Tolerance mechanisms for breeding wheat against heat stress: A review
S. Sarkara, A.K.M.Aminul Islamb,*, N.C.D. Barmab, J.U. Ahmedc,* a Department of Genetics and Plant Breeding, Faculty of Agriculture, Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur 1706, Bangladesh b Bangladesh Wheat and Maize Research Institute, Nashipur, Dinajpur, Bangladesh c Department of Crop Botany, Faculty of Agriculture, Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur 1706, Bangladesh
A R T I C L E I N F O Article History:
Received 3 April 2020 Revised 3 November 2020 Accepted 4 January 2021
Available online 23 January 2021 Edited by S Barnard
A B S T R A C T Heat stress is one of the major abiotic stresses affecting the growth and yield-related characters of wheat.
Using various genetic approaches we can develop heat tolerant wheat varieties in order to mitigate the effect of heat stress on wheat production. Currently different strategies have been adopted to develop thermotoler- ance in wheat. Development of thermotolerant wheat varieties is one of the major steps toward the improve- ment of wheat yield against heat stress. For this purpose, it is important to have a complete and clear concept of the morpho-physiological, biochemical and molecular mechanisms of heat tolerance in wheat. This review may provide better knowledge about heat tolerance through discussing the morphological, physiological, biochemical and molecular mechanisms of heat tolerance in wheat based on different parameters such as grain filling duration, grain yield, leaf senescence, canopy temperature depression, photosynthesis, chloro- phyll content, membrane thermostability, translocation of photo-assimilates, starch synthesis, antioxidant response, protein synthesis and omics approaches.
© 2021 SAAB. Published by Elsevier B.V. All rights reserved.
Keywords:
Heat stress Tolerance Canopy Photosynthesis Membrane stability
Antioxidants Omics Grain yield 1. Introduction The changes in world climate has been severely affecting the global wheat production (Qin et al., 2002). As a strategic cereal crop of several countries in the world, production of wheat has become one of the ultimate factors for food security (Curtis and Halford,
2014). Wheat provides ̴ 55% and ̴ 20% of the global consumption of carbohydrates and calories respectively (Enghiad et al., 2017). By
2050, considerable research attentions will be continued toward wheat in order to feed around nine billion population of the world (Godfray et al., 2010). With growing global population, it is antici- pated that the demand for wheat will be increased which will require an increase of global wheat production by 2% annually (Gill et al.,
2004). But, one of the major problems in wheat production is the shortening of winter period which causes temperature stress to wheat. The primary cause of increasing global mean temperature is the rise in atmospheric CO2 that increases the frequency, intensity and duration of heat waves (Chavan et al., 2019). This increasing tem- perature leads to cause heat stress that has a profound effect on global wheat production (Melloy et al., 2014; Liu et al., 2017). An increase of 1 °C atmospheric temperature may reduce the wheat yield by 10% (Lesk et al., 2016). In warmer regions, grain yield of wheat are more likely to be reduced than in cooler regions (Liu et al., 2019). The annual mean temperature in a warmer region like Mediterranean basin has been supposed to be increased by 3 to 4 °C which may lead to the decrease in total wheat grain yield of about 18% to 24% in this area (Asseng et al., 2015). Rise in temperature that occurs between heading and maturity stage of crop is considered as terminal heat stress (El Hassouni et al., 2019). This terminal heat stress at reproduc- tive phase of wheat affects the anthesis and grain filling causing a severe yield reduction (Hays et al., 2007). For flowering and grain fill- ing of wheat, the optimum temperature ranges from 12 °C to 22 °C (Kumudini et al., 2014). Significant loss in grain yield may occur when wheat is subjected to ambient temperature more than 35 °C for a short period of time (Wolfgang et al., 2018). Based on the duration and extent of temperature, plant responses may significantly differ to heat stress (Table 1) (Ruelland and Zachowski, 2010).
Under heat stress, plants exhibit different morphological, physio- logical, biochemical and molecular alteration and adaptation strate- gies to develop heat tolerance (Fig. 1). Good germination potential, better vegetative growth, leaf rolling or leaf folding, inhibition of early leaf senescence, better plant biomass accumulation etc. can be considered as morphological adaptations of wheat against heat stress. Early maturation with smaller yield losses may also be attrib- uted as an avoidance mechanism under heat stress. Physiological responses of wheat plant to heat stress can be divided into two dis- tinct mechanisms; avoidance and tolerance (Adams et al., 2001).
* Corresponding author.
E-mail address: jahmed06@bsmrau.edu.bd (J.U. Ahmed). https://doi.org/10.1016/j.sajb.2021.01.003
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South African Journal of Botany 138 (2021) 262277
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Increased root system, enhanced stomatal conductance, changing leaf orientation, increased leaf thickness and increased transpirational cooling are the avoidance mechanisms those help to escape heat stress where water stress is not a limiting factor (Fahad et al., 2017).
But a different scenery of decreasing stomatal and lenticular conduc- tance has been found as avoidance mechanism to drought stress (Goufo et al., 2017). Many changes also occur at the molecular level like alteration in gene expression and transcripts accumulation that lead to stress-related protein synthesis and act as a strategy of stress tolerance (Iba, 2002). Denaturation and aggregation of protein are the direct injuries of high temperature (Essemine et al., 2010) whereas indirect injuries include inhibition of protein synthesis, protein degradation, enzymes inactivation in chloroplast and mito- chondria and loss of membrane integrity (Howarth, 2005).
Therefore, heat-tolerant wheat line selection may help to figure out how this crop respond to high temperature and how heat toler- ance mechanisms can be improved in wheat (Halford, 2009). The first step towards wheat breeding program for heat stress is to identify heat stress tolerant genotypes by exploring local genotypes of wheat that are highly adapted to heats stress (Bita and Gerats, 2013). There- fore, the main objective of this review paper is to accumulate the present understanding about the effect of heat stress and heat toler- ance mechanisms in wheat which may help to identify heat tolerant wheat genotypes.
Table 1 Responses of plant to heat stress at different growth and developmental stages of wheat.
