It
is involved in different functions in plant development,
growth, and regulation of different processes, e.g., stressed
responses, adaptation, and programmed cell death (Wende-
henne et al. 2004; Shapiro 2005; Neill et al. 2008). It shows
beneficial behavior toward the regulation of respiration
due to its affinity for mitochondrial and glycolysis oxida-
tion enzymes (Zottini et al. 2002). Sodium nitroprusside
(SNP) (Nitric oxide donor) elevates the heat tolerance by
activating the antioxidant enzymes (Karpets et al. 2011).
Song et al. (2013) observed that SNPs (10 µM) enhanced
the heat tolerance in rice plant upon increasing the photo-
synthetic rate and maximal fluorescence, and decreased the
initial fluorescence significantly. Moreover, H­ 2O2 content
and electrolyte leakage were reduced with the application
of SNP, which was increased due to heat stress (40, 45, and
50 °C) in rice plant. Another study was done by Yang et al.
(2011) who observed the SNP role in mediating the harm-
ful effects of heat stress on Chrysanthemum morifolium.
Sodium nitroprusside slowed the heat-induced reduction in
net photosynthetic rate and photosynthetic pigment; and also
lowered the malondialdehyde accumulation and nonphoto-
chemical quenching of fluorescence, and finally improved
the activities of antioxidant POD, SOD, and catalase under
heat stress.
13

470
Salicylic Acid
Salicylic acid (SA) is an endogenous growth regulator and
phenolic hormone of the plant which is involved in different
responses as a signaling molecule, e.g., nutrient uptake and
transport, chlorophyll and protein synthesis, stomatal clo-
sure, and exchange in the plant (Amin et al. 2013). Salicylic
acid in low concentration has been proven beneficial for the
plant in reproductive yield and high biomass (Amin et al.
2013; Elwan and El-Hamahmy 2009; Gharib 2006). Martel
and Qaderi (2016) reported that SA (1.0 mM) mitigate the
harmful effect of heat stress (day/night 28/24 °C) on pea
plant and improved growth and defense system by increas-
ing the biomass, chlorophyll content, transpiration rate, sto-
matal conductance, and water-use efficiency compared to
without SA under heat stress. In another study, Kumar et al.
(2015) observed that SA (100 mM foliar spray) enhanced the
thermotolerance of wheat by regulating the accumulation
of osmolytes, stress-associated gene, and total antioxidant
capacity under heat stress (38 °C).
Proline
Proline is an amino acid that have a potential to protect plant
under abiotic stress (Verbruggen and Hermans 2008) and
play important roles in different plant mechanisms, e.g.,
turgor generation, antioxidant defense system, and stor-
age of carbon and nitrogen (Smirnoff and Cumbes 1989),
adaptive response (Verbruggen and Hermans 2008), stabi-
lizing the structure of protein, and maintaining the redox
status and cytosolic pH (Maggio et al. 2002). Kaushal et al.
(2011) reported that proline (10 µM) significantly improved
the growth parameter of chickpea under heat stress (day/
night 30/20, 35/25, 40/30, and 45/35 °C). Proline alleviated
harmful effects of heat by decreasing the contents of ­H2O2
and MDA and enhanced the activities of antioxidants such
as catalase, ascorbate peroxidase, superoxide dismutase,
and glutathione reductase, and also increased the level of
osmolytes’ (proline, ascorbic acid, and glutathione) produc-
tion in stressed plants. Proline proved beneficial in reducing
the cellular injury and protecting the several enzymes asso-
ciated with carbon and oxidative metabolisms in chickpea
plants.
Trehalose
Trehalose accumulation was reported by Benaroudj et al.
(2001) during heat stress which protects cellular proteins
of Saccharomyces cerevisiae from oxidative damage. In
plants, chloroplast thylakoid membrane is highly suscepti-
ble to high temperature. Heat stress leads to the detachment
lipid bilayer and causes damage to an oxygen-evolving com-
plex of PSII (Los and Murata 2004; Komayama et al. 2007).
13
Journal of Plant Growth Regulation (2020) 39:456–480
Luo et al. (2010) reported that trehalose (1.5 mM) increased
the amount of endogenous trehalose, protected the protein
in thylakoid membrane, and improved the photosynthetic
capacity in wheat plant under heat stress.
Spermidine is common polyamine which is involved in
the adaptation of plants toward different abiotic stresses,
e.g., heat (Tian et  al. 2012), chilling (Yamamoto et  al.
