Research Progress on Heat Stress of Rice at Flowering Stage

Wang Yaliang, Wang Lei, Zhou Jianxia, Hu Shengbo, Chen Huizhe, Xiang Jing, Zhang Yikai, Zeng Yongjun, Shi Qinghua, Zhu Defeng, Zhang Yuping

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Research Progress on Heat Stress of Rice at Flowering Stage

Wang Yaliang1, 2, Wang Lei2, Zhou Jianxia3, Hu Shengbo2, Chen Huizhe2, Xiang Jing2, Zhang Yikai2, Zeng Yongjun1, Shi Qinghua1, Zhu Defeng2, Zhang Yuping2

(College of Agronomy, Jiangxi Agricultural University / Key Laboratory of Crop Physiology, Ecology and Genetics Breeding, Ministry of Education, Nanchang 330045, China; China National Rice Research Institute / State Key Laboratory of Rice Biology, Hangzhou 310006, China; Jinhua Municipal Institute of Agricultural Sciences, Jinhua 321017, China)

Global warming has caused frequent occurrence of heat stress at the flowering stage of single-season rice in the Yangtze River region of China, which results in declines of spikelet fertility and yield in rice. Rice flowering stage is the most sensitive period to high temperatures, and therefore, the key for heat stress happening is the flowering stage coinciding with high temperature, which causes spikelet fertility decreasing in heat-sensitive varieties, and is the major factor for heat injury differences among various rice planting regions. With the development of rice breeding, temperature indexes for heat stress has been converted from daily maximum temperature of 35 oC to 38 oC with the stress duration of more than 3 d. During the flowering stage, anther dehiscence inhibition and low pollen shedding onto the stigma are two main reasons for spikelet fertility reduction under high temperatures. At panicle initiation stage, high temperatures aggravate spikelet degeneration, and destroy floral organ development. Various types of rice varieties coexist in production, andhybrid rice demonstrates the highest heat resistance in general, followed byandrice varieties. In production, avoiding high temperature is the main strategy of preventing heat stress, and planting suitable cultivars and adjustment of sowing date are the most effective measures. Irrigation is an effective real-time cultivation measure to decline the canopy temperature during the rice flowering stage. We suggested that further study should be focused on exploring heat injury differences among different rice variety types, and innovating rice-planting methods according to planting system changes in rice planting regions with extreme heat stress. Meanwhile, high temperature monitor and warning systems should be improved to achieve optimal heat stress management efficiencies.

flowering stage; heat stress; spikelet fertility; high temperature; yield; variety

Global climate change has led to an increase in the earth’s surface temperature in recent decades, and the temperature is predicted to rise by 2 oC to 4 oC by 2050 (Stocher et al, 2013). Such changes have caused increases of summer temperature at the Yangtze River region in China, with the highest temperature being above 40 oC and lasting for 10–15 d (Tang et al, 2014; Liu and Han, 2016). High temperatures result in serious adverse effects on rice production (Shi et al, 2017).

Since 1970s, the rice-planting pattern has gradually changed from double-season to single-season planting. The flowering stage of single-season rice occurs at the period with the highest temperatures, which can adversely affect rice yield. High temperatures during flowering and grain filling stages lead to heat stress, resulting in large reductions in spikelet fertility and deterioration in rice quality (Shi et al, 2016). With the intensification of climate change, summer heat stress has become an important environmental factor in limiting rice yield (Espe et al, 2017). Indeed, in recent years, temperatures above 35 oC have been reported to last for over 20 d during the flowering period of single-season rice (Wang P et al, 2015).

In view of heat stress at the flowering stage, the temperature indexes of heat stress, differences in heat resistance among rice varieties, and cultivation methods to alleviate heat stress have all been investigated. A maximum of 35 oC is thought to be the critical temperature for spikelet fertility. Previous studies found that spikelet fertility decreases under high temperatures because of anther dehiscence inhibition and a reduction of pollen activity (Satake and Yoshida, 1978; Matsui and Omasa, 2002; Zhang Z J et al, 2014; Coast et al, 2016). Additionally, high temperatures inhibit grain filling during the early stages of ripening (Wei et al, 2002).