Temperature, Duration Major responses to heat stress
References 34/26 °C (day/night), 16 days Shortening of grain filling and maturity period; Drastic reduction in both fresh and dry weight, starch content and protein in grain; grain size and yield reduction
Pradhan and Prasad (2015) 35 °C, 1 h Reduction in water soluble carbohydrate content in peduncle by 26%
Talukder et al. (2014) 37/28 °C day/night leaf temperature increase; reduction of leaf chlorophyll content and maximum quantum yield of photosystem- II; reduction of individual grain weight and grain yield
Hurkman et al. (2009) 38 °C, 15 h Increase of H2O2 content
Iqbal et al. (2015) 45 °C, 2 h Reduction in length and dry mass of shoot and root; decrease in membrane stability index and chlorophyll content
Gupta et al. (2013a) 42 °C, 24 h Roots and first leaves development inhibition; increase in lipid peroxidation (LP) products and reactive oxygen species (ROS) in the developing organs
Savicka and Skute (2010) 40 °C, 2 + 5 h Photochemical efficiency (Fv/Fm) and quantum yield (F’q/F’m) of PSII inhibition
Haque et al. (2014) Source: Akter and Islam (2017); Ihsan et al. (2019).
Fig. 1. Development of heat tolerance in plants; SOD= Superoxide dismutase, CAT= Catalase, APX= Ascorbate peroxidase.
S. Sarkar, A.K.M.A. Islam, N.C.D. Barma et al.
South African Journal of Botany 138 (2021) 262277
263 2. Mechanism of heat tolerance Before knowing about the mechanisms of heat tolerance, it is very important to have a clear concept about the critical stages of wheat that can be affected by heat stress. This knowledge may help in plan- ning management strategies and breeding program that incorporate information about plant growth to avoid damage of crop against stress environment and to minimize crop yield loss. Different scales have been used to explain the critical stages of crop such as BBCH scale (Fig. 2).
A decimal code system is used by BBCH-scale which is divided into principal and secondary growth stages based on the cereal code system (Zadoks scale) developed by Zadoks (Table 2) (Zadoks et al.,
1974). The flowering stage of wheat has been found the most sensi- tive stage to heat stress (Kaushal et al., 2016). Complex interaction between the sensitivity of growth phases to the stress environment and the timing of phenological stages finally influences the grain yield (Balla et al., 2019).
3. Morphological mechanisms 3.1. Leaf senescence Senescence of leaf is a physiological process which is responsible for chlorophyll destruction and nutrients remobilization to younger and reproductive plant parts (Vijayalakshmi et al., 2010). Premature induction of leaf senescence often occurs by heat stress which there- fore causes massive yield losses through inefficient resources recy- cling (Talukder et al., 2014; Hosseini et al., 2016). Heat stress changes the structure of leaf and sometimes produces thinner leaves by increasing the leaf area (Poorter et al., 2009). The metabolisms of leaf particularly CO2 assimilation decreases during leaf senescence when catabolism is enhanced by chloroplast degradation, decrease in pho- tosynthetic capacity and deterioration of macromolecular materials (Lira et al., 2017). In many studies, it has been shown that leaf yellow- ing or leaf chlorosis is one of the earliest symptoms of premature leaf senescence which is caused by heatinduced chlorophyll degrada- tion or heat inhibited chlorophyll biosynthesis (Robson et al., 2013;
Bergkamp et al., 2018). Particularly, the term ‘stay-green,’ that means the maintenance of photosynthetic capacity and leaf chlorophyll is believed as an indicator of heat tolerance (Thomas and
Howarth, 2000; Sakuraba et al., 2014). This stay-green character has been technically used in breeding line selection by visual assessment since many years (Thomas and Ougham, 2014). Under eminent tem- peratures, stay-green genotypes should have better ability in main- taining grain filling because less assimilation of current carbon into grains is occurred by the loss of chlorophyll. It has been found that for the increment of productivity, stay-green phenotype is very effec- tive (Pinto et al., 2016). Delayed leaf senescence in wheat helps to achieve higher seed weight and grain yield (Borrell et al., 2014). Leaf senescence can be delayed by applying 3-cyclopropyl-1-enyl-propa- noic acid sodium salt (CPAS) which acts as an antagonist against eth- ylene, helps to improve the grain yield of wheat under heat stress (Huberman et al., 2014). Delayed leaf senescence development in wheat can also be accelerated through molecular marker assisted selection (Yang et al., 2017).
There are three major phases of leaf senescence- initiation, re- organization and terminal phase (Holland et al., 2016). The re-organi- zation phase of leaf senescence is characterized by major alterations in cellular metabolism which is accelerated by declining cytokinins (CK), enhancing Abscisic acid (ABA) and ROS levels (Sarwat et al.,
2013). ABA and CK are involved in controlling heat-induced senes- cence in wheat particularly plant senescence and C remobilization are enhanced by high level of ABA which accelerate grain-filling rate (Jan et al., 2019). Early genotypes having an efficient remobilization capacity of the stem carbohydrate reserves can be considered more valuable under late heat stress (Abdelrahman et al., 2020). Macronu- trient mobilization enhanced within grains from senescing leaves with the increase in ABA levels under heat and drought stress (Thomas, 2013). On the other hand, CK have a potential function in controlling source to sink reallocation (Yu et al., 2015). An inverse
Fig. 2. Critical stages of wheat according to BBCH scale (Source: Lancashire et al., 1991).
Table 2 Decimal growth stages scale proposed by Zadoks (Z0.0 to Z9.9).
Main stages Description Main stages Description Stage 0
Germination Stage 5 Heading Stage 1 Main shoot leaf production
Stage 6 Anthesis Stage 2 Tiller production Stage 7
Grain milk stage Stage 3 Main shoot node production (stem elongation)
Stage 8 Grain dough stage Stage 4 Booting Stage 9 Ripening
Source: Zadoks et al. (1974).
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South African Journal of Botany 138 (2021) 262277
264 association with photosynthetic rate and pigment content is exhib- ited by decreased levels of CK (Sami et al., 2016). Tolerant plants can expose augmented anti-oxidative defense with the translocation of nutrients from senescing to young leaves, until plants thrive under stress conditions and resume their normal growth (Have et al., 2017).
3.2. Grain filling duration and grain yield Under heat stress, one of the most critical aspects for the improve- ment of wheat is maintaining high grain yield (Aziz et al., 2018).
Wheat genotypes that may able to produce high and stable yield under heat stress can be used as a donor parent in wheat breeding program for heat tolerance (Al-Otayk, 2010). The facts those are directly involved in the decrease of wheat grain yield by heat stress are reduction in photosynthetic capacity of plant (Wahid et al., 2007), reduction of metabolic processes (Farooq et al., 2011), enhancement of oxidative damage through reactive oxidative species (ROS) pro- duction (Wang et al., 2011), reduction in the development of pollen tube, sterility of pollen (Saini et al., 2010), abortion of grain by ethyl- ene production (Hays et al., 2007) and oxidative damage chloroplast.
