Ecophysiological Responses of Rice (Oryza sativa L.) to Drought and High Temperature

Abstract

Global rice crop production is being threatened by a frequent rise in high temperatures and drought. Drought and heat stresses adversely affect the morphological, physiological, and biochemical characteristics of rice, resulting in reduced crop productivity. Heat and drought stresses entail physiological changes in rice plants, such as stomata closure, reduced photosynthesis, loss of turgor adjustment, and reduction in crop productivity. These stresses also cause metabolic changes by increasing the activities of antioxidative enzymes, phytohormones, abscisic acid, reactive oxygen species, and reactive stress metabolites. Among the different growth stages of rice, the reproductive stage is the most sensitive stage to high temperature and drought, resulting in low seed setting and grain yield. Genetic improvement and development of drought and heat-stress-tolerant rice varieties increase seed setting and enhance yield production even under stress conditions. Because of the multigenic nature of traits, the development of drought and high-temperature-tolerant varieties through genetic improvement is the best approach. Here, we summarized the effects of heat and drought stresses on the physiological traits of rice. We focused on different approaches to managing high-temperature and drought stresses, such as an adjustment in cultural practices, genetic improvement through molecular breeding, and the development of transgenics and chemical spray from an agricultural practice perspective.

1. Introduction

Rice crop production is severely affected by drought and high temperatures. Moreover, the impact of the environment on physiological traits plays a crucial role in the overall development of the crop plant [1]. The ecological factors are affected by climate change, which is expected to have increasingly negative effects in the years to come [2]. In general, plants exhibit broader physiological and ecophysiological responses under sub-optimal environmental conditions. These conditions significantly affect functional diversity, growth rates, population dynamics, and productivity [3]. Various abiotic stresses, such as heat, drought, salinity, water logging, phytotoxicity, inadequate minerals supply, and others, directly affect yield and its contributing traits. However, plants attempt to adapt to environmental variations with internal mechanisms that confer resistance against these stresses. Therefore, to enhance the capabilities of plants to withstand abiotic stresses in challenging environments, breeding programs should be aimed at developing stress-tolerant/resistant crop varieties [3]. Among the various abiotic stresses, increasing drought and high temperatures are the primary factors adversely affecting agricultural productivity [4,5,6]. Globally, the demand for food is rising along with population growth [7,8,9]. This challenge can be addressed by increasing crop production, reducing postharvest losses, and efficiently utilizing natural resources, such as minimizing soil degradation, enhancing water use efficiency, and maintaining the agroecosystem [9,10,11].

The geographical distribution of cultivated plant species is determined by environmental stresses, particularly temperature variations, drought, and other environmental factors. The accumulation of metabolites, such as glycine betaine and proline, changes in carbohydrate metabolism, accumulation of reactive oxygen species (ROS), alterations in stomatal conductivity, and reduction in photosynthesis are typical indicators of physiological responses of plants due to environmental stresses [12,13]. Under high temperatures, plants exhibit acclimatization characteristics due to the increased ability to withstand physicochemical changes occurring within cells. Under high temperatures, nitrogenous compounds like glycine betaine and proline, as well as osmolytes such as soluble sugars and alcohols, are generated in plant cells [12,14]. The production of osmolytes triggers the induction of stress-related dehydrins, proteins, and transcription factors (TFs), such as abscisic acid binding factors (ABFs) or abscisic acid-responsive elements binding factors (AREBs), which contribute directly to stress tolerance through the abscisic acid (ABA)-dependent pathway [12,14]. These stress-induced proteins help to remove ROS, stabilize membrane phospholipids, and maintain ionic homeostasis. However, low temperatures elicit complex responses involving the regulation of metabolic and morphological adaptive pathways, as well as the control of stress damage repair [12,15].

Rice, being the staple cereal crop for about half of the world’s population, is mainly cultivated in tropical and sub-tropical Asian countries. It is grown in 118 countries, covering an area of 167 million hectares, with an annual grain production of 782 million tons [16]. The world population is increasing at a fast pace and is expected to exceed 9 billion by 2050. To feed the ever-increasing population, rice production must be increased to cater to their need [17]. Rice is grown from below the mean sea level (msl) to 3000 m above the msl, and its productivity faces challenges due to extreme weather conditions. Rice is globally cultivated in lowland and upland conditions, with approximately 57% of the total area being irrigated lowland, contributing to more than 75% of the world’s rice production [18]. The rice crop undergoes various stages, including seed germination, development of plumule and radicals, root growth, stem growth, leaf development, tillering, booting, heading, flowering, fertilization, milky stage, dough stage, and ripening of the seed. Environmental changes greatly influence these phases, leading to reduced rice productivity and grain quality [19]. Although ecophysiological mechanisms of abiotic stress resistance in rice crops have been well studied, further research is needed to understand the ecophysiology of plant phenotypic flexibility and the involvement of assimilates from source to sink in response to abiotic stress. Moreover, the integration of high throughput molecular/genomic resources with ecophysiological studies may be needed to understand the interaction between rice genotypes and various environmental variations [2]. This study could lead to the development of climate-resilient rice varieties capable of withstanding stress conditions.