2012), heavy metals (Xu et al. 2011) and drought (Kubis
2008). Spermidine is closely related to the enhancement of
the antioxidative capacity of the plant under stressful condi-
tions (Tian et al. 2012). Mostofa et al. (2014) observed that
foliar spray of spermidine (1 mM) improved the rice toler-
ance by decreasing the oxidative damage and enhanced the
antioxidants while also improving the photosynthetic rate
under heat stress (42 °C). Similarly, exogenous spermidine
increased the heat-stressed cucumber growth and chloro-
phyll concentration in leaves compared to the control (Zhou
and Guo 2009).
Glutathione
Glutathione (GSH) is a nonprotein, water-soluble thiol com-
pound which is account for 1–2% of total sulfur (S) com-
pound in plants. It plays an important role in the biochemical
function of plants (Foyer and Noctor 2003). Reduced GSH
works as an antioxidant and reduces the production of ROS
(Shao et al. 2005). While in the glyoxalase system, it acts as
cofactor during the process of methylglyoxal detoxification
(Yadav et al. 2008). Nahar et al. (2015) reported that GSH
improved the thermotolerance in mungbean by improving
the photosynthetic system, and antioxidant and glyoxa-
lase systems by reducing the ROS production. Moreover,
it increased the endogenous GSH content and reduced the
methylglyoxal under heat stress.
5‑Aminolevulinic Acid
5-aminolevulinic acid (ALA) is an important precursor in
the biosynthesis of porphyrin compounds (Von Wettstein
et al. 1995). Many studies reported the beneficial effects of
ALA on the plant in improving tolerance under abiotic stress
(Balestrasse et al. 2010; Xu et al. 2015). Zhang et al. (2012)
concluded that foliar application of ALA (3 µM) improved
the activity of antioxidant enzymes and reduced the pro-
duction of MDA, ­H2O2, and superoxide radical under heat
stress.
Thiourea
Thiourea is an important molecule in alleviating the abi-
otic stress as it contains two beneficial functional groups,
“thiol” plays an important role in oxidative stress while
“imino” group fulfills the nitrogen requirement in stressed
Journal of Plant Growth Regulation (2020) 39:456–480 471
plants (Akladious 2014). Studies reported that thiourea spray
reduced the biosynthesis of ABA and enhanced the uptake of
potassium ion in chickpea under high temperature (Aldasoro
et al. 1981). Akladious (2014) observed that seed pretreat-
ment with thiourea (10 mM) increased the growth param-
eters, chlorophylls, relative leaf water content, nitrate reduc-
tase activity, nutrient status, and oil content in sunflower
under heat stress (35 and 45 °C). Moreover, it also improved
the antioxidants’ (enzymes and nonenzymes) activities.
Coronatine
Many studies suggested the application of some signal-
ing molecules to prepare the plant defense system before
exposure to the stress condition. For example, Ceylan
et  al. (2013) observed that pretreatment of coronatine
(0.01 µM) increased the heat tolerance in chickpea plant.
In the untreated plant, MDA, H ­ 2O2, and proline levels were
increased rapidly when exposed to heat stress; however, in
coronatine, ROS production was significantly reduced and
the heat tolerance significantly improved.
Exogenous Application of Microbes
In plants, many beneficial microbes play an important role
in promoting plant growth, yield, and defense through sym-
biotic relationship by enhancing nutrient and water uptake,
water-use efficiency, survivability without any harm, and
endogenous hormone levels (Khan et al. (2012). Application
of arbuscular mycorrhizal fungi (AMF) has been reported
to improve the tolerance in plants against the different
abiotic stresses (Birhane et al. 2012). Under heat stress,
AMF improved the growth by enhancing the nutrient and
water uptake, and also increased the activity of antioxidant
enzymes in cycleman plant (Maya and Matsubara 2013).
The arbuscular mycorrhizal fungus also improved the pho-
tosynthetic rate and water-use efficiency in maize and wheat
plants under heat stress (Zhu et al. 2011a, b). Cabral et al.
(2016) observed that AMF increased the number of grain per
spike in wheat plant under heat stress compared to the heat
stress alone. The carbon concentration in spikes was also
increased due to the application of AMF which might be due
to the change in source–sink of carbon allocation. Another
possibility of an increased level of carbon in spike might
be the availability of carbon during growth stage which is
considered as a symbiotic phenomenon of AMF. This higher
level of carbon in spikes also contributes to the photosyn-
thetic activity in the plant. Waqas et al. (2015) conducted a
study to observe the effects of endophytic fungus, Paecilo-
myces formosus, on rice under heat stress and observed that
fungus application improved the rice growth, regulated the
phytohormones, e.g., ABA and JA by reducing the impact
of heat stress, and increased the total protein content in
rice plant under heat stress compared to noninoculated rice
plants.
