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Review

High temperature-mediated disturbance of carbohydrate metabolism and gene expressional regulation in rice: a review

Deng Qin-Dia College of Coastal Agricultural Sciences, Guangdong Ocean University, Zhanjiang,China
,
Jian Gui-Huaa College of Coastal Agricultural Sciences, Guangdong Ocean University, Zhanjiang,China
,
Wang Xiu-Nenga College of Coastal Agricultural Sciences, Guangdong Ocean University, Zhanjiang,China
,
Mo Zun-Guanga College of Coastal Agricultural Sciences, Guangdong Ocean University, Zhanjiang,China
,
Peng Qing-Yonga College of Coastal Agricultural Sciences, Guangdong Ocean University, Zhanjiang,China
,
Chen Shiyuna College of Coastal Agricultural Sciences, Guangdong Ocean University, Zhanjiang,China
,
Mo Yu-Jiana College of Coastal Agricultural Sciences, Guangdong Ocean University, Zhanjiang,China
,
Zhou Shuang-Xib New Zealand Institute for Plant and Food Research Limited, Hawke’s Bay,New Zealand
,
Huang Yong-Xianga College of Coastal Agricultural Sciences, Guangdong Ocean University, Zhanjiang,ChinaCorrespondencehyx978025@126.com
ORCID Iconhttps://orcid.org/0000-0003-1188-4852
ORCID Icon &
Ling Yua College of Coastal Agricultural Sciences, Guangdong Ocean University, Zhanjiang,ChinaCorrespondencelingyu820110@163.com
ORCID Iconhttps://orcid.org/0000-0002-8067-523X
ORCID Icon show all
Article: 1862564
Received 08 Oct 2020
Accepted 07 Dec 2020
Published online: 20 Jan 2021

Review

High temperature-mediated disturbance of carbohydrate metabolism and gene expressional regulation in rice: a review

ABSTRACT

ABSTRACT

Global warming has induced higher frequencies of excessively high-temperature weather episodes, which pose damage risk to rice growth and production. Past studies seldom specified how high temperature-induced carbohydrate metabolism disturbances from both source and sink affect rice fertilization and production. Here we discuss the mechanism of heat-triggered damage to rice quality and production through disturbance of carbohydrate generation and consumption under high temperatures. Furthermore, we provide strong evidence from past studies that rice varieties that maintain high photosynthesis and carbohydrate usage efficiencies under high temperatures will suffer less heat-induced damage during reproductive developmental stages. We also discuss the complexity of expressional regulation of rice genes in response to high temperatures, while highlighting the important roles of heat-inducible post-transcriptional regulations of gene expression. Lastly, we predict future directions in heat-tolerant rice breeding and also propose challenges that need to be conquered in the future.

Introduction

The Earth is getting warmer and extreme weathers are becoming more frequent. According to the Intergovernmental Panel on Climate Change Prediction, the temperature will increase by 2°C to 5°C by the end of the 21st century.1 Global warming means more frequent extreme high-temperature weather events, the dramatic effects of which can result in significant production losses.2 Rice (Oryza sativa) is one of the most important crops in the world, the production of which needs to increase significantly to meet the demands from increasing populations. However, high temperatures caused by global warming are predicted to cause losses of rice yields in many parts of the world, especially Asia. It has been estimated that as much as 10% of rice yields might be lost with every 1°C rise.3

The damage from high temperature can vary at different developmental stages of rice, from germination4 to seedling,5,6 flowering and grain maturation stages.7,8 Flowering and grain-filling stages are heat sensitive phases in rice plants. Heat damage at these stages can cause significant economic loss to rice production.7,9,10 During the fertilization phase, high temperatures could affect dehiscence of anthers and also cause generation of defective pollen grains, subsequently inhibiting pollination and reducing grain yield.11,12 The heat damage to anthers is positively correlated with their surrounding temperatures, as it has been found that the fertility and grain weight of superior spikelets decreased more than those of inferior spikelets because of their differential surface temperatures.13 During the process of grain ripening, especially in the early stage of grain filling, high temperatures lead to decreased grain weight and produce chalky and/or empty grains.14