Crop establishment and floral fertility are adversely affected if pre- anthesis period faces heat stress (Al-Ajlouni et al., 2016).
Reproductive phase of wheat is highly sensitive to heat stress (Dwivedi et al., 2017) and in maximum wheat growing region, the grain filling period faces the highest temperature that affects the pro- cess of grain filling (Singh et al., 2011; Pradhan and Prasad, 2015).
Kernel number and weight and quality of wheat grain are found to be considerably affected by heat stress (Mohammadi et al., 2012;
Hutsch et al., 2019). Grain yield declines significantly due to the exposure of anthesis and grain filling period to heat stress (Stratonovitch and Semenov, 2015). There are also many other exper- imental evidences which show that there is a correlation between heat stress during flowering and reduction in the number and weight (Zhang et al., 2018) of grain along with significant negative effect on grain yield (Barnabas et al., 2008). Yin et al., 2009 observed a reduc- tion in the grain filling duration by 12 days, increase in grain filling rate and reduction of seed size in wheat for each 5 °C temperature increase after 20 °C. Although he didn’t find increase in grain filling rate over 30 °C temperature. Talukder et al. (2013) found 10 to 26% percent reduction in individual grain size and 1123% reduction in grain number by exposing wheat genotypes to a short term heat stress like single-day heat event (maximum 35 °C temperature) under controlled environment (CE).
Heat stress reduces the maturity period as well as the grain filling duration of wheat up to 15% (Ahamed et al., 2010). In summer season, early maturation with lesser yield loss exhibits possible involvement in heat stress tolerance (Adams et al., 2001). So, the genotypes of wheat that mature earlier and provide a minimum yield loss compar- ing to control condition can be considered as truly compatible to escape heat stress injury (Menshawy, 2007).
4. Physiological mechanisms 4.1. Canopy temperature depression (CTD)
The term CTD describes the deviation of canopy temperature from ambient temperature (Deva et al., 2020). Canopy temperature depression (CTD) can be used as a good indicator of a genotype’s fit- ness under heat stress (Urban et al., 2018). CTD plays an important role in sustaining physiological basis of grain yield of wheat after exposing to heat stress. During grain filling period, cool canopy acts as a significant physiological principle for heat stress tolerance in wheat (Munjal et al., 2003). CTD functions based on a number of envi- ronmental factors especially air temperature, relative humidity, soil water status and incident radiation (Fig. 3). CTD is best evolved at high vapor pressure deficit (VPD) conditions that is associated with warm air temperature and low relative humidity (Medina et al.,
2019). Vapor pressure deficit (VPD) is a combined function of air tem- perature and relative humidity and changes in VPD regulates the transpiration rate of the plant (Belko et al., 2013). Heat tolerant varie- ties show greater stomatal conductance and a better association between VPD and leaf cooling (Kholova et al., 2012). On the other hand, in case of combined effect by heat and drought stress- proper root growth, increase in root hydraulic conductivity, reduction in sto- matal conductance and leaf expansion are maintained by Abscisic acid (ABA) biosynthesis that increases thermotolerance of photosys- tem II (Urban et al., 2018). In response to changes in VPD, the heat tolerant wheat genotypes cool more than the heat sensitive genotype because of enhanced transpirational cooling (Deva et al., 2020). A stronger association between VPD and leaf cooling helps in maintain- ing higher leaf water content under heat stress conditions which allows a greater transpirational response to VPD and enhances the transpirational cooling (Omae et al., 2012). This is also facilitated by an increase in the density and diameter of vascular tissues like xylem vessels or tracheids that better continues the upward flow of water for enhancing transpirational cooling under heat stress (Qaderi et al.,
2019).
Assessment of CTD has allowed the breeders to explore the yield stability of wheat as it is correlated with many adaptive physiological traits (Saxena et al., 2014). In different varieties with comparatively cooler canopy, there is a positive correlation of CTD with root traits (Man et al., 2016), leaf area index (Othmani et al., 2015), stomatal conductance (Reynolds et al., 2005), water usage (Reynolds et al.,
2005), transpiration rate (Gautam et al., 2015), and grain yield (Olivares et al., 2007). Total chlorophyll content and CTD may play an important role in recognizing heat tolerant genotypes of wheat (Saxena et al., 2014). Greater CTD has been found in heat tolerant wheat genotypes as compared to sensitive genotypes which is caused by better photosynthetic enzyme activity (Wanjura et al., 1995) and greater leaf conductance (Hatfield et al., 1987). Under heat stress con- dition, it is estimated that around seven to nine percent gain in yield can be achieved by canopy temperature depression and remobiliza- tion of stem carbohydrates (Reynolds et al., 2007). So, high CTD is associated with the rise in yield (Fischer et al., 1998) and can be uti- lized as a selection criterion for the improvement of heat tolerance in wheat (Balota et al., 2007).
4.2. Photosynthesis Photosynthesis is adversely affected by high temperature in vari- ous ways (Shah and
Paulsen, 2003).
According to Hemantaranjan et al. (2014) there is a link between thermotolerance increase of photosynthetic apparatus and heat stress protection mechanism. The most unstable cell components under heat stress are thylakoid membranes and Photosystem II (PSII) (Ristic et al., 2007).
Thermal damage of PSII is caused by heat stress through affecting
ATP synthesis and photosynthetic electron transfer (Akter et al.,
2017; Jat et al., 2018). Increasing leakiness, swelling, disruption of
PSII-mediated electron transfer, physical separation of the chloro- phyll light harvesting complex II from the PSII core complex and damaged chloroplast structure (Brestic et al., 2016; Chen et al., 2017) are occurred in thylakoid membranes under high temperature (Ristic et al., 2008). This heat stress-induced injuries cause alterations of photochemical reactions in thylakoid membranes leading to a sig- nificant reduction in the ratio of variable fluorescence to maximum fluorescence (Fv / Fm) (Wahid et al., 2007). Heat stress causes oxida- tive stress in plants that leads to oxygen evolving complex (OEC) dis- sociation in PSII, which also inhibits transportation of electron from
OEC to the acceptor side of PSII (Allakhverdiev et al., 2008). Heat stress disrupts OEC of PSII in the stroma of chloroplast as well as causes dysfunction in the carbon assimilation metabolism of Calvin cycle. There are many evidences supporting that primary reduction