Recently, many changes have occurred in rice planting systems and the rice varieties in China, and these changes greatly influence the occurrence of heat stress. Developments in breeding technologies have increased the number of rice varieties used in production,including thehybrid rice. However, traditional temperature index for heat stress may be not suitable for new varieties, and the characteristics of heat resistance in different varieties are unclear. Although many studies have been conducted on heat stress mechanisms using heat-resistant materials and mutants (Poli et al, 2013; Wang D et al, 2016; Han et al, 2018; Zhang et al, 2018), these are differed from the varieties used in production. With the intensify of global warming and the innovation of rice cultivars, heat stress phenomenon and the characteristics of heat resistance among rice varieties differ from those in traditional studies (Hu, 2013; Zhang S et al, 2016). Therefore, this review aimed to summarize the characteristics of heat stress at present, the changing of temperature indexes for high temperature damage at rice flowering stage, and provide theoretical support for further research on the damage management of heat stress based on the occurrence mechanisms of heat stress.

Characteristics of heat stress at rice flowering stage

In China, the planting pattern and rice production mode of rice are different due to large planting area and various varieties. Rice flowering stage is the most sensitive period to high temperatures, and heat stress has occurred frequently in the past 15 years. In 2003, heat stress caused a loss of 5.18 × 107t in rice yield (Tian et al, 2007). In 2013, the yield declined by 10%–20% in Anhui Province, China, because of high temperatures experienced during the rice flowering stage (Luo et al, 2015; Wang, 2016), and in 2017, spikelet fertility was also damaged by high temperatures in different regions (He et al, 2017). The flowering stage of single-season rice in the Yangtze River region is majorly in July and August, which typically have the highest temperatures of the entire year. According to Table 1, an average of 18.3 d suffered high temperatures above 35 oC during rice flowering periods at six represent places at Yangtze River region, and an average of 4.4 d was above 38 oC. Hefei City experienced much more high temperature days during the flowering period than the other rice production regions.

The key factor for heat stress is rice flowerng stage coincided with high temperature. In July and August of 2013, daily maximum temperature above 40 oC was observed for 23 d in Hangzhou, but because of the late flowering period in this region, the maximum temperature was lower in Hangzhou than in Hefei during rice flowering period, which results that rice yield was less affected by high temperature in Hangzhou. In 2017, rice flowering period in Hefei encountered with a period of high temperature above 38 oCduring 22 to 28 July, which results that spikelet fertility rate declined by 15%–25% in some rice cultivars (Fig. 1).

The occurrence of high temperatures is often accompanied by a decrease in rainfall. An overlap between high temperature and drought is often observed at the middle and lower reaches of Yangtze River region and the middle and eastern parts of Sichuan basin, which aggravate the yield loss by 43.9% compared with single high temperature stress (Jagadish et al, 2011; Rang et al, 2011). In recent years, extreme high temperatures occurred in north of China and heat stress occurs in the southern part of Henan Province in China (Fan et al, 2013).

Table 1. Duration of high temperature during flowering period of single-season rice at six represent locations of Yangtze River region in China.

The temperature data were from China Meteorological Data Sharing Service System (http://data.cma.cn/).

Fig. 1. Maximum temperatures in summer of Hangzhou and Hefei, China, in 2013 and 2017.

The flowering period is from 15 July to 15 August in Hefei and from 15 August to 15 September in Hangzhou, China.The temperature data were from China Meteorological Data Sharing Service System (http://data.cma.cn/).

Temperature indexes of heat stress at rice flowering stage

Temperature differences result in various degree of heat injury. Satake and Yoshida (1978) reported different heat tolerances among threerice varieties at 35 oC, and Matusi et al (2015) found that gradient high temperature treatment above 35 oC could accurately distinguish heat tolerance differences among ninerice cultivars. In 1980s, average maximum temperatures were 35 oC, and an average temperature above 30 oC was determined to be critical for determining rice spikelet sterility (Tan et al, 1985). Moreover, high temperature duration of 3–5 d is considered as mild heat injury, 5–7 d is moderate heat injury, and above 8 d is severe heat injury (Wei et al, 2008).