Plants have developed intricate systems to respond to a variety of environmental challenges, including heat stress.15 The fundamental heat response system in plants involves activation of heat-responsive genes. Deciphered heat-inducible transcriptomes from different plants imply common and species-specific gene regulatory machineries co-existing in different plant species, including the model plant Arabidopsis16 and important commercial crops such as wheat,17 rice8 and tomato.18 With the assistance of sequencing technologies, rapidly accumulating evidence has proved the importance of gene expressional regulation at a post-transcriptional level during plant growth and development, especially in response to environmental cues.19–22

During fertilization and grain-filling stages, there is strongly activated sugar and energy metabolism in the floral organs of rice plants.23,24 Although some studies have recently discussed the impacts of high temperature on rice from different points, only a few have specified the heat damage to fertilization and/or to grain development in rice, mediated as global disturbances to carbohydrate generation, allocation and usage.7,25,26 Furthermore, any recent discussion of involvement of different gene expressional regulatory machinery in response to heat stress in rice is rare. In this review, we provide an update on recent findings on high temperature affecting carbohydrate metabolism in rice during the reproductive stages, and we propose a hypothesis that the impact of sugar/energy consumption and transportations contributes to heat-inducible damage to rice production and grain quality. In addition, heat-inducible gene expressional regulatory machineries in rice are discussed, while highlighting recent findings on RNA-mediated gene post-transcriptional regulations.

The impact of high temperature on carbohydrate source

As we well know, assimilates in higher plants are originally sourced from the chloroplasts by photosynthesis.27 Reactive oxygen species (ROS), including singlet oxygen (1O2), superoxide (O2−), hydroxyl radicals (•OH), and hydrogen peroxide (H2O2), are unavoidable by-products of photosynthesis.28 Although ROS are important for maintaining energy and metabolic fluxes, optimizing cell functions, and controlling whole-plant systemic signaling pathways, the over-accumulation of these under stress conditions, such as high temperatures, will destroy essential molecules, and denature proteins and membrane systems.29,30

The connection between ROS metabolism and heat tolerance in rice has been studied thoroughly. Heat-induced ROS accumulation affects rice plant growth and development through its lifecycle, from seed germination to seedling growth and grain maturation.31–33 Different studies have shown that rice varieties possessing strong antioxidant capacity are generally more resistant to high temperatures, and the amount and activity of antioxidants are positively correlated with heat tolerance in rice plants.34,35 Furthermore, ROS cleavage capacity in the vegetative tissues of the rice plant can directly affect its yield and grain quality. Over-expression of a Golgi/plastid localized protein, manganese SOD 1 (MSD1), significantly enhances the heat tolerance of transgenic rice, which possesses a stronger ROS-scavenging ability and generates grains with better quality than wild-type (WT) rice. Accordingly, suppression of MSD1 markedly reduces the heat tolerance of the rice plants.36 These studies demonstrated that heat shock caused rice plants to over-produce ROS. In contrast, activation of the ROS cleavage system in the affected plants appeared to be a conventional response during the process of acclimation to this environmental change, and moreover, the ROS-scavenging capacity of the affected plant usually corresponded with reduced heat damage to both vegetative tissues and grains.