Presently, heat and drought stresses are the major issues as the Earth’s ecosystem is rapidly changing. Global warming has increased since the 19th century, resulting in a temperature rise of 0.9 °C [20]. In the 21st century, it is projected that temperatures may further increase by 1.5 to 4.5 °C [21] and possibly even more in the future. The increase in the global temperature changes the growth patterns and geographical distribution of crops. Under severe environmental conditions, each crop species has its own ecophysiological processes for germination, vegetative growth, and reproduction. While drought and high-temperature stress negatively affect the vegetative and reproductive phases of rice, the plant exhibits the ability to undergo morphological, physiological, and biochemical changes to resist these stresses (Figure 1). For optimal plant growth, an ideal temperature and moisture level are required, and deviations from these conditions result in significant crop yield losses [22]. Drought and high-temperature stress beyond a certain threshold irreversibly impair the physiological and morphological growth of crop plants [23]. Globally, an inverse relationship exists between crop productivity, particularly in cereal crops, and high-temperature and drought stresses [24].

Rice production is impeded by various biotic and abiotic stresses, and among the abiotic stresses, high temperature and drought are the main yield-reducing stresses [25]. Drought and high temperatures are closely correlated [26], with extreme heat exacerbating drought stress by increasing plant transpiration through stomata opening and soil evaporation [27]. The combined effect of heat and drought stresses can inflict damage on rice plants at different crop growth stages, including germination, seedling, vegetative, reproductive, and grain maturation. The stresses caused by temperature fluctuations affect seed germination, increase the seedling period, impede development and photosynthetic capacity, induce leaf chlorosis, and reduce plant height. The most sensitive and important stage of the rice crop is the reproductive stage, and stress during this stage leads to a decline in crop yield and productivity [9].

Each plant responds quickly to environmental changes through stress-responsive genes as an active and complex signaling system influences gene expression [9,28,29,30]. The response of plants’ response to high-temperature and drought stresses include cell damage, osmotic adjustment, inhibition of photosynthesis, changes in gene expression, induction of repair systems and chaperones, and metabolic alterations [31]. Plants under induced heat and drought stresses produce two types of proteins. These regulate gene expression and signal transduction pathways, such as transcriptional factors (TFs) and those that protect cells against stress, including chaperones, late embryogenesis abundant (LEA) proteins, detoxification enzymes, and antifreeze proteins [30].

Drought and high temperatures are the main factors affecting plant growth [32]. The incidence of high-temperature and drought stresses have a significant adverse effect on seed germination, tillering, reproduction, grain yield, and quality characteristics of rice crops. In the coming years, reduced precipitation and rising global temperatures will further intensify the frequency and severity of these stresses, thereby reducing grain yield and exacerbating challenges in rice crop production [33]. Drought and high-temperature stresses are very complex and not fully understood [34]. Moreover, the combined impact of these stresses has more adverse and severe effects on rice grain production [35]. Here, we summarized the ecophysiological effects of high-temperature and drought stresses on rice crops with a particular emphasis on seed germination, tillering, and vegetative and reproductive stages, and explore how these challenges can be managed through cultural practices and the development of stress-tolerant rice varieties by using advanced high throughput phenotyping (HTP) and high throughput genotyping (HTG) techniques.

2. High-Temperature Stress

Among various abiotic stresses, high temperatures pose a significant threat to world food production [36]. Although rice is an important crop globally, it is not naturally tolerant to heat [37,38]. The rice crop is susceptible to climate change, and its yield fluctuates under different heat stresses [39,40]. Global climate change is underway, and it is projected that the Earth’s temperature will increase by 4.5 °C during the 21st century [41]. Studies have shown that rice production decreases by 2.6% with every 1 °C rise in temperature [42]. Optimal rice production occurs within a temperature range of 32–36 °C, and the grain yield decreases beyond this threshold [43]. While heat stress affects every growth stage of rice, the flowering stage is particularly sensitive, leading to reduced yields [17]. Heat stress during flowering results in poor grain filling, pollen sterility, compromised seed setting, and reduced grain weight accumulation [44]. The threshold temperatures for rice at the flowering and anthesis stages are 35 °C and 33.7 °C, respectively [39]. Heat stress not only reduces rice yield but also has detrimental effects on grain quality, especially for basmati rice varieties [45].

The intensity, timing, and duration of exposure to heat stress impact different critical growth phases of the rice plant [46]. Yield losses in rice are attributed to spikelet sterility, pollen sterility, impaired pollen germination on stigma, anther dehiscence, and limited pollen tube extension within the carpel under heat stress [21,47]. It is anticipated that high-temperature stress may lead to more than a 41% yield reduction in rice by the end of this century [48]. Various growth stages of rice, including vegetative, flowering, and grain filling stages, suffer from heat stress, resulting in grain yield losses. The seedling stage of rice is highly sensitive, with a critical high temperature of 35 °C, and further temperature increases can lead to plant death [48,49]. Heat stress induces the accumulation of ROS in cells, leading to lipid peroxidation and membrane instability, ultimately resulting in crop losses [50].