These beneficial effects might be due to the production
of different organic acids, e.g., quinic acid, malic acid, tar-
taric acid, and oxalic acid by P. formosus fungus (Waqas
et al. 2014), which finally lowered the pH of surrounding
soil and due to acidifying condition, mineral released the
inorganic phosphate which was in available form for uptake
by plant (Rodriguez and Fraga 1999). In addition, seed treat-
ment with microbes increased the growth and tolerance in
heat-stressed wheat seedlings (El-Daim et al. 2014). Overall,
from the above studies, it seems that the use of microbes
might be a useful biotechnological tool to enhance heat
stress tolerance in plants. However, further studies might be
helpful to identify the mechanisms of microbes assisted heat
stress tolerance in plants.
Use of Inorganic Amendments
Selenium (Se) is an essential constituent of animal and
human nutrition due to its presence in guaiacol peroxi-
dase (GPXs) (Seleno-enzyme) at an active site, therefore
Se often itself performs as an antioxidant (Djanaguira-
man et al. 2010). The use of Se has been shown to enhance
plant tolerance under different abiotic stresses such as heat
(Haghighi et al. 2014; Balal et al. 2016), heavy metal (Qing
et al. 2015), and drought (Durán et al. 2016). Selenium
enhances the growth and yield in plants under heat stress
by improving the heat resistance. For example, Balal et al.
(2016) reported that foliar spray of Se (8 µM) showed ben-
eficial effects on cucumber plant under heat stress (day/night
40/30 °C) by improving photosynthetic rate, stomatal con-
ductance, and transpiration rate. Exogenous application of
Se also increased the chlorophyll contents and antioxidative
activities, while it decreases electrolyte leakage, MDA and
­H2O2 content, and also improves the osmotic-adjustment
capacity of wheat under heat stress (Iqbal et al. 2015). Seed
priming with Se (60 µM) enhanced the rice tolerance to heat
stress by reducing the oxidative stress and enhancing the
antioxidant activities (Hussaine et al. 2016). Similarly, Se
application in hydroponic solution reduced the oxidative
stress and enhanced the activities of SOD, CAT, APX, GR,
and MDHAR in heat-stressed maize roots compared to the
control (Yildiztugay et al. 2017).
Goswami et al. (2015) observed that exogenous applica-
tion of Ca ion increased the proline, amino acid content, and
total antioxidant capacity and reduced the oxidative stress in
wheat under heat stress. Similarly, Ca decreased the oxida-
tive stress and increased POD, SOD, and CAT activities in
wheat under heat stress (Kolupaev et al. 2005). Similarly,
Ca improved the photosynthesis in tobacco under heat stress
(Tan et al. 2011). Mengutay et al. (2013) reported that ade-
quate supply of Mg (450 µM) enhances the crop tolerance
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472
and growth and biomass under heat stress by improving the
photosynthetic rate, regulating the antioxidant enzymes in
wheat and maize plants compared to the low supply of Mg
(15, 20 µM) in the hydroponic medium. Studies reported
that chlorophyll content was significantly decreased in S
deficient plant under heat stress (Astolfi et al. 2003; Mobin
2010). Mobin et al. (2017) reported that adequate S appli-
cation increased the plant biomass and growth under heat-
stressed condition compared to S-starved plants. Moreover,
S mitigated the oxidative stress by reducing the generation of
reactive oxygen species and also increased chlorophyll con-
tents under heat stress compared to S-starved plants. Zinc
(Zn) nutrition helps the plant to enhance the defense system
against heat stress by maintaining the membrane integrity
(Graham 2004).
Peck and McDonald (2010) observed that low Zn sup-
ply significantly reduced the growth parameters, while the
adequate supply of Zn minimized the negative effect of heat
stress. An antioxidant property such as SOD activity was
observed to be more stable with the application of Zn on
wheat plant under heat stress compared to control. Plants
with low Zn treatment showed higher sensitivity toward heat
stress compared to adequate Zn treatment. Nitrogen applica-
tion regulates the nutrient uptake in plants under heat stress
(Zhao et al. 2008; Demmig-Adams et al. 2014). Hassan et al.
(2015) reported that foliar application of N levels increased
the chlorophyll content, net photosynthetic rate, and sto-
matal conductance of heat-stressed wheat seedlings. Shi
et al. (2017) reported that total N did not reduce the adverse
effects of high night temperature on rice growth and yield.