S. Sarkar, A.K.M.A. Islam, N.C.D. Barma et al.
South African Journal of Botany 138 (2021) 262277
265 in photosynthesis occurred by the reduced activity of Rubisco in RuBP (Ribulose-1, 5-bisphosphate) carboxylation (addition of CO2 with
RuBP) due to the failure in RCA (Rubiscoactivase) enzyme activation (Fig. 3) (Perdomo et al., 2017). RCA activates Rubisco and helps in
RuBP carboxylation which is essential for running the Calvin cycle under normal condition. High temperature stimulates the Rubisco activity inhibitor synthesis like XuBP (xylulose-1, 5-bisphosphate) that binds at the catalytic site of Rubisco and block this site. (Parry et al., 2008). Rubisco activase enzyme removes the tightly bound inhibitors from the catalytic site of Rubisco. Under heat stress, a stable RCA structure and maintenance of Rubisco activity can ensure the regular running of Calvin cycle (Wang et al., 2010;
Chen et al., 2015). During day time when the stomata closure is a lim- iting factor, it is necessary to possess thermostable RCA in order to support the metabolic flux of Calvin-Benson-Bassham cycle under heat stress (Shivhare and Mueller, 2017).
Loss of organic matter and product of photosynthesis leads to reactive oxygen species (ROS) production and oxidative damage (Fig. 4) (Mathur et al., 2014). The production and accumulation of
ROS is triggered by heat stress (Almeselmani et al., 2009). In Photo- system II, ROS produced by lipid peroxidation causes damage to D1 protein (Pospisil et al., 2017). A family of serine-type ATP-indepen- dent proteases is involved in the deterioration of Photosystem II reac- tion center protein D1 (Jarvi et al., 2015; Cheregi et al., 2016). Photo inhibition of PSII under heat stress can be mitigated by maintaining
ROS at limited level (Martins et al., 2016). Therefore, it is important to protect the plant from heat stress by the detoxification of ROS through antioxidant defense systems (Suzuki and Mittler, 2006).
Heat tolerant plants tend to synthesize various ROS scavenging and detoxification systems to create protection against the damaging effects of ROS (Apel and Hirt, 2004). Thermotolerance can be induced by maintaining enhanced membrane thermostability and low level of
ROS accumulation (Hameed et al., 2012) by improving antioxidant capacity (Chakraborty and Pradhan, 2011). Impairment in the photo- synthetic apparatus was found to be more severe in heat-sensitive cultivars comparing to heat-tolerant cultivars because of high level of
ROS and malondialdehyde (MDA) accumulation (Zou et al., 2017).
Besides antioxidant defense systems, plants use some other mechanisms to protect the photosystems such as cyclic electron flow (CEF), alternative oxidase (AOX) pathway, oxidative electron transport and mitochondrial reactions of photorespiration (Sunil et al., 2019). CEF, AOX and photorespiration activities are cru- cial among these mechanisms (Hodges et al., 2016). Photorespiration can dissolve excess ROS both directly and indirectly (Voss et al.,
2013). The photorespiration reactions can serve as direct sinks for
ATP, NADPH and reduced ferredoxin those are generated photosyn- thetically (Araujo et al., 2014). In direct way, the peroxisomal catalase scavenge H2O2 and CEF optimization, promotion of AOX pathway and
CO2 release from glycine decarboxylation for intracellular recycling are the indirect ways to protect photosystem (Ziotti et al., 2019).
Additionally, photorespiratory metabolism generates glycine as a source for glutathione which acts as a major antioxidant in plant cells (Hodges et al., 2016).
4.3. Chlorophyll content Chlorophyll content is a stay-green trait and associated with heat tolerance in wheat (Feng et al., 2014; Cao et al., 2015). Wheat biomass and yield are also regulated by chlorophyll content under heat stress (Tattaris et al., 2016). High chlorophyll content can be utilized as a selection criterion for heat stress tolerance in wheat (Ramya et al.,
2015; Munjal and Dhanda, 2016). High chlorophyll content under heat stress conveys low degree of photo inhibition, as a result it is considered as a desirable trait for heat tolerance in wheat (Talebi, 2011; Choudhary et al., 2020). Chlorophyll content can be involved in the mechanism of heat tolerance by being associated with transpiration efficiency (Reynolds and Trethowan, 2007). At high light intensity and high temperature when water stress is absent, increased stomatal conductance induces the transpiration rate as well as light absorption by chlorophyll in order to keep the transpirational cooling and photosynthetic activity stable respec- tively (Morales et al., 2020). A significant positive relationship has been found between leaf chlorophyll content and transpiration effi- ciency in heat tolerant genotypes (Sheshshayee et al., 2006). Yield is associated with photosynthesis rate and leaf chlorophyll content dur- ing grain filling period (Reynolds and Trethowan, 2007). The loss of chlorophyll in leaves occurs due to rapid breakdown of chlorophyll under heat stress (Jespersen et al., 2016). Breakdown of chlorophyll occurs when photosynthetic mechanisms undergo complete destruc- tion under heat stress. Declining in chlorophyll content causes a
Fig. 3. Factors those affect canopy temperature depression under heat stress (Source: Reynolds et al., 2001b).
S. Sarkar, A.K.M.A. Islam, N.C.D. Barma et al.
South African Journal of Botany 138 (2021) 262277
266 typical symptom in wheat called chlorosis (Rossi et al., 2017). Numer- ous enzymes that involve in the chlorophyll biosynthesis mechanism are degraded under high-temperature resulting the inhibition of chlorophyll biosynthesis (Reda and Mandoura, 2011).
High temperature firstly affects plastid particularly chloroplast that causes the impairment and reduction of chlorophyll biosynthesis (Dutta et al., 2009; Li et al., 2010; Reda and Mandoura, 2011). It has been shown in previous studies that chloroplast plays a significant role in the activation of signaling of the cellular stimuli under heat stress (Yuan et al., 2015). Chloroplasts helps to induce the expression of nuclear heat-response genes. Heat stress response in the nuclear is required translation of chloroplast protein to stimulate retrograde signaling (Yang and Guo, 2014). Retrograde signaling can be defined as a communication pathway where the nuclear transcriptional activ- ities are regulated in part by signals that are derived from plastids and mitochondria. According to previous studies, in retrograde sig- naling- two categories can be largely classified including develop- mental control of organelle biogenesis, and operational control to acclimate to environmental stresses (Sun and Guo, 2016). Chloro- plasts act as a specialized sensor of intra- and extracellular stimuli and combines a variety of intracellular signals and pathways for sus- taining homeostasis both at cellular and organismal levels (Pogson et al., 2008). A thorough studies aiming on the initiation of transcriptional changes in the nucleus and signaling cascades in the chloroplast may help to understand the chloroplast-nuclear signaling as a response to environmental stimuli (Schmidt et al., 2019). Various genes and proteins are stimulated and regulated to help and protect chloroplast for normal functioning and improving heat tolerance of plants (Hu et al., 2020).