Environmental stresses, particularly heat stress, have been shown to influence rice grain quality traits, including HRR, milling percentage, nutritional quality, appearance quality, and cooking quality. High temperature hastens the grain-filling process, shortens the grain-filling period, reduces grain weight, and deteriorates grain-milling quality due to increased chalkiness and fissures in rice grains [51]. During the first 15–20 days of grain filling, rice obtains the highest grain yields within the optimal temperature range of 25–29 °C. Different rice cultivars respond differently to heat stress during grain filling, whereas the early and middle phases of grain filling are the most sensitive stages [40,52]. Furthermore, grain quality parameters in rice are influenced by the interaction between genotype and environment. High temperature significantly affects rice grain quality traits, and the head rice recovery (HRR) decreases by 24–35% at temperatures of 30 °C during grain filling [53]. A negative correlation has been observed between high temperatures and the amylose content of rice [54,55]. High temperature decreases the amylose content in endosperm starches due to an increase in the amylopectin B chain that results in a change in the fine structure of amylopectin [54]. Under high temperature, the accumulation of storage protein and starch in rice grains are significantly affected, particularly after heading [44,56].

3. Drought

Drought occurs when unusually dry weather persists long enough to cause serious problems such as crop damage [57]. It is a significant constraint in crop production, affecting over 50% of the world’s rice-growing areas. Drought stress reduces plant growth and disrupts the functions of plant phytohormones and antioxidants by promoting reactive oxygen species (ROS) accumulation [58]. Drought alters morphological, biochemical, physiological, and molecular responses by regulating stress-induced gene and protein functions [59,60]. It is a complex trait that depends on the action and interaction of different morphological, biochemical, and physiological responses [61]. The water requirements of the rice crop vary across different growth stages that directly influence grain yield production. While drought stress affects all stages of rice growth, the flowering stage is more sensitive than the booting and grain-filling stages [62]. Low grain yield under drought conditions is primarily due to increased spikelet sterility and reduced grain filling. Adverse drought stress results in reduced leaf surface area, poor root growth, stem growth inhibition, and early maturity in rice plants [63]. Drought stress during the tillering stage occurs due to reduced uptake of soil moisture, resulting in limited food preparation and decreased cell division in meristem tissues [61,64]. Grain-filling stages suffer due to a reduction in photosynthesis rates and a decrease in assimilate transportation from source to sink. This results in poor translocation of assimilate to the grains enhances spikelet sterility, and empty grains. In drought-stressed conditions, low grain yield is also attributed to a decrease in effective tillers, an increase in spikelet sterility, and a reduction in filled grains and grain weight [61,65]. Breeders should consider these crucial parameters while developing drought-tolerant rice varieties.

Among various stresses, drought stress is the major factor limiting rice crop yield [66]. In rice, leaf rolling is the first symptom of drought stress, resulting in a reduction in the total leaf area [67]. This reduction ultimately leads to decreased plant photosynthesis and assimilate production [68]. However, rice plants respond to severe drought by increasing root density and the growth of root hairs, providing a certain level of compensation under such conditions [69,70]. Drought can also cause sterile pollen grains, leaf senescence, abnormal anther cracking, and a prolonged flowering period in rice [71]. Drought stress reduces dry matter production in rice plants due to a decrease in photosynthesis rates. The severity of drought stress at different stages of rice growth is linked to grain yield, such as stress during the tillering stage resulting in fewer effective tillers and stress during the flowering stage leading to shriveled and fewer grains [72]. However, mild drought stress during the tillering stage can increase the number of effective tillers, seed set, and grain yield per plant [72].

Rice grain quality traits are severely influenced by the interaction between genetic characteristics and environmental conditions [70,73,74]. Among various environmental factors, including heat stress, drought stress is a significant factor limiting rice grain quality. During the grain-filling stage of rice, key enzymes responsible for viscosity and disintegration values, the sucrose–starch metabolic pathway, chalkiness, and other factors play a crucial role in grain quality, which is severely affected under drought stress conditions [75]. The grain filling in rice panicles are directly influenced by the low translocation of the photosynthates from source to sink. In rice, the reduction in photosynthetic rates is mainly caused by stomatal closure and reduced stomatal conductance, leading to low CO₂ supply [76]. Drought stress also adversely affects the structure of the photosystem II (PSII), chlorophyll content, and ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco), resulting in reduced photosynthesis rates [77]. While ROS regulates rice growth and development, excessive accumulation of ROS under drought stress damages the lipid structure of cell membranes [70]. Drought stress also affects various plant growth hormones in rice grains, such as ABA and gibberellin. Overall, drought stress hampers various metabolic activities in rice plants, significantly impacting growth, grain yield, and grain quality. The impact is particularly severe when drought stress affects the grain quality of basmati rice, leading to significant economic losses for the nation [70].

4. Impact of High-temperature and Drought Stresses on Different Growth Stages of Rice

High-temperature and drought stresses have a significant impact on various stages of plant growth and development in rice, ultimately leading to a reduction in grain yield. Although these stresses affect different growth stages of rice plants, the specific responses of each stage are still unclear. In most rice cultivars, a reduction in plant height has been observed under high temperature and water stress during the vegetative stage. These stresses also decrease the rate of photosynthesis and dry matter accumulation, resulting in reduced biomass production [78].