However, in recent years, temperatures in July and August at Yangtze River region of China have significantly increased. The number of days with temperatures above 35 oC has increased, while temperatures above 38 oC also occur more often. With the development of rice breeding in China, rice plant architecture and its yield formation characteristics has changed greatly, and the characters in heat resistance have changed in general. Hu (2013) evaluated the heat tolerance of 42 dominant single-season rice cultivars, and the results showed that no significant difference in spikelet fertility rate between 32 oC and35 oC is observed, however, spikelet fertility significantly declines at 38 oC compared with 32 oC and 35 oC (Fig. 2-A). Additionally, spikelet fertility presents a significant decline after treatment at 38 oC for 3 or more days (Fig. 2-B). These findings suggested that heat tolerance threshold of rice cultivar in production at present have increased compared to the traditional heat stress temperature indexes (35 oC), indicating that the temperature indexes of heat stress should be increased from 35 oC to 38 oC (Ministry of Agriculture of the People?s Republic of China, 2017).

Fig. 2. Spikelet fertility rates of single season rice cultivars under high temperature treatments.

A, Spikelet fertility rate of 42 dominant rice cultivars. B, Spikelet fertility rate of 5 dominant rice cultivars. Data are Mean ± SD (= 42 in A and 5 in B). Data are from Hu (2013). Different letters indicate significant difference at the 0.05 level.

For a single rice spikelet, spikelet opening to pollination last for 0.5–1.0 h, and the flowering period is the most sensitive to high temperatures. Little effects on spikelet fertility were observed following treatments with high temperature both before and after flowering (Fig. 3). Moreover, the higher temperature in spikelet, the worse heat damages on spikelet fertility (Das et al, 2014).

Effect of heat stress on spikelet fertility

Decline in spikelet number

Rice plants at the panicle initiation stage will encounter with high temperatures because of postponing sowing dates and unpredictable weather, which has a negative effect on spikelet formation and floral development. High temperatures inhibit spikelet differentiation, and aggravate spikelet degeneration, and reduce the number of spikelets (Jagadish et al, 2013; Wang Y L et al, 2015). In field conditions, daily maximum temperatures above 38 oC also aggravate spikelet degeneration, and the spikelet degeneration rate ofrice cultivars increases more quickly than that ofrice cultivars (Fig. 4). Wu et al (2017) found that high temperature inhibited spikelet formation is associated with the synthesis and decomposition of cytokines. Additionally, high temperatures lead to peroxide accumulation in the spikelets, which destroys cellular construction (Fu et al, 2015a) and reduces spikelet number. High temperatures also inhibit anther filling at the panicle initiation stage, which leads to a decline in pollen activity (Wang Y L et al, 2016).

Fig. 3. Relative spikelet fertility after high temperature treatment at 1 h before flowering (-1), flowering (0), and 1 h after flowering (+1).

Relative spikelet fertility rate (%) = Spikelet fertility rate under high temperature (38 oC) / Spikelet fertility rate under normal temperature (32 oC) × 100.Data are presented as Mean ± SD (= 5). Different letters indicate significant difference (< 0.05). Data are from Zhou (2014).

Fig. 4. Relationship between maximum temperature during panicle initiation stage and spikelet degeneration of Chujing 27 and Huanghuazhan.

Data are from Wang Y L et al (2016).

Inhibition of spikelet fertilization

Previous study showed that high temperatures result in spikelet sterility through decreasing pollen vitality, inhibiting anther dehiscence, and impeding pollen tube germination (Das et al, 2014; Cao et al, 2015; Coast et al, 2016; Zhang et al, 2018). Poor anther dehiscence and low pollen grain numbers on the stigma are the main factors for reducing the spikelet fertility rate under high temperature stress (Matsui and Omasa, 2002; Kobayashi et al, 2011; Zhao et al, 2016). Correlation analysis showed that anther dehiscence and the number of pollen grains on the stigma are significantly correlated with spikelet fertility rate (Fig. 5-A and -B), but no correlation is observed between spikelet fertility and pollen activity under high temperature conditions (Fig. 5-C).

Pollen activity is more influenced by high temperatures before spikelet flowering, which is the reason why no significant correlation is observed between fertilization rate and pollen viability in spikelet exposed to high temperatures. The decrease of pollen activity under high temperatures is induced by the stunted development of pollen mother cells and abnormal decomposition of the tapetum (Abiko et al, 2005; Oshino et al, 2007; Deng et al, 2010). Endo et al (2009) showed that a high temperature of 39 oC results in the insufficient accumulation of nutrients in pollen grains, leading to reduced pollen activity, but normal pollen morphology in response to the accumulation of peroxide and a decrease in carbon metabolism are observed (Muller and Rieu, 2016). Similarly, Cao (2014) reported that high temperatures inhibit the transport of sugars to pollen, which inhibits pollen filling and decreases its activity levels.