4.4. Photoassimilate translocation The transport and transfer processes of plant are greatly affected by the symplastic and apoplastic translocation of assimilate under high temperatures (Taiz and Zeiger, 2006). Three major elements of the plant system namely source (flag leaf blade), sink (spike), and transport pathway (peduncle) were examined to clarify about the agents responsible for reducing grain filling under high temperatures in wheat (Thakur et al., 2010). Around 90 to 95% of carbon needed for grain filling is achieved from current carbon assimilation under ideal conditions (Kobata et al., 1992). However under heat stress, changes were found in the pre-anthesis stored reserves and current assimila- tion contribution (Wang et al., 2011). Heat stress reduces the translo- cation of assimilates from the photosynthetic source provoking the remobilization of variant source like stem reserves for grain filling (Aslam et al., 2013). Under heat stress, the need of stem reserves is highly increased from the range of 6 to 100% based on the heat- incited decrement in photosynthesis (Blum, 1998). An effective heat tolerance mechanism in wheat is enhancing the mobilization of stem reserves (Bala and Sikder, 2017). Water soluble carbohydrates (WSC) reserves are reduced in wheat stem and remobilization of these car- bohydrates plays a significant role in improving grain yield against heat stress (Gupta et al., 2011). During wheat grain filling WSC can be a major source of carbon as both the photosynthesis and respiration are reduced by heat stress (Wang et al., 2012). When the temperature rises above 30 °C, the translocation of assimilate from flag leaf to grain is reduced remarkably whereas there is no impact of tempera- ture (1 to 50 °C) on assimilates translocation from the stem. This phe- nomenon concludes that, although the rate of the transportation of
Fig. 4. Photosynthetic response in wheat under heat stress (Source: Wang et al., 2018; Salvucci and Crafts, 2004).
S. Sarkar, A.K.M.A. Islam, N.C.D. Barma et al.
South African Journal of Botany 138 (2021) 262277
267 assimilate from vegetative parts to grain in wheat is reduced by heat stress, the impact on assimilate translocation by heat stress is indirect (Plaut et al., 2004). Therefore, it can be suggested that leaves, stem or other plant parts reserves can be used as an efficient contrivance by increasing their solidarity to improve grain filling and yield in wheat under heat stress.
4.5. Membrane thermostability Membrane thermostability (MTS) is a significant physiological mechanism for heat tolerance which helps plants to adapt in high ambient temperatures (Barma et al., 2011). The tertiary and quater- nary structures of membrane proteins are altered by heat stress. This type of alteration enhances the loss of electrolytes, as a result decreasing membrane thermostability. The kinetic energy is acceler- ated by heat stress and it makes the molecules movable along mem- branes by detaching the chemical bonds into molecules of biological membranes. Thus, the lipid bilayers of the membranes become more fluid due to proteins denaturation or unsaturated fatty acids increase (Savchenko et al., 2002; Higashi and Saito, 2019). The efflux of released electrolytes into surrounding solution from the affected cells or leaf tissue can be used to measure cell membrane damage caused by heat stress (AHN and Zimmerman, 2006; Choudhary et al., 2020).
The membrane thermostability (MTS) can be evaluated using this for- mula: MTS ¼ ð1 T1=T2Þ 100, here T1 is reading of conductivity after heat treatment and T2 is reading of conductivity after autoclav- ing (Ibrahim and Quick, 2001).
The increase in solute leakage is suggested as an indicator of decrease in cell membrane thermostability that can be used as an indirect measure of heat-stress tolerance in wheat (Ram et al., 2014;
Bala and Sikder, 2017). Membrane systems which remain functional during heat stress lead to the adaptation of plants to high tempera- ture (Blum, 1988). Thus, the tolerance to heat stress is determined by the efficiency of plant in maintaining the integrity and function of membrane (Almeselmani et al., 2011). After exposing plant to pre- hardening treatment, it is recommended to assess cell membrane sta- bility for estimating cellular thermotolerance of plants (Ibrahim and
Quick, 2001). If grain filling occurred under stress conditions, then the wheat lines with high membrane thermostability attend better yield as compared to the lines with low membrane thermal stability (Khatoon et al., 2016). In wheat, cell membrane thermostability pro- vides as a fair index of genetic variation and shows a liable relation- ship to the performance of plant under heat stress and may consider as an important selection criterion for heat tolerance (Behle et al.,
1993).
5. Biochemical mechanisms 5.1. Starch synthesis In wheat, 5575% of total grain dry weight is occupied by a major component which is starch (Gillies et al., 2012). During grain filling period, two types (A and B type) of starch granules are derived in wheat grain (Zheng et al., 2014). Wheat starch contains amylase and amylopectin which are being synthesized in the amyloplast (Li et al.,
2018). Starch is more vulnerable to heat stress comparing to protein (Farooq et al., 2011) because the amylopectin of starch readily decreases under high temperature which leads to a reduction in starch content (Liu et al., 2011). Starch synthesis is remarkably dis- turbed by reduction in the activities of sucrose phosphate synthase (Chaitanya et al., 2001), ADP glucose pyrophosphorylase and inver- tase (Vu et al., 2001). A study has shown that the impact of heat stress on the starch quality of bread wheat could be extreme (Labuschagne et al., 2009). The starch content of wheat grain reduces at a critical level under heat stress that results into the reduction of kernel weight and diameter (Poudel and Poudel, 2020). Heat stress significantly affects the starch content during grain development of wheat resulting in poor grain quality, grain size and yield (Chinnusamy and Khanna-Chopra, 2003). The duration needed for starch biosynthesis and grain filling is reduced if the temperatures increase over 1822 °C (Spiertz et al., 2006). There are three enzymes that limit starch biosynthesis in wheat namely soluble starch syn- thase (SSS), sucrose synthase and granule bound starch synthase (Hawker and Jenner, 1993). Starch synthesis rate is determined by sucrose synthase (Hawker and Jenner, 1993), on the other hand the amylose biosynthesis is controlled by granule-bound starch synthase (Morell et al., 2001). Starch synthesis is regulated by SSS (soluble starch synthase) which is mostly sensitive to heat stress (Keeling et al., 1993). SSS activity is deteriorated in wheat by heat stress which causes declining in grain growth and starch accumula- tion (Prakash et al., 2004). Recent observations suggest that the solu- ble starch synthase enzyme can be an important indicator for the improvement of heat stress tolerance as high temperature tolerance for grain growth in wheat is closely associated with the catalytic effi- ciency of this enzyme (Tian et al., 2018).