Drought and high-temperature stresses also affect seed germination, dormancy, emergence, establishment, seed quality, and seed vigor [79]. Heat stress, in particular, has a significant detrimental effect on seed germination, leading to poor germination rates and reduced seed viability [46]. Both drought and high temperature affect membrane fluidity and thermostability, leading to decreased seed vigor and germination [46]. High-temperature stress is associated with delayed activation of kinases, heat shock proteins (HSPs), heat shock factors, and Ca²⁺ signaling [80]. Overall, during seed development, especially during the grain-filling stage, heat and drought stresses reduce seed size, resulting in shriveled seeds and endosperm collapse, which significantly reduces seed viability [81].

Drought and heat stresses adversely affect seedling and root growth, causing yellowing, curling, and withering of leaves. Furthermore, there is a decline in the production of biomass and tiller numbers during the tillering stage [82]. However, different rice varieties exhibit varying responses to these stresses due to their diverse genetic makeup. For instance, drought and high temperature have a greater impact on tillering and panicle number in japonica-type rice varieties compared to indica types [83]. As a result, the hybridization of indica × japonica types has led to the development of rice varieties that are tolerant to drought and heat stresses [84]. Here, we discuss the impact of drought and high-temperature stresses on different reproductive stages of rice.

4.1. Impact on the Reproductive Stage

The reproductive phase is the most sensitive stage of the rice crop cycle to various stresses, starting from panicle initiation until physiological grain maturity [22]. Continuous heat stress during the pre-flowering stage for 15 days can reduce panicle numbers by more than 75% and significantly decrease yield. Drought and heat stresses accelerate the distortion of floral organs, resulting in a reduction in their number and grain size [82]. For instance, when a popular rice variety IR64 is exposed to high temperatures (40 °C day/35 °C night), the spikelet number has been reduced by 33%. High temperatures and drought also reduce the number of pollen grains, and in extreme cases, embryo abortion occurs during rice crop flowering [85].

4.2. Impact on Gametophyte and Pollen Development

Drought and high-temperature stresses have a greater impact on anther formation and pollen viability than on the ovule in rice plants [46]. In rice genotypes, both qualitative and quantitative changes in pollen proteins result in a reduction of pollen viability and increased spikelet sterility [86]. Drought stress adversely affects pollen grain moisture, which is crucial for anthesis, pollen grain dispersal, and germination on the stigma [86]. These stresses also lead to a decline in iron uptake by microspores or pollen tubes, reducing pollen germination and viability and further aggravating spikelet sterility in rice [87]. The initial microspore stage after meiosis is particularly susceptible to heat and drought stresses, with complete spikelet sterility occurring after 7 days of continuous stress [88]. Heat and drought stress causes premature tapetal cell degeneration and fragmentation during the pollen mother cell (PMC) meiosis stage, leading to the disruption of microspore nutrition, destruction of pollen wall, and eventual abortion of pollen grains in rice [89]. If these stresses persist for more than 10 days, spikelet fertility and the number of seed settings are reduced by 21.2% and 51.5%, respectively [89].

4.3. Impact on Pollination and Fertilization

In rice, anthesis is the most critical phase of flowering, and stresses caused by high temperature and drought substantially inhibit anther dehiscence [45]. Under stress conditions, the shape of the anther in rice is altered, resulting in reduced pollen viability, diminished pollen number on the stigma, decreased pollen swelling, reduced anther dehiscence, shortened pollen tube length, decreased pollen germination on the stigma, reduced pollen viability, and decreased stigma length [88,90]. The affected components of flowering interrupt pollination and fertilization, resulting in spikelet sterility and grain yield loss in rice [91]. Maximum spikelet sterility in rice is reported when these stresses occur during flowering [82]. Even a brief period of drought and high-temperature stress during anthesis, or even before its start, can negatively impact seed setting. In some cases, complete sterile spikelets have been observed, depending on the genetic makeup of the genotypes [92].

The processes of pollination and fertilization, including anther dehiscence, pollen grain deposition, germination of pollen grains on the stigma, and pollen tube growth, are essential for spikelet fertility and seed setting in rice [93]. If high-temperature and drought stresses interfere with any of these processes, they disrupt phytohormone concentrations in pollen grains and carbohydrate metabolism [94], ultimately resulting in poor anther dehiscence, inadequate pollination and fertilization, and reduced seed setting in the rice crop [22,47,91,95]. It has been observed that drought and heat stresses cause insufficient shedding of pollen grains onto the stigma. Generally, more than 20 pollen grains are required for the germination of 10 pollen on the stigma [96].

4.4. Impact on Seed Setting

The spikelet fertility and seed setting in plants are adversely affected by drought and heat stresses, depending on the genetic makeup of the genotypes [97]. The stresses caused by high temperatures and drought inhibit spikelet differentiation, leading to the degeneration of spikelets and a reduction in spikelet number [98]. Cytokine generation is associated with spikelet development, and the stresses inhibit the process of cytokine generation in plants [99]. Additionally, heat and drought stresses lead to the accumulation of peroxide in the spikelets, damaging the cellular structure, reducing spikelet fertility, and ultimately resulting in low seed setting in rice [22,100].