Silicon (Si) has been shown to reduce the toxic effects of
abiotic stresses in plants (Rizwan et al. 2012, 2015). Si is
involved in the thermal stability of lipids in the cell mem-
brane of plants under heat stress (Agarie et al. 1998). Silicon
application increased the transpiration rate and antioxidant
enzymes’ activity, which alleviate the toxic effect of ROS
under heat stress (Soundararajan et al. 2014).
Use of Organic Amendments
A large number of organic amendments have been used for
the mitigation of abiotic stresses in crop plants (Rehman
et  al. 2016; Rizwan et  al. 2016). These organic amend-
ments mainly include composts, manures, crop residues,
and biochar. Studies regarding the use of organic amend-
ments in reducing heat stress in plants are rare. Recently, it
has been reported that biochar, a pyrolyzed organic mate-
rial produced under reduced oxygen supply, applied along
with mineral nutrients such as P may alleviate heat stress
in plants (Fahad et al. 2015a, b; Fahad et al. 2016a, b, c, d,
e). Fahad et al. (2015a, b) reported the beneficial effects of
P and biochar effects on rice plants under heat stress. Bio-
char alone or in combination with P increased the pollen
13
Journal of Plant Growth Regulation (2020) 39:456–480
attributes (pollen germination rate, spike fertility, and anther
dehiscence) in heat-stressed rice cultivars compared to the
only heat-stressed plants (Fahad et al. 2015a, b). In another
study, Fahad et al. (2016b) observed the beneficial effects of
P and biochar on different morphological and physiological
attributes of rice under heat stress. The highest water-use
efficiency and photosynthetic rate were observed in P and
biochar combined treatment in heat-stressed rice plants.
Maximum grain yield, spikelets per spike, grain filling rate,
and 1000 grains weight were observed in P + biochar treat-
ments compared to the control. The authors suggested that
the increase in pollen fertility and rice biomass with biochar
application under heat stress might be due to the release of
nutrients from the biochar. Application of farm manure with
other amendments increased the tomato growth and biomass
under heat stress (Paul et al. 2017).
Other Agricultural Practices
Many scientists also suggested some agricultural practices
to minimize the harmful effect of heat on plant growth and
development. Kaolin is a white, inert clay mineral, and its
foliar spray can reduce the harmful effect of light and heat
stresses on physiology of plant and quality of product by
reflecting the infrared and ultraviolet, which improves the
water condition in plant (Glenn and Puterka 2005; Glenn
et al. 2010; Ou et al. 2010). Dinis et al. (2016) reported that
kaolin (5% w/v) application decreased the susceptibility to
photoinhibition with more efficient photochemical quench-
ing and increased the active PSII reaction centers’ accumula-
tion in grapevine plant.
Grafting is an established technique for asexual propa-
gation in agriculture and horticulture. Rootstock and scion
grafts were reported to improve the biotic and abiotic
stresses tolerance in plants (Kim et al. 2001; Prassinos et al.
2009; Xing et al. 2015). Studies on grafting unions have
become interesting for horticulturists using genomic and
proteomic techniques to observe the transfer of signal trans-
duction and genetic material pathways from root to shoot
and shoot to root (Cookson et al. 2013; Vitale et al. 2014;
Kumari et al. 2015). Grafting union development is a com-
plex process during which physiological and histological
changes occur, e.g., regeneration of organs and exchange of
genetic material between scions and rootstocks (Stegemann
and Bock 2009). Muneer et al. (2016) conducted a study
on grafting union and reported that graft interface defended
the plant system against heat stress by adjusting their prot-
eomic and physiological responses to develop new cellular
homeostasis and also upregulated many proteins for cellular
defense under diverse temperatures.
Soil management practices can also be beneficial to mini-
mize the harmful effect of heat stress (Singh et al. 2009).
Mulching possesses water-conserving effect by decreasing
Journal of Plant Growth Regulation (2020) 39:456–480 473
evaporative loss and runoff, and also adjusts the soil tem-
perature oscillations (Pieri 1989). Under hot conditions,
surface soil layer (if bare) temperature can be exceeded by
10–15 °C. Under such conditions, staw mulch can enhance
seedling survival and emergence (Fischer et al. 2002). Paul
et al. (2017) well documented the positive effect of soil
treated with inorganic nutrient (N, P, K, Ca, Zn) in com-
bination with organic material, e.g., farm yar manure (10 t
­ha−1) and straw mulch (6 t ­ha−1) on tomato plant under heat
stress. These amendments significantly improved the chloro-
phyll content, membrane integrity, SOD, and soluble sugar
in potato plant under heat stress. Proper crop rotation and
adjusting N supply may reduce the harmful effects of global
warming without affecting the economic benefits (Min
et al. 2016). Similarly, the negative effects of heat stress
can also be minimized by adjusting the sowing dates of the
crops in areas susceptible to heat stress during the growth
period (Zhu et al. 2013). Heat priming at preanthesis stage
enhanced the postanthesis heat tolerance in wheat (Xin et al.