5.2. Antioxidant response It has been indicated in several studies that under heat stress, damage to membrane is increased and level of antioxidants is decreased in wheat at the stages of seedling (Yogita et al., 2015), anthesis (Narayanan et al., 2015) and grain filling period (Balla et al.,
2013). Plants are able to survive under heat stress if they can be pro- tected from heat-induced oxidative stress. ROS singlet oxygen, super- oxide radicals and hydrogen peroxide reactions are among usual events in cell under heat stress. To avoid cell damage by these reac- tions, plants initiate antioxidants defense system (Suzuki et al.,
2014). Different types of antioxidants from variable pathways are accumulated in plants under heat stress (Bokszczanin and Fragkoste- fanakis, 2013). There are mainly two types of defense system of anti- oxidants found in wheat enzymatic and non-enzymatic (Sattar et al.,
2020). Catalase (CAT), ascorbate peroxidase (APX), monodehydroas- corbate reductase (MDHAR), dehydroascorbate reductase (DHAR), glutathione-S-transferase (GST), superoxide dismutase (SOD), guaia- col peroxidase (GPX) and glutathione reductase (GR) are the enzy- matic antioxidant system (Noctor and
Foyer, 1998) whereas ascorbate (AsA), glutathione (GHS) and tocopherols are non-enzy- matic antioxidant systems. SOD is one of the major antioxidants that helps to convert superoxide into H2O2. On the other hand, detoxifica- tion of ROS is governed by APX, GPX and CAT (Buttar et al., 2020). To detoxify H2O2, APX requires AsA and reduced glutathione (GSH) that are produced via AsA-glutathione cycle to convert H2O2 into H2O with the help of AsA oxidation into monodehydroascorbate (MDHA) which again dismutate to dehydroascorbate (DHA) (Fig.
5) (Asthir, 2015). Catalase, ascorbate peroxidase, and superoxide dis- mutase activities extenuated at 50 °C but before reaching at this temperature, these enzymes activities are initially increased (Chakrabortty and Pradhan, 2011) whereas peroxidase (POX) and glutathione reductase activities are decreased at a temperatures range from 20 to 50 °C. In tolerant wheat varieties total antioxi- dant activity was highest at 3540 °C and in the case of suscepti- ble varieties highest antioxidant activities was shown at 30 °C (Chakrabortty and Pradhan, 2011). Activities of these enzymes are also varied with the growth stages and growing season of wheat (Chakraborty and Pradhan, 2011). Enzymatic antioxidants were considerably increased at the reproductive phase of heat tolerant genotypes of wheat when subjected to heat stress (Balla et al., 2009). Catalase and superoxide dismutase activities have the competence to attain thermotolerance in wheat (Almeselmani et al., 2009) as well as a strong correlation with heat stress at the reproductive phase (Zhao et al., 2007). Heat stress tolerance wheat varieties demonstrate enhanced GST, APX
S. Sarkar, A.K.M.A. Islam, N.C.D. Barma et al.
South African Journal of Botany 138 (2021) 262277
268 and CAT activities and protection against heat stress injuries (Ahmad and Prasad, 2011).
6. Molecular mechanism 6.1. Protein synthesis Plant develops some defense mechanisms under heat stress such as expression of particular genes that only express under stress con- dition (Feder, 2006). These genes may be either Heat-Shock Proteins (HSPs) or Stress-Induced Proteins or Stress Proteins (Lindquist and
Craig, 1988). Heat-Shock Proteins are a group of protein synthesized in wheat coleoptiles when exposed to heat stress (Blumenthal et al.,
1990). To understand the role of HSPs in adaptation under heat stress, membranes associations must be considered because under heat stress about two third of the chloroplast HSPs are transferred to thy- lakoid membranes (Bernfur et al., 2017). In general, HSPs act as molecular chaperones and play a vital role in regulating the accumu- lation, folding, localization and degradation of proteins in plants (Gupta et al., 2010). At vegetative stage of wheat, proteins in ER (endoplasmic reticulum) and cytosol found to become unfolded via
ROS (reactive oxygen species) regulatory mechanisms under heat stress (Sun and Guo, 2016; Kataoka et al., 2017). However, HSPs as chaperones inhibit other proteins from aggregating irreversibly by taking part in refolding of those proteins (Morrow and Tanguay, 2012) which hinders apoptosis or cell death (Fig. 6) (Altenbach et al., 2003).
Under heat stress, heat shock genes are activated in wheat plant dur- ing grain filling period, generating more HSPs in the mature grains (Blumenthal et al., al.,1991) and producing weaker dough (Zhang et al., 2018). In many studies it has been suggested that plants develop thermotolerance by overexpression of HSPs (Grover et al.,
2013). Various types of HSPs are developed in different tissues of wheat plant based on type and duration of heat stress (Xu et al.,
2011). HSPs can be divided into five classes: HSP100, HSP90, HSP70,
HSP60 and HSP20 (Swindell et al., 2007). An increase in ABA (abscisic acid) content in the embryo of wheat is accompanied with HSPs development during the period of grain filling and maturation (Xue et al., 2014).
Heat inducible genes regulation is contributed by heat shock fac- tors (HSFs) as a process of acclimation in heat stress (Yabuta, 2016).