High-temperature and drought stresses are also associated with a reduction in grain weight during filling in rice. Stressed plants have less grain weight due to a shorter duration of grain setting and less time for pollination and fertilization in rice plants. The seeds developed under these conditions are shrunken with underdeveloped embryos and small size [101]. The small-sized grain weight is also attributed to underdeveloped vascular bundles and the production of fewer nonstructural carbohydrates [101]. Drought and heat stresses also reduce the photosynthetic rate of the plant, leading to functional leaf senescence and undernourished embryo development and seed formation [102]. Under these stresses, starch biosynthesis is inhibited, and the enzymes responsible for starch production are frequently disturbed [103]. The seeds developed under stress conditions contain many immature starch granules in the endosperm cells [22]. Sometimes, a moderate rise in temperature enhances the grain-filling process, but extremely high temperatures significantly reduce seed setting and ultimately lower yield [104].

5. Biochemical and Physiological Impact of High Temperature and Drought Stress

In most cases, drought and heat stress lead to a decrease in the growth of plant stems, roots, leaves, and fruit. Drought stress causes a reduction in turgor pressure and water potential in growing cells, accelerating the process of cell differentiation [105]. Under stress conditions, not all plant parts or organs of rice are affected equally, but there is a significant decrease in the leaf-to-stem ratio. Rice tillering slows down, older leaves die sooner, and tiller death increases under severe heat and drought stress conditions. The main physiological impacts of drought on rice plants include a reduction in the rate of photosynthesis, a reduction in intercellular space during wilting, an enhancement of the respiration rate, a reduction in relative water content, an accumulation of sugars, an enhancement of metabolism, a reduction in abscisic acid hormones, and the breakdown of proteins [105]. In general, drought and high-temperature stress influence the physiological processes of rice, such as photosynthesis, chlorophyll contents, RuBP carboxylase activities, and respiration [106]. Both stresses inhibit the synthesis of cytokines, aggravate spikelet degeneration, and disrupt spikelet formation in rice [44,99].

Drought and high temperature are highly correlated, and their combination reduces SII photochemical efficiency and photosynthetic rate. Moreover, the combination of high-temperature and drought stresses has a more adverse impact on physiological processes than individual stress [107]. A significant reduction in grain yield and quality has been observed under the combination of these stresses [26]. During flowering, rice panicle temperature has a greater influence on spikelet sterility than the air temperature. Although rice plants homeostatically try to adjust the panicle temperature through transpiration cooling, extremely high air temperature leads to spikelet sterility [108]. Drought stress in the panicle is more detrimental to rice seed development, its shape, size, weight, and quality. Moreover, extreme drought and high-temperature conditions result in a reduction of water potential in the panicle, ultimately affecting starch synthesis and hindering seed growth [109]. At the time of rice seed maturity, vacuolar structures are preserved in the cytosol due to osmotic adjustments, resulting in the formation of chalkiness in the grain. Solutes are accumulated in the endosperm cells of rice through osmotic adjustment under high temperatures and drought stress [109].

In rice plant cells, the plasma membrane is more sensitive, and increased temperature and drought stresses cause protein desaturation and alteration of saturated to unsaturated fatty acids, leading to increased permeability and fluidity, enhanced organic and inorganic ion leakage from cells, and affecting membrane integrity [110]. These stresses also change the lipid composition and membrane lipid saturation and generate ROS. They activate calcium channels localized in the membrane and increase the level of cytoplasmic calcium, resulting in the repression or activation of Ca²⁺/CaM-related kinases, transcription factors, and phosphatases [111]. Additionally, heat and drought stresses affect the photosynthetic machinery, particularly photosystem II, leading to the disintegration of thylakoid membranes and grana and the alteration of photochemical reactions [112]. This results in a reduction in the activity of Rubisco due to the inactivation of Rubisco activase [113]. However, some of the important morphological, physiological, and biochemical changes that occur during drought and high-temperature stresses are listed below (

Table 1. Morpho-physiological and biochemical changes under drought and high-temperature stresses.

Morphological	Physiological	Biochemical
Leaf rolling	Reduction in photosynthesis	Activate oxidative reactions
Root length decrease	Cell membrane damage	Increase in mannitol
Reduced fruit width and fruit weight	Phytohormone imbalance	Accumulation of hydrogen peroxide
Shortened period for days to booting, heading, and anthesis	Reduced starch biosynthesis	Electrolyte leakage
Decrease in effective tillers, grains per panicle, and kernel weight	Photosynthesis damages	Accumulation of secondary metabolites
Early maturity	Disturbance of carbohydrate metabolism	Increases phenols
Increase in spikelet sterility	Repression of photosynthesis genes	Increases flavonoids
Shortened duration of grain filling	Down regulation of photosynthesis	Increases proline
Increased the proportion of abnormal seeds	More carbohydrate accumulation in sink	Increase in inositol
Reduction in grain yield	Increase in CO2/O2 ratio	Increase in sorbitol
Reduced the rates of pollen	Decrease in chlorophyll (chl) content, chl a fluorescence, decreased photosystem II (PSII)	Disruption of proteins and enzymes in cell membrane
Reduced pollen tube	Thylakoid membrane damage	Activation of stress-responsive genes, e.g., heat shock protein genes
Lesser number of pollen grain	Increase in leaf temperature	Activation of antioxidant
Decrease in pollen grain germination on stigma	Senescence of functional leaves	Excessive production of ROS
Lesser pollen grain swelling	Higher water use efficiency	Reduces hemicellulose and cellulose
Impede pollination and fertilization	Higher canopy transpiration	Decrease in the CO2 assimilation rate
Tapetum degeneration	Decrease stomatal conductance and stomata opening	Decrease in growth regulator production such as auxin, IBA, cytokinin, etc.
Distort floral organs	Decrease relative water content (RWC)	Production of primarily superoxide and hydrogen peroxide

).