Being an aerobic physiological process, photosynthesis unavoidably produces ROS in chloroplasts under both normal and heat-stress conditions.37,38 Chloroplasts are some of the largest ROS producers in green tissues of plants, together with peroxisome, producing as high as 20-fold more ROS than mitochondria in the daytime. And this feature makes the chloroplast itself as the biggest target of ROS attack.39–43 Because several photosynthetic enzymes, such as Rubisco, are sensitive to higher temperatures (>35°C), the Calvin cycle procedures will not run smoothly under heat stress.44,45 Over-accumulation of ROS in chloroplasts occurs when more electrons are released in the electron transport chain (ETC) than the electron-consuming capacity of the Calvin cycle under stress conditions.38,46,47 The accumulated potent ROS therefore quickly attack the overall structural integrity of the chloroplast, especially thylakoid membranes.48,49 It has been reported that ROS destroy the function of core proteins in the photosystem II (PSII) system, such as the D1 protein38,47,50 and then repress the repair process of PSII by inhibiting the de novo synthesis of PSII proteins,51–53 although a large number of enzymatic and non-enzymatic antioxidants are generated to reduce the accumulation of ROS in chloroplasts.54,55 The impact of over-produced ROS on assimilate accumulation in leaves comes in a second way. To mitigate the toxic effects of ROS, the radical scavenging enzymes are activated in the affected cells. Radical scavenging enzymes are triggered and energized by the ATP-producing processes, such as glycolysis and the tricarboxylic acid cycle (TCA) pathways,56 indicating that the affected plant has consumed large amounts of energy to remove ROS from cells on the leaves under heat stress conditions. Taken together, these studies demonstrated that the heat-mediated over-accumulation of ROS will decrease the efficiency of assimilation in rice leaves, implying reduction of the influx of carbohydrates to floral organs during this reproductive stage.

Energy production systems are highly affected by high temperature in rice leaves. Many proteins participating in energy production process in the TCA cycle and its branching circuits, including Mt ATP synthase beta chain, inorganic pyrophosphatase (PPase), and also Ferredoxin-NADP(H) oxidoreductase (FNR), were decreased by heat treatment.57,58 Notably, disturbance of TCA, to a certain extent, is negatively correlated with heat tolerance in rice,57 suggesting more severe disturbances happening in heat-sensitive rice cultivars when facing hot weather. Supportively, results from other studies indicate that the majority of genes involved in TCA cycle metabolism are down-regulated in rice leaves when under high temperature, although some others involved in this procedure and many of those participating in glycolysis metabolism are significantly induced.8,59–61

A stable photosynthetic system could alleviate the heat-inducible damage and increase grain yield in rice under heat stress conditions. It has been found that improving the activity of the Calvin cycle enzyme sedoheptulose-1,7-bisphosphatase (SBPase) by gene overexpression could partially counteract the impact of high temperature on photosynthesis of transgenic rice.62 Supporting this, transgenic rice plants expressing more Rubisco activase (RCA) possessed higher thermotolerance and grew better at high temperature than wild-type (WT) plants.63 The same conclusion comes from comparisons between different rice relatives. A wild rice relative, O. meridionalis, growing in northern Australia, was found to be a more heat-tolerant than O. sativa, with correspondingly higher abundance of enzymes involved in the Calvin Cycle.58 Furthermore, another heat-tolerant rice relative, O. australiensis, also possesses a stable photosynthesis system under high temperature. The photosynthetic rate of O. australiensis keeps unaffected at 45°C, while that of O. sativa was almost halved under the same condition. Further experiments showed that there are some amino acid sequence differences between the RCAs from O. australiensis and those from O. sativa, suggesting the heat tolerance in O. australiensis can be attributed to the thermal stability of its RCAs, which enable the Rubisco to remain active under high temperature.64 Coinciding with the findings mentioned above, the capacity of the leaf photosynthetic system directly affects rice growth and its grain yield, and changing photosynthetic electron transport rates via manipulation of the cytochrome b6/f complex to enhance photosynthesis has been suggested as a potential way to increase rice grain yield.55

In summary, heat triggered over-production of ROS cuts down carbohydrate accumulation, not only through inhibition on carbohydrate generation but also through competition between limited sugars to remove these toxic items, which will result in disturbance of assimilate allocation and decrease in the amount of carbohydrates for transportation. Rice cultivars that have the ability to maintain net carbohydrate gain under high temperature conditions show better heat-tolerant capacity.