The chloroplast protein synthesis elongation factor, EF-Tu (elongation factor thermo unstable) may avail to heat tolerance in wheat as it acts as a molecular chaperone and has the ability to protect chloroplast protein from thermal aggregation (Ristic et al., 2007). In a study by
Djukic et al., 2019, 25% higher accumulation of chloroplast EF-Tu found under high temperature (38 °C) comparing to accumulation at
Fig. 5. Antioxidants defense system in wheat under heat stress (Source: Wang et al., 2018); Superoxide dismutase (SOD), catalase (CAT), guaiacol peroxidase (GPX), ascorbate per- oxidase (APX), ascorbate (AsA), monodehydroascorbate reductase (MDHAR), monodehydroascorbate (MDHA), dehydroascorbate reductase (DHAR), dehydroascorbate (DHA), gluta- thione reductase (GR), glutathione (GSH), glutathione disulfide (GSSG). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
S. Sarkar, A.K.M.A. Islam, N.C.D. Barma et al.
South African Journal of Botany 138 (2021) 262277
269 a moderate temperature (23 °C) in a winter wheat cultivar named
Zvezdana and this cultivar was better able to decrease protein aggregation under heat stress comparing to other cultivars. The accumulation of EF-Tu in mature plants induces by high tempera- ture and the plants where EF-Tu are highly accumulated show more resistance to heat stress indicating the fact that EF-Tu may play a vital role in adapting plants to heat stress (Ristic et al.,
2008).
6.2. Omics approaches The large-scale studies of cellular processes and their genetic con- trol over the entire genetic, structural and functional components are called omics. Genomics, transcriptomics, metabolomics and proteo- mics are the major components of omics (Fig. 7). Several heat stress tolerance genes containing genomic DNA is the initial site of all molecular approaches associated with heat stress tolerance in wheat plant (Deshmukh et al., 2014). Studies of genomic screen and genome expression have been used to identify the role of genes in heat tolerance of wheat (Yeh et al., 2012). Transcriptomes (Transcriptom- ics) are produced from mRNAs (transcript products) of heat tolerance genes and proteomes (proteomics) are produced when mRNAs of such genes are translated into functional proteins (responsible for heat stress tolerance). Plants reveal some post-transcriptional gene expression by small non-protein coding RNAs (also called micro- RNAs). Study of microRNAs and micromics helps in better under- standing of the heat tolerance mechanisms in wheat (Chinnusamy et al., 2007).
Metabolomics are another omics approaches that can be uti- lized for phenotyping of genetically modified plants and consider- able similarity testing, gene function determination and observing responses to biotic and abiotic stresses (Abdelrahman et al.,
2020). Metabolomics studies can provide an indication of alter- ation in plant metabolites under heat stress (Roessner and
Bowne, 2009). The ability of wheat grains to accumulate available assimilates that is related to metabolic activities of sink organs, plays an important role in controlling wheat grain yields under heat stress (Girousse et al., 2018; Hutsch et al., 2019). Under heat
Fig. 6. Heat shock protein synthesis in wheat plant under heat stress (Source: Whitley et al., 1999).
S. Sarkar, A.K.M.A. Islam, N.C.D. Barma et al.
South African Journal of Botany 138 (2021) 262277
270 stress, primary metabolites such as carbohydrates accumulation increases the protein stability and firmness of cell membrane bilayer structure (Sairam and Tyagi, 2004). Thus, approaches that accelerate the increase in soluble carbohydrates and the capacity of fatty acids synthesis that protect cell from damage can be sug- gested as a efficient protective mechanism against heat stress (Sardans et al., 2020).
7. Breeding for heat tolerance in wheat 7.1. Conventional breeding
In general, breeding programs are conducted within the region similar to where the crop is being grown. Therefore, selection of breeding lines for heat tolerance should be done under hot condi- tions (Mickelbart et al., 2015). In order to identifying superior genetic stock for progress in heat tolerance, it is a common approach to evaluate wheat genotypes for yield stability under heat stress throughout different locations (Mishra et al., 2014).
Screening of genetic resources must be practiced to identify donor genotypes for heat tolerance. Recurrent selection has effec- tively exercised to improve grain filling rate and grain size in
BC1F6 plants of wheat under heat stress using ancestor Triricum tauschii as a donor parent (Gororo et al., 2002). In southern Aus- tralia, selected F2-derivedlines of backcross derivatives obtained from synthetic hexaploid wheats (T. turgidum / T. tauschii) were evaluated under heat stress condition. In F6 generation, re-selec- tion was carried out and further evaluation was done for high grain yield, yield components and grain growth characters under heat stress and T. tauschii found with exceptional capacity to improve wheat yield (Gororo et al., 2002).
7.2. Advanced breeding Marker-assisted recurrent selection and genome-wide selec- tion are among advanced breeding strategies that have been used to develop heat stress tolerant varieties. Adaptation to heat stress can be obtained through inter-specific genome diversity which is used as a source of heat tolerance genes. As heat tolerance is a polygenically controlled trait, identification of quantitative trait loci (QTL) helps to achieve the understanding of thermo-tolerance in wheat (Wahid et al., 2007). Different Quantitative trait loci (QTL) has been identified for different traits of wheat associated with drought or heat stress; combined dry and hot conditions (Table 3).
Low-density simple sequence repeat (SSR) markers and/or ampli- fied fragment length polymorphism (AFLP) markers have been used in mapping Most of these reported QTL (Lu et al., 2020). GWAS (Genome-wide association studies), QTL mapping and GS (Genomic selection) have provided the basis for the development of different molecular markers like SNP (single nucleotide polymorphism), SSR (simple sequence repeat), NGS (next generation sequencing) etc. (Sonah et al., 2012; Cabral et al., 2018). QTL or GWAS can be com- bined with GS to maximize the breeding values which represent an estimate of the genomic merit correlated with all minor or major effects throughout the entire genome (Bassi et al., 2016). Genome wide analysis has been proved as a valuable method to identify heat stress responsive genes with the complexity of the underlying heat tolerance mechanisms (Wang et al., 2015). Recent advances in wheat gene transformation technology and transgenic study has accelerated the evolution in functional analysis of heat-responsive genes in wheat (Clavijo et al., 2017). The functions of some genes has been characterized by overexpression of these genes involved in sensing and responding to heat stress in wheat (Zang et al., 2017) (Table 4).
Beside these, a new breeding method named ‘speed breeding’ has been developed (Watson et al., 2018) to shorten the generation time which can be utilized to speed up the breeding program for heat tol- erance in wheat. This speed breeding method can be used to get up to six generations of both bread wheat (Triticum aestivum) and durum wheat (Triticum durum) every year (Watson et al., 2018). In recent times, genome editing tools and resources like CRISPR-Cas9,
TILLING etc. (Liang et al., 2017) are being used to improve wheat for heat tolerance. In spite of having such advances, the slow generation time may continue to impose a barrier toward developing heat toler- ant wheat variety (Watson et al., 2018). Therefore, combination of these advance tools with speed breeding may provide the scientists an effective inducement to perform improvement research for heat tolerance in wheat.