Moreover, heat and drought stresses also disrupt phytohormone balance, disturb photo-assimilate partitioning, and affect glucose metabolism [45]. During the process of anthesis, the sugar content in anthers fades, leading to a poor supply of nutrients for the development of pollen grains [114]. At the spikelet and seed development stages of rice, heat, and drought stresses inhibit the synthesis and activation of various regulatory hormones such as gibberellin, indole-3-acetic acid, and cytokinin, ultimately resulting in spikelet sterility, reduction in seed size, and decreased grain weight [99]. However, the level of abscisic acid increases in the anthers and seeds, resulting in pollen abortion, poor seed germination, and impaired seedling establishment in rice [115]. Under extremely high-temperature stress, starch degradation occurs due to increased enzymatic activity and alterations in the expressions of α-amylase genes in rice [116]. In rice, the metabolism in the phloem and sucrose transportation in the stem, sheath, and grains are also inhibited under drought and high-temperature stresses [117]. Both stresses in rice can lead to a starch shortage, reduced grain size, decreased grain weight, altered appearance, and compromised grain quality [97].

Role of Phytohormones and Antioxidants

Under drought and high-temperature stresses on plants, reflex mechanisms, such as physical stature, physiology, and biochemical, cellular, and molecular-based processes, occurred. To combat the stresses, the prominent features of plants like stomatal adjustment, comparative water contents, improving the root system, osmotic balance, and leaf structure are considered the most important [118]. In addition, the signal transduction pathway and reactive clearance of oxygen are crucial mechanisms for coping with drought and high-temperature stresses via calcium and phytohormones, such as auxin, abscisic acid, brassinosteroids, cytokinin, salicylic acid, jasmonate, and ethylene. Moreover, the exogenous applications of phytohormones prior to or parallel to these stresses render plants with enhanced drought and heat tolerance [119]. Furthermore, the application of exogenous substances like nitric oxide, epibrassinolide, glycine betaine, and proline is also equally important for enhancing drought and high-temperature tolerance in plants [120]. Under drought and high-temperature stress conditions, antioxidants play a significant role in stress resistance. Both enzymatic and non-enzymatic components of the antioxidant defense system occur in the plant cell. Drought and high-temperature stresses increase the activity of antioxidant enzymes such as guaiacol peroxidase, catalase, and ascorbate peroxidize [121]. These scavenging antioxidant enzymes play a crucial to remove the major ROS in plant cells [121].

6. Molecular Basis of High-Temperature and Drought Stresses

To develop rice varieties tolerant to abiotic stress, a deeper understanding of rice genetics, genomics, physiology, proteomics, and molecular breeding is essential [122]. Quantifying and understanding the ecophysiological factors underlying different mechanisms of crop growth and grain yield determination are crucial for future varietal development and crop management [123]. Environmental variations give rise to biotic and abiotic stresses in rice, particularly high temperature and drought that reduce grain yield and quality characteristics [46]. During heat and drought stresses, a dynamic and highly complex signaling system acts on stress-responsive genes to reprogram gene expression [124]. Overall, these stresses induce changes at the molecular, biochemical, physiological, and morphological levels [125]. Both high-temperature and drought stresses are quantitatively controlled by polygenes, and several quantitative trait loci (QTLs) present in the rice genome confer resistance to these stresses. Under stress conditions, changes in gene expression, osmotic adjustment, cell damage, induction of repair systems and chaperones, metabolism, and inhibition of photosynthesis occur [125]. Stress-responsive genes produce two types of proteins: those that regulate gene expression and signal transduction pathways, such as transcription factors (TFs), and those that directly protect the cell against stress, including chaperones, late embryogenesis abundant (LEA) proteins, detoxification enzymes, and antifreeze proteins [126]. Heat shock transcription factors (TFs) in the cytoplasm of a cell lead to the transcription of heat shock proteins (HSPs). The heat shock TFs activate the signal transduction pathway that triggers the expression of heat-responsive genes [69]. Under drought and high-temperature conditions, HSPs play a significant role in minimizing cell damage and promoting stress tolerance. HSPs function as molecular chaperones, assisting in protein folding, accumulation, and localization and playing various roles in cellular processes. Proteases, on the other hand, aid in the degradation of damaged proteins [127].