High temperature causes sucrose and energy deficiency in rice floral organs

The fertility efficiency and grain quality of rice are affected by sugar and starch metabolic activities. Wu et al. (2015) identified five highly up-regulated pectinases from floral organs of heat-treated rice plants,65 suggesting that a pectinase-mediated metabolism could be involved in rice fertilization. The soluble sugar contents also significantly decreased in the rice lodicules when plants were exposed to high temperatures, correlating with a low percentage of opened spikelets t,53 which may consequently contribute to low grain yields. More supporting evidence comes from molecular studies. By analyzing metabolomic and transcriptomic changes in anthers, pistils before pollination, and pollinated pistils in different rice cultivars, Li et al. (2015b) proved that a sugar metabolism-related enzyme, invertase 4 (INV4), were the crucial metabolic and transcriptional component that differentiated floral organ tolerance or susceptibility to hot weather.60 Jiang et al. (2020) found most recently that a heat-tolerant rice variety (TLY83) accumulated more NAD (H), ATP, and antioxidant capacity under high-temperature conditions than a heat-sensitive variety (LLY72).66 Further analysis revealed that reduced suppression of acid invertase (INV) activity in TLY83 resulted in more stable sucrose metabolic activities in pollen grains under high temperatures. Transcriptional levels of all invertase-encoding genes tested in this study, including CINV1, CINV2, INV2, and INV3, were significantly induced by high temperature in TYL83. Moreover, CINV1 and INV2 are also highly induced in LLY72. Notably, although these genes were up-regulated at transcriptional level upon heat stress, their activities decreased when compared with those from plants growing under control conditions,66 indicating that posttranscriptional modulation fine-tuned the abundance of the enzymes or had other impacts withdrawing the activities of proteins under high temperatures.

During the development of rice grains after fertilization, several important sucrose hydrolases and transferases genes, including Os09g0553200, Os06g0229800, Os02g0141300, Os01g0952600, Os02g0661100, and Os02g0528300, are significantly repressed by high temperatures, corresponding to decreases of α- and β- amylase activities, and lower sucrose and starch contents in the affected grains.67 In support of this finding, it has been found that the sucrose synthase 3 from the ‘Habataki’ allele (SUS3) participates in starch formation in rice grains. The expression of SUS3 is increased more significantly under high-temperature conditions in the heat-tolerant cultivar ‘Habataki’ than in the heat-sensitive cultivar ‘Nipponbare’. Transformation of the ‘Habataki’ SUS3 gene into ‘Nipponbare’ increased heat tolerance of transgenic rice during grain ripening,68 highlighting the strong connection between sucrose synthesis and rice grain acclimation to high temperatures. In addition, heat-mediated inhibitions of sucrose/starch production related genes, including cyPPDK, GBSSI, BEIIb, and AGPS2b, have been proved to play essential roles in the generation of chalky rice grains during high-temperature weather.69–71 These studies demonstrated that inhibitions of enzymes functioning in sucrose and starch syntheses posed significant harm to grain yields and quality under hot weather. Moreover, a worse situation also exists: Enzymatic responses for starch consuming and degradation, such as alpha-Amylases (α-Amy), including Amy1A, Amy3D and Amy3E, and soluble starch synthase (SSS) isoforms (SSSIIb, SSSIIc, SSSIIIb and SSSIVa), are significantly induced by high temperature, which consequently aggravates the shortage of starch and promotes the generation of chalky rice grains.69,72,73 Thus, consumption of starch does not always bring benefits for energy (ATP) supply in the developing grains, as high temperatures can disrupt electron transport in the mitochondria,72 which subsequently affects the TCA procedure and suppresses the generation of ATP, making carbon usage less efficient. Furthermore, similar to what happened in the vegetative organs, over-accumulation of ROS has been reported in different studies. In addition to its damage to energy production, removing ROS consumes large amounts of energy in the developing grains under heat stress. This has been thoroughly studied in the past few years.74–76