2016). This showed that a slight increase in temperature at
an early growth stage might be effective in reducing heat
stress at later growth stages. Drought priming at vegetative
growth stages enhanced the wheat tolerance to drought and
heat stresses during grain filling (Wang et al. 2010).
Genetic Engineering
Genetic engineering is a modern technique to enhance
tolerance in the plant under different biotic and abiotic
stresses. In this technique, a specific gene which controls
the mechanism and production of different osmolytes
is isolated from tolerant plant and then introduced in
another sensitive plant which enhances the tolerance of
plant against different stresses (Khan et al. 2009; Wang
et al. 2009). Li et al. (2014a, b, c, d) isolated a cDNA
clone encoding BADH gene (betaine aldehyde dehydro-
genase) from a heat-tolerant spinach plant and introduced
it into tomato plant via Agrobacterium-mediated trans-
formation and observed that the BADH gene enhanced
the plant tolerance by enhancing capabilities of glycine
betaine accumulation, improving the photosynthetic
capacity, reducing the production of ROS, and increasing
the antioxidant capacity in transgenic tomato plant com-
pared to nontransgenic plant under heat stress. A similar
study was done by Wang et al. (2014), and they gener-
ated a wheat variety by introducing the pABH9 plasmid
encoding the BADH gene cloned from Atriplex hortensis
plant (Guo et al. 2000) which enhanced the plant toler-
ance by increasing the GB content, and improving the
photosynthetic activity and antioxidant defense systems
under heat and drought stresses. Zhang et al. (2016a, b)
improved the heat tolerance in tobacco plant by expressing
a chloroplast small heat shock gene (LeHSP21) in tobacco
via Agrobacterium-mediated transformation. Under heat
stress, these transgenic tobacco plants showed better toler-
ance by significantly increasing the antioxidant enzymes
and proline content compared to the nontransgenic wild-
type plants. Overexpression of OsMYB55 upregulated the
genes involved in heat and drought stresses in maize and
improved the growth and reduced the leaf damage under
heat stress (Casaretto et al. 2016).
Conclusion and Future Perspectives
Heat stress negatively affected the plant growth, biomass,
yield, chlorophyll contents, photosynthetic parameters,
and caused the ultrastructural alteration in different parts
of the plants. Heat stress caused the oxidative stress in
plants. Ultrastructural changes in plants were observed
under heat stress. Mineral nutrient uptake and osmolyte
production in plants were affected during heat stress.
Plants can tolerate certain levels of heat stress by modify-
ing antioxidant enzyme activities and by regulating heat
shock proteins. Exogenous application of PGRs, microbes,
proper mineral nutrition, and use of soil amendments
have been employed for the mitigation of heat stress in
plants. Furthermore, selection of heat-tolerant cultivars,
genetic engineering, and proper agricultural practices also
enhanced the plant tolerance to heat stress. However, the
response of each management strategy varied with time
and duration of heat stress as well as plant species. The
selection of heat-tolerant cultivars with combined appli-
cation of amendments and proper agricultural practices
might be an effective strategy in reducing heat stress in
plants. Although, recently, a large number of approaches
have been evaluated in reducing the heat stress in plants,
further studies will help to enhance the heat tolerance in
plants including the following:
• There is a need to evaluate the effects of different organic
amendments in plants under high-temperature stress.
• Only a few studies have reported the beneficial effects
of microbes in reducing heat stress in plants, and fur-
ther studies will be helpful to identify the mechanisms
of microbes assisted heat stress tolerance in plants.
• There is a need to evaluate the integrative soil manage-
ment practices in reducing heat stress in crop plants.
• Although selection and growth of heat-tolerant cultivars
may be an effective strategy in reducing the negative
effects of heat stress on crops, there is further need to
develop heat-tolerant cultivars through breeding pro-
grams.
• There is a need to identify the heat-tolerance mechanisms
at molecular levels in many plant species.
13

474
Acknowledgements  The authors wants to say thanks to Higher Edu-
cation Commission (HEC), Pakistan for financial support. This study
also financially assisted by HEC, Pakistan under HEC Project No.
20-3653/NRPU/R&D/HEC/14/437 and NRPU Project No. 5634/
Punjab/NRPU/R&D/HEC/2016.
Compliance with Ethical Standards  30:118–151
Conflict of interest  The authors declare that there are no conflicts of
interest or any competing interests regarding the publication of this
paper.
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