Overexpression of HSPs under heat and drought stresses delays the adverse effects of these stresses [128]. The expression of different HSFs in response to high-temperature stress indicates their involvement in the regulation of multiple mechanisms. HSPs have been found to be crucial and rapidly expressed under severe high-temperature conditions [128]. In rice, numerous QTLs are linked to different morphological and physiological traits associated with resistance against heat and drought stresses. Therefore, an extensive selection process in breeding can be employed to identify heat and drought-tolerant rice varieties. Several drought-resistant QTLs have been identified in rice, such as qDTY2.1 [129], qDTY2.2 [130], qDTHI2.3 [131], qDTY3.1 and qDTY6.1 [132], qDTR8 [133], qDLR8.1 [134], qDTY9.1A [129], and qDTY12.1 [135]. These QTLs can be utilized in marker-assisted breeding (MAB) programs to develop drought-tolerant rice varieties [61]. Similarly, QTLs associated with high-temperature stress, such as qEMF3, rlht5.1, qHTSF4.1, and qHTT8, have been identified in rice [136,137]. These identified QTLs can be deployed in MAB to develop heat-stress-tolerant rice varieties [138].

7. Management Strategies

Although rice is cultivated in diverse agroclimatic conditions, it is still susceptible to adverse environmental changes. To withstand the challenges posed by high temperatures and drought, certain management practices should be adopted. Rice germplasm possesses diverse genetic resources with varying levels of stress tolerance [139]. Cultural practices, such as adjusting sowing time, water management, nutrient management, and use of plant growth regulators for acclimation, should be implemented to manage high-temperature and drought stresses. Adjusting the sowing dates of the rice crop is another strategy for managing high-temperature and drought stresses, and in some cases, early morning sowing is recommended. Additionally, intensifying pollination and fertilization in rice play a significant role in stress management [46,83]. Developed drought and heat-stress-tolerant varieties have less influence of these stresses on seed setting and yield production, thus important for reducing the economic losses [1]. Screening rice germplasm for drought and high-temperature tolerance and utilizing identified genotypes in breeding programs can contribute to the development of tolerant varieties.

The intensity and duration of stresses, growth stage of rice plants, growth period, age, plant height, and types of rice varieties all play significant roles in managing high-temperature and drought stresses. Targeted breeding programs, including hybridization, can be employed to select high-temperature and drought-stress-tolerant rice varieties. Furthermore, diverse rice germplasm can be screened to identify drought and heat-stress-tolerant varieties [61]. In this regard, the International Rice Research Institute (IRRI) in Manila, Philippines, has initiated the green super rice (GSR) program. The main aim of the GSR program is to develop stable, high-yielding rice varieties with several green traits suitable to be grown under lower input conditions, multiple-stress tolerance, and more nutrient- and water-use efficiency with high genetic gains for various targeted ecosystems [122,140].

7.1. Improvement in Rice Crop Management Practices

To minimize the impact of high temperatures and drought on rice, cultivation and farming techniques can be employed to reduce the adverse effects on grain yield and quality traits [141]. The following agricultural practices can help manage both high-temperature and drought stresses in rice crops:

• Under severe drought and temperature conditions, rice nurseries can be sown early in the morning, or direct sowing can be carried out [81];
• Mulching with paddy straw, peat, or wood chips can be implemented to prevent soil moisture loss in rice crops;
• The use of compost or manure can minimize evapotranspiration and provide nutrients to the soil after decomposition;
• Conservation tillage practices can enhance water conservation, protect the soil surface from harsh weather conditions, and reduce evapotranspiration, thereby maintaining soil health;
• Deep tillage can improve soil permeability and porosity, allowing for maximum water absorption;
• Crop rotation can be practiced to enhance water-holding capacity and improve soil structure throughout the seasons;
• Adding green manure to the soil can improve moisture-holding capacity and enhance soil quality;
• Rainwater harvesting and strip cropping are soil and water conservation techniques that reduce runoff and optimize water usage for irrigation;
• Interplanting and mixed cropping of different crops at different times and durations can provide better water utilization and improve overall crop resilience;
• Contour plowing can be adopted to retain more water in the soil and ensure its even distribution across the cropped area.

By implementing these management practices, the adverse effects of high temperatures and drought on rice crops can be mitigated, leading to improved productivity and sustainability.

7.2. Development of Heat- and Drought-Stress-Tolerant Varieties

Different rice varieties possess diverse genetic makeup and show different levels of tolerance to drought and heat stresses. Cultivating high-temperature- and drought-tolerant varieties to a certain extent can reduce the impact of these stresses. However, the traits involved in genetic improvement and the development of drought and high-temperature-tolerant rice varieties are complex and present a significant challenge for plant breeders [142]. Integrating genomic resources with conventional plant breeding approaches can be helpful in the development of high-temperature- and drought-tolerant rice varieties [143,144]. Rice crops are highly sensitive to high-temperature and drought stresses, and allelic variation can be identified among wild species, subspecies, and rice varieties, offering potential genetic diversity [145,146]. DNA-based molecular markers have been developed for characterizing rice germplasm based on diversity [147]. The diverse drought and high-temperature-tolerant rice genotypes can be used in breeding programs for developing drought and heat-stress-tolerant varieties [148].