The floral organ, both before and after fertilization, is the growth center of the plant, which demands sucrose from the source (leaves) to alleviate its carbon and energy starvation under heat stress. Severe shortages of carbon and energy supplies, caused by disturbance of sucrose and starch metabolism, make flowers and grains of rice vulnerable to high environmental temperatures, and thus pose threats to rice propagation. Actually, there is some evidence that the rice plant may activate a self-salvation system to mitigate heat-inducible damage to its reproduction. ABA-mediated enhancement of sucrose transport is suggested to maintain energy homeostasis of the rice spikelet and reduce ATP consumption, subsequently improving heat tolerance of rice.77 Furthermore, activation of sucrose transporters is critical for maintenance of photo-assimilate supply to the filling grains and contributes to starch accumulation in grains under high-temperature conditions. A heat-tolerant rice cultivar, ‘Genkitsukushi’, showed better tolerance and produced fewer chalky grains than a heat-sensitive cultivar ‘Tsukushiroman’. Further experiments demonstrated that the relative higher expression of a sucrose transporter, OsSUT1, in both leaves and floral organs, was responsible for the stable starch accumulation in ‘Genkitsukushi’ grains under high temperature.78

Based on the studies mentioned above, high temperature causes significant variations in carbohydrate metabolism in cells from various rice tissues, resulting in low efficiency of assimilate generation and application. Sufficient input of carbohydrates from the source, and high efficiency in using these, would alleviate heat damage to fertilization and grain development in hot weather. To summarize, a working model describing carbohydrate flows and their metabolism in rice plants under heat stress is illustrated in Figure 1. We propose that the capacity to maintain sufficient carbohydrate influx to floral organs, and the efficiency of starch synthesis, will mitigate heat-induced harm to rice production.

Figure 1. Heat stress-mediated disturbances of sucrose and starch metabolism-related genes and processes in rice. The pink-framed box shows changes in rice floral organs, with details of differential expressed genes related to the process. The light blue-framed box shows changes in rice leaves. Green arrows stand for up-regulation of gene(s) or promotion of a procedure. Red “T” signs stand for down-regulation of gene(s) or inhibition of a procedure. Green arrows stand promotion of procedure. Red “T” signs stand for inhibition of procedure

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3. Expressional regulations of heat responsive genes in rice

Functional genes, including those participating in ROS generation and cleavage and photosynthesis, together with those playing roles in regulating carbohydrate production and consumption, are significantly changed in response to high temperatures, as we discussed above. Expressional changes of these genes are the fundamental response to high temperature, which is regulated through different layers. Like those of other higher plants, heat shock transcription factors (HSFs) and also non-HSF transcription factors from rice play essential roles in controlling gene expression upon heat stress, while accumulated evidence has demonstrated the important functions of post-transcriptional regulations during high-temperature responses.

3.1 Heat-inducible HSFs and their downstream genes HSPs in rice

Heat shock transcription factors (HSFs) can be divided into three types: A, B and C. The function of HSFA is the most important. Generally, HSFA exists in the cytoplasm as a monomer. When subjected to heat stress, it rapidly assembles into a trimer, then recognizes and binds with the heat shock element (HSE) on the promoter region of heat shock protein (HSP) coding gene, resulting in activations of downstream gene expression to cope with the adverse environmental temperature.79 The expression pattern and function of different HSFs vary in rice. Among tens of HSF genes, OsHSFA1 has stable expression in different tissues and under various stressful stimuli, whereas OsHSFA2a is the most significantly up-regulated HSFs by high temperature, with strong expressions of its downstream target genes, suggesting that OsHSFA2a plays the most important role in rice acclimation to high temperatures.80 As supporting evidence of this, HSFA2 protein has also been proved to be the master HSF in other plants suffering heat stress.81–83 Rice transcriptome analysis showed that 12 of the 21 HSFs, namely OsHsfA2a, OsHsfA2b, OsHsfA2c, OsHsfA2d, OsHsfA3, OsHsfA4b, OsHsfA4d, OsHsfA7, OsHsfB1, OsHsfB2a, OsHsfB2b and OsHsfB2c, were significantly up-regulated in the early stage of high-temperature treatment,8 suggesting their important roles in triggering expressions of downstream genes in rice at the beginning of temperature rises.