Fig. 7. Omics approaches for heat tolerance in wheat (Source: Hasanuzzaman et al., 2013).
S. Sarkar, A.K.M.A. Islam, N.C.D. Barma et al.
South African Journal of Botany 138 (2021) 262277
271 8. Conclusion Heat stress is one of the major concerns for wheat production in the world. To develop thermotolerant and high yielding wheat varieties, we first should systematically understand different metabolic and developmental mechanisms of plant associated with heat stress. This review paper briefly explains different aspects of heat stress and various morpho-physiological, bio- chemical and molecular basis of heat tolerance which is required for the improvement of wheat yield under the upcoming warmer environment. It is well established that molecular study may confirm increasing economic crop yield, but full potential yield expression of wheat under heat stress must be estimated at field level. Different agronomic options along with biochemical and molecular approaches required to combine for exploring the actual effect of heat stress at field level. Finally, collaborative efforts from plant physiologist, molecular biologist and breeder would contribute to the success of developing heat tolerant wheat varieties.
Declaration of Competing Interest The author(s) declare(s) that there is no conflict of interest regard- ing the publication of this paper.
Consent for publication All co-authors has consent for submission of manuscript.
Acknowledgments The author would like to acknowledge their gratitude towards
Bangabandhu Sheikh Mujibur Rahman Agricultural University authority for their support.
Table 3 QTL found in wheat associated with drought or heat stress; combined dry and hot conditions.
Trait Chromosome References Heat stress Grain yield
1A, 1BL, 1D, 2BS, 3A, 3BS, 3BL, 3D, 4A, 4B, 4DL, 5A, 5B, 6A, 6B, 6D,
7AS, 7AL, 7BS, 7BL Merchuk-Ovnat et al. (2016); Ogbonnaya et al. (2017)
Rate of senescence 2A, 6A, 6B Vijayalakshmi et al. (2010)
Thousand grain weight 1A, 2A, 2B, 2D, 3A, 3BS, 3D, 4A, 4B, 4D, 5A, 5B, 5D, 6A, 6B, 6D, 7A, 7D
Tahmasebi et al. (2016) Days to maturity 1B, 1D, 2A, 2B, 3B, 4D, 5A, 5B, 5D, 6A, 6B, 6D, 7A, 7B, 7DS
Ogbonnaya et al. (2017) Canopy temperature depression
7BL Paliwal et al. (2012) Chlorophyll content 1A, 1B, 1D, 2B, 3A, 3BS, 4A, 4D, 5A, 5B, 6A, 6D, 7A, 7B, 7D
Tahmasebi et al. (2016) Fv/Fm chlorophyll fluorescence
7A Vijayalakshmi et al. (2010) Grain filling duration
1B, 1D, 2A, 2B, 2D, 3BS, 5A, 6A, 6B, 6D Shirdelmoghanloo et al. (2016); Ogbonnaya et al. (2017)
Number of grains 1A, 2A, 3B, 4A, 5B Pinto et al. (2010)
Drought stress Grain yield 2D, 3D, 3DL, 4AL, 4BS, 4DL, 5A, 5B, 5DL, 6B, 6D, 7AL, 7BL, 7D
Kadam et al. (2012); Tahmasebi et al. (2016) Thousand grain weight
1B, 1D, 2A, 2B, 3A, 3D, 4A, 4D, 5A, 6A, 6D, 7A, 7B
Xu et al. (2017) Flag leaf rolling 4B, 5A Tahmasebi et al. (2016)
Root length 2D, 4B, 5D, 6B Kadam et al. (2012) Stomatal conductance
5A Xu et al. (2017) Chlorophyll content 1B, 2B, 5B, 7A, 7B
Tahmasebi et al. (2016); Xu et al. (2017) Transpiration rate
3Al, 4BL, 6D Parent et al. (2015); Xu et al. (2017)
Water use efficiency 2AL, 4D Parent et al. (2015); Xu et al. (2017)
Combined dry and hot conditions Grain yield 1AL, 1B, 1D, 2A, 2BL, 3A, 3B, 4AL, 4B, 5A, 6A, 6B, 7A, 7B, 7D
Merchuk-Ovnat et al. (2016); Tahmasebi et al. (2016)
Thousand grain weight 1D, 2B, 3A, 3B, 4A, 6A, 7A, 7B, 7D
Bennett et al. (2012); Tahmasebi et al. (2016) Biomass
2BS, 4AL, 4B, 5A, 7AS Tahmasebi et al. (2016) Canopy temperature depression
1A, 2A, 2B, 3A, 3B, 4A, 4B, 5A, 5B, 6A, 6B, 7A, 7B
Diab et al. (2008) Chlorophyll content 1A, 1B, 3A, 4A, 4B, 4D, 5A, 5B, 6A, 6B, 7A
Bennett et al. (2012) Grain filling duration 4AL Kirigwi et al. (2007)
Days to maturity 1A, 1D,5A, 7B, 7D Tahmasebi et al. (2016)
Stomatal density 4AS, 5AS, 7AL Shahinnia et al. (2016)
Source: Farooq et al., 2011; Tricker et al. (2018).
Table 4 Genes identified to function in heat tolerance through transgenic studies.
Gene Trans- host Source Function References TaHsfA6f
T. aestivum T. aestivum Transgenic plants overexpressing TaHsfA6f showed improved thermotolerance
Xue et al. (2015) TaHsfC2a T. aestivum T. aestivum
Improved thermotolerance Hu et al. (2018) TaFER-5B
T. aestivum T. aestivum Transgenic plants exhibited enhanced thermotolerance
Zang et al. (2017) TaGASR1 T. aestivum T. aestivum
Enhanced tolerance to oxidative stress Zhang et al. (2017)
Sucrose transporter gene HvSUT1 T. aestivum Hordeum vulgare
Sucrose transport enhancement and a superior performance for many yield- related traits
Weichert et al. (2017) EF-Tu T. aestivum Zea mays Improved thermotolerance
Fu et al. (2008) TamiR159 Oryza sativa T. aestivum
TamiR159 overexpressing plants were more sensitive to heat stress relative to the wild type
Wang et al. (2012) TaMBF1c Oryza sativa T. aestivum
Overexpress TaMBF1c showed higher thermotolerance than control plants at both seedling and reproductive stages
Qin et al. (2015) Source: Ni et al. (2018); Janni et al. (2020).
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South African Journal of Botany 138 (2021) 262277
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