With advances in high-throughput sequencing (HTS) technologies, dense molecular markers can be used to construct QTL maps for drought and high-temperature traits. The closely linked markers to high temperature and drought can be utilized in MAB programs for developing tolerant rice varieties. For example, in the construction of a mapping population for QTL mapping, a cross was made between the high-temperature-tolerant rice variety HT54 and the temperature-sensitive variety HT13. Molecular markers were used to identify the QTL OsHTAS, which regulates heat tolerance at the seedling stage of the rice variety HT54 [149]. Similarly, a drought-tolerant QTL, qDTY4.1, has been identified in rice and successfully introgressed into the rice variety IR64 through the MAB program [150]. Further genetic improvement is essential for the development of drought and high-temperature stress-tolerant varieties, and advanced technologies, such as high-throughput sequencing, genomics, transcriptomics, metabolomics, and proteomics, can be employed [150]. These techniques will aid in the efficient utilization of wild species and other genetic resources for improving rice varieties [151]. In addition, functional genomics approaches like allele mining, association mapping, targeting induced local lesions in genomes (TILLING), and homologous recombinant (HR) strategies can be used for the development of drought and high-temperature-tolerant rice varieties [147].

7.3. Genetic Engineering

Although high-temperature and drought-tolerant rice varieties have been developed through conventional breeding programs, this process is time-consuming and limited by certain issues, such as sterility and embryo rescue, when cultivated rice genotypes are crossed with wild species [152,153]. Transgenic techniques have addressed several challenges that conventional breeding approaches encounter, including hybridization, sterility, and embryo rescue. Moreover, rice varieties developed through genetic engineering (GE) approaches are more efficient and stable compared to traditional rice breeding methods [154]. Genetic engineering allows the transfer of high-temperature- and drought-stress-tolerant genes, even from outside the kingdoms, into rice varieties [155]. Genes regulating drought (qDTY2.1, qDTY2.2, qDTHI2.3, qDTY3.1, qDTY6.1, qDTR8, qDLR8.1, qDTY9.1A, and qDTY12.1) and heat stress (qEMF3, rlht5.1, qHTSF4.1, and qHTT8) tolerance can be transferred into rice varieties through GE approaches [156].

Recently, with the advancement of technologies, new techniques, such as high-throughput whole-genome DNA sequences, pangenomes, genome editing, etc., enable high genetic transformation for the improvement and development of elite genotypes. Among these techniques, genome editing enables targeted and precise modifications in genomes that can improve the traits of existing crops. It enables efficient and specific trait generation and selection without adversely impacting native phenotypes. Genome editing is a revolutionary technology in the field of plant sciences and is widely accepted worldwide, even in countries opposing transgenics [157]. It is part of a precision plant breeding approach in which genes of interest can be introduced with minimal changes to the recipient genome. Genome editing through programmable endonucleases is the most recent approach to genetic engineering. Endonucleases are used to specifically induce double-strand breaks in target genes of interest. Among the various genome editing techniques, such as clustered regularly interspaced short palindromic repeats/CRISPR-associated protein 9 (CRISPR/Cas9), zinc finger nuclease (ZFN), and transcription activator-like effector nuclease (TALEN), CRISPR/Cas9 and its variants, has become a powerful technology in plant breeding. Recent advances in CRISPR/Cas-based gene editing techniques have enabled more rapid development of gene-edited lines for crop improvement. Genome editing techniques have been implemented in various crop species to develop crop varieties resistant to various biotic and abiotic stresses [158]. The genetic resources developed through genome editing technology can also be used to develop drought- and heat-stress-tolerant varieties through molecular breeding methods [159].

7.4. Chemical Control Technology

Exogenous application of substances to rice crops can help to reduce the impact of high-temperature stress and improve grain yield and quality [70,160]. For example, spraying 0.2% boron fertilizer during the flowering stage of rice plants increases the activity of antioxidant enzymes, enhances membrane stability, and improves sugar transportation. Boron spray minimizes the adverse effects of high temperature, increases spikelet fertility, improves pollen vigor, and ultimately enhances grain yield production [161]. Similarly, the use of brassinolide on rice crops promotes the synthesis of HSPs, which can tolerate extreme heat [162]. In some cases, a combination of 3–4 plant growth regulators can be sprayed on rice plants under high-temperature conditions to enhance the photosynthesis rate, improve spikelet fertility, promote grain filling, and increase grain yield [163]. Drought stress in rice crops can be mitigated by spraying growth regulators, such as brassinolide and salicylic acid [164]. The application of acetate also plays a significant role in increasing drought tolerance in rice [165,166].

8. Conclusions and Future Perspectives

High-temperature and drought stresses have a significant impact on various morphological, physiological, biochemical, and molecular traits of rice, ultimately resulting in reduced yield and grain quality. Efforts have been made to manage these stresses through adjustments in agronomic practices and genetic improvement of rice varieties using molecular breeding techniques. Drought and high-temperature stresses induce physiological, biochemical, and molecular changes to combat these stresses. The morphological features of plants, such as stomatal opening, improving the root system, leaf structure, etc., are considered the most important to avoid these stresses. The signal transduction pathway, ROS, phytohormones, and antioxidants play a significant role against drought and high-temperature stresses. Genetic engineering and genome editing hold promise for the genetic improvement and development of high-temperature- and drought-tolerant rice crop varieties. In the future, haplotype-based breeding may facilitate the identification of superior haplotypes that can be utilized for the development of high-temperature- and drought-tolerant rice varieties.