The small HSP (sHSP) subfamily is the most abundant HSP in plants. In rice, it has been reported that sHSP encoding genes OsHSP26.7, OsHSP23.2, OsHSP17.9A, OsHSP17.4 and OsHSP16.9A are upregulated as a heat response at seedling and also flowering stages. Further analysis showed that the expression levels of these five sHSPs are positively correlated with the heat resistance of rice.84 Similarly, Guo and colleagues showed that sHSP, OsHSP20 responded quickly (increased up to 4000 times within 1 h) and that overexpression of OsHSP20 improved the heat tolerance of rice at different developmental stages.85 Another sHSP, OsHSP26, is suggested to be able to protect the PSII in rice leaves under heat stimuli.86

Other HSPs from rice are also essential in responses to high temperature. A recent study demonstrated that in addition to sHSPs, HSP70-OsEnS-45, OsHSP74.8 and OsHSP70 were differentially expressed between heat-resistant and heat-sensitive rice genotypes under long-term high-temperature treatments.87 These genes are considered to be functional marking genes for screening of heat-resistant rice varieties. OsHSP82 can affect nitrogen metabolism, whereas OsHSP81-1 is involved in maintaining sugar or starch synthesis in rice under hot weather, and the expression intensity of them both directly affects the heat tolerance of rice.84 HSP100 family proteins mainly play the role of depolymerizing or degrading proteins, helping to alleviate heat stress in rice. Transgenic rice overexpressing OsHSP101 was more resistant to high temperature during vegetative growth than WT,88 which could be attributed to HSP101 regulating protein-protein interaction-mediated thiamine synthesis during heat shock.84 Interestingly, it has been demonstrated that O. japonica rice ‘Nipponbare’ and O. indica rice ‘N22ʹ have contrasting basic heat tolerance and long-term acquired heat tolerance because of the complicated interaction between HSP101 and another heat-responsive protein HSA32.89

3.2 Other transcription factors in rice involved in heat stress response

In addition to the HSF-HSP regulons, other heat-responsive regulatory pathways have been found in rice, other enzymes and transcription factors activated by heat shock. A transcription factor responsive to drought stress, DREB-a1, is significantly up-regulated under short-term heat shock,8 and this is not a unique instance: a stress-responsive NAC transcription factor SNAC3 has also been considered beneficial for both drought and heat tolerance through modulation of ROS in rice.90 Expression levels of OsBBX22 and OsBBX24, two transcription factors from a B-box domain-containing transcription factor family in rice, increase accordingly to the high temperature span, indicating their involvement in the expressional regulatory networks of heat-responsive genes.91,92 By comparing the transcriptome data of panicles from two rice varieties (heat-resistant ‘Huanghuazhan’ and heat-sensitive ‘IR36ʹ) growing at 40°C and 32°C, Wang et al. (2019) identified 1675 commonly regulated heat-responsive genes in the two varieties, 1688 genes specifically changed in heat-tolerant varieties and 707 genes altered in heat-sensitive varieties. Gene Ontology (GO) analysis showed that the specific response genes in the heat-resistant variety were significantly enriched in 54 gene ontologies, including WRKY, HD-ZIP, ERF and MADS. KEGG analysis showed that the genes specifically expressed in heat-resistant and heat-sensitive varieties also belonged to different metabolic pathways.93 Similar results were found in an earlier study.94 These examples indicate that regulatory pathways of heat response and other abiotic stimuli could partially overlap. Other studies demonstrated that a group of transcription factors, including HSFs, together with WRKYs, MYBs, NACs, AP2/ERFs, bHLHs, bZIPs and C2H2s, comprise the main transcription factors, binding to cis-elements, such as GCC box, HSE, ABRE and CE3, to trigger the activation of target genes at different stages of heat shock.8,61 Interestingly, two MYB transcription factors, MYBS1 and MYBS2, regulate the on/off switch of Amylase (α-Amy) expression in rice by competing for the same DNA sequence in the gene promoter. Sugar shortage triggers nuclear importation of MYBS1, which induces α-Amy expression subsequently, whereas provision of sugar promotes nuclear importation of MYBS2 and represses the gene expression. High temperature down-regulates the expression of MYBS2, and subsequently induces α-Amy3. Activation of α-Amy3 and suppression of MYBS2 enhance heat tolerance in rice. These findings reveal insights into a unique regulatory mechanism for α-Amy gene expression in maintaining sugar homeostatic states under different growth conditions.95

3.3 Heat responsive post-transcriptional regulations in rice

Evidence for epigenetic regulations involved in heat response has increased quickly in recent years. Pre-mRNA alternative splicing is an important regulation of gene expression at the post-transcriptional level, which has been proved to be involved in activation of heat tolerance in Arabidopsis.96 In rice, the stress-responsive transcription factor OsDREB2B produces two different mature mRNA variants through alternative splicing. The mRNA variant that would be translated into protein with transcriptional function was markedly increased under stress conditions. Further experiments demonstrated that stress-inducible alternative splicing of pre-mRNA played an important role in regulation of OsDREB2B after transcription.97 One of the key HSFs in rice, OsHSFA2d, encodes two major variants, OsHSFA2d I and OsHSFA2d II through alternative splicing. OsHSFA2d II, without the transcriptional activity, is the major splice form under normal growth conditions. However, when exposed to high temperatures, pre-mRNAs of OsHSFA2d are selectively spliced into the transcriptional active form OsHSFA2d I, coding functional protein products that participate in the heat response. This nucleus-localized protein regulates the upregulation of unfolded protein response sensors OsIRE1 and OsbZIP39/OsbZIP60 and the unfolded protein response marker OsBiP1.98 OsbZIP58 can promote the expression of a variety of seed storage protein genes and starch synthesis genes, and inhibit the expression of some starch hydrolysis α – amylase genes under high temperature. Interestingly, high temperature regulates the alternative splicing of OsbZIP58 and promotes the formation of truncated OsbZIP58-β protein by suppressing the production of OsbZIP58-α. The transcriptional activity of OsbZIP58-β in rice at the grain-filling stage is lower than that of OsbZIP58-α. It has been demonstrated that less alternative splicing activity occurs on the OsbZIP58 gene in rice varieties that are less sensitive to hot weather.99 Moreover, OsbZIP74 also underwent alternative splicing upon increased temperatures (Lu et al., 2012). These studies demonstrate that high temperature activates the unfolded protein reaction signaling pathways to rebuild cellular protein homeostasis, possibly by means of alternative splicing. Alternative polyadenylation (APA) is another important RNA way to regulate gene expression at the mRNA process level. In rice, significant APA events were carried on by high temperature and other kinds of stresses. Genes highly induced by stresses tended to undergo APA, accumulating isoforms with a short 3ʹ untranslated region (3ʹ UTR). The stress-responsive APA events were widely involved in crucial stress-responsive genes and pathways. Thus, APA acted as a negative regulator in heat tolerance. Furthermore, because of its involvements in regulations of glutathione metabolism and MAPK signaling pathways, APA is considered to be a brigde connecting the abiotic and biotic stress-responsive regulatory networks in rice.100

MicroRNA (miRNA) regulates its target gene expression after transcription. The development and application of RNA-sequencing technology have provided a great help in mining microRNA expression under different conditions. In a comparison study, several microRNAs, including osa-miR1439, osa-miR1848, osa-miR2096, osa-miR2106, osa-miR2875, osa-miR3981, osa-miR5079, osa-miR5151, osa-miR5484, osa-miR5792 and osa-miR5812, were detected only in the heat-resistant cultivar N22, but not in a heat-sensitive cultivar,101 suggesting that these miRNAs may play special roles in enhancing heat tolerance of rice. Recently, a study on the rice variety ‘Pusa Basmati-1ʹ found that expressions of 31 and 24 microRNAs significantly increased and decreased, respectively, in flag leaves upon heat shock. Moreover, in addition to a group of microRNAs commonly regulated in both leaves from young seedlings and flag leaves during the reproductive stage, there were nine microRNAs specifically expressed in seedling leaves and 60 microRNAs expressed uniquely in flag leaves. It is noteworthy that a subgroup of microRNAs, including osa-miR166d-5p, osa-miR166h-5p, osa-miR172d-5p, osa-miR396a-5p, b-5p, osa-miR1879, and osa-miR6249a, b, showed opposite expressional regulatory patterns in leaves from young seedlings and flag leaves,102 suggesting differential roles of their target genes during different developmental stages when suffering heat stress.

Recently, Tang and colleagues (2020) revealed the role of RNA modification in rice acclimation to hot weather, mainly pointing to photosynthesis metabolism. An RNA 5-methylcytosine (m5C) methyltransferase mutation osnsun2 was hyper-sensitive to high temperature. Interestingly, about one-third of the mRNA m5C methylation sites mediated by OsNSUN2 are distributed on the mRNA sequences those encoding chloroplast proteins. OsNSUN2-mediated m5C modifications of mRNAs of many genes that are involved in photosynthesis and detoxification system in rice, such as β-OsLCY, OsHO2, OsPAL1 and OsGLYI4, are accumulated by heat shock, which may consequently enhance the efficiency of the generation of target proteins. Therefore, the methyltransferase OsNSUN2 could play an essential role in maintaining normal photosynthesis and metabolism of rice at higher temperature, by regulating the m5C modification of mRNAs.103

In summary, analysis of large-scale datasets revealed that not only transcriptional but also post-transcriptional, regulations are critical for rice acclimation to environmental high-temperature challenges. Heat-responsive transcription factors co-operating with post-transcriptional regulations on the RNA layer fine-tune the final expression of heat-responsive proteins. This interaction between different regulatory layers upon heat shock makes the gene expressional regulatory networks more complicated.

Perspective and challenges

The increasing frequency of heat shock caused by global warming has posed serious threats to rice production in the past decades. And unfortunately, present climate projections predict that extreme high temperature on Earth will be more common and severe in future.104 Previous studies have shown the physiological changes in energy allocation and consumption in rice in response to heat stress, and also, to a certain extent, gene expressional regulation. One of the challenges in breeding heat-tolerant rice varieties should be to focus on how to maintain the efficiency of carbohydrate accumulation in both vegetative and reproductive organs under high temperatures. This work could be accelerated by deciphering the regulatory mechanisms of carbohydrate metabolic procedures, using the application of modern plant biology approaches. Although the gene expressional mechanisms underlying the heat stress response are not totally clear yet, accumulating evidence has shown the involvement of posttranscriptional regulations on the RNA layer, such as alternative splicing, small RNAs, and RNA modifications during the heat stress response. Furthermore, answers are needed as to whether and how other kinds of non-coding RNAs, such as long non-coding RNA and circle RNA, function in these regulatory networks.

Acknowledgments

This study was supported by National Undergraduate Training Programs for Innovation and Entrepreneurship (230419145) and University Improvement Program (230419099) from Guangdong Ocean University. We apologize for not being able to cite all publications in the literature owing to space and time limitations.

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