The anther dehiscence index in heat-resistant rice cultivars is higher than that in heat-sensitive ones, which can be explained by abnormal pollen dehydration and aberrant expansion (Matsui et al, 2000). Anther dehiscence is closely inversely related to the number of anther cell layers (Matsui and Omasa, 2002), while cumulative effects of high temperature duration positively affect the anther dehiscence index (Tian et al, 2010).

Pollen germinates after implantation on the stigma, and pollen tube elongation is associated with the activity of both pollen and stigma. Within spikelets that are opening, the osmotic regulation of pollen is destroyed when exposed to high temperatures for 10 min, followed by decreasing in soluble sugar, protein, and vitamin C contents, resulted in pollen tube elongation inhibition in stigma (Zhang et al, 2013; Coast et al, 2016; Zhang C X et al, 2016; Rieu et al, 2017). Pollen tube elongation last for 0.5 to 2.0 h after pollination. It was thought that high temperatures have little effect on vitality of the rice stigma (Satake and Yoshida, 1978), but Zhang G L et al (2014) showed that stigma viability was reduced by 35%–70% in high temperatures treatment of 37 oC. Zhang et al (2018) also reported that poor pollen tube elongation is induced by indole-3-acetic acid content deficiencies in the stigma under high temperatures during the flowering period. However, high temperature effects on rice stigma are still ambiguous, which need to be further studied.

Heat resistance characteristics of rice varieties

Rice variety innovation leads to heat resistance differences among different rice variety types. The Rice Production and Physiology Research Group in China National Rice Research Institute evaluated the heat tolerance of 116 rice varieties which were dominant planted in the middle and lower reaches of the Yangtze River region, and the results indicated thathybrid rice presents higher heat resistance compared toandrice in general, but there are individual differences among different varieties in the three types (Table 2). The difference in spikelet flowering habit is an important factor for the better heat resistance inrice than inrice with spikelet flowering generally before 12:00 inrice, and after 12:00 inrice (Fig. 6). The daily temperature is typically higher during the spikelet flowering period forrice, resulting in severe spikelet sterility, which suggests that early flowering cultivar type could reduce the high temperature damage.

Fig. 5. Relationship between rice spikelet fertility rate and floral characteristics under high temperature (38oC) at flowering period.

A, Correlation between anther dehiscence and spikelet fertility rate. B, Correlation between the number of pollen grains on the stigma and spikelet fertility rate. C, Correlation between pollen activity and spikelet fertility rate.Data are from Hu (2013).

Table 2. Response of spikelet fertility of,andhybrid rice varieties to high temperature at flowering stage.

Relative spikelet fertility rate (%) = Spikelet fertility rate under high temperature (38 oC) / Spikelet fertility rate under normal temperature (32 oC) × 100. Data are provided by Rice Production and Physiology Group ofChina National Rice Research Institute, Hangzhou, China.

Fig. 6. Daily spikelet flowering rate inand fiverice cultivars.

Spikelet anthesis rate (%) = No. of anthesis spikelet / Daily total spikelet anthesis × 100. Different letters indicate significant difference (< 0.05). Data are Mean ± SD (= 5). Data are provided by Rice Production and Physiology Group ofChina National Rice Research Institute, Hangzhou, China.

There are three types of heat resistance in rice, heat defense, heat avoidance and heat tolerance. Heat defense refers to the process of morphological growth regulation and leaf transpiration to reduce the panicle temperature and prevent damage from high temperature. Heat avoidance involves an adjustment of spikelet flowering time through short flowering duration and early flowering, which is a particularly favorable trait for heat-resistant rice cultivar breeding (Ishimaru et al, 2012; Bheemanahalli et al, 2017). Heat tolerance describes the maintenance of normal life activity under high temperatures. Li et al (2015) isolated and cloned a major quantitative trait locus,, in African wild rice that maintains the balance of cell metabolism and enables plants to survive under extreme high temperatures.

At the Yangtze River region of China,hybrid rice is the major rice type in production. Hu (2013) found that heat resistance of hybrid rice is associated with the female parent, while Fu et al (2015b) reported that the male parent contributes much more to heat resistance after evaluating the characteristics of restorer and maintainer lines commonly used in China. Thus, heat tolerance of hybrid rice is related to both female and male parents. Backcrossing is an effective means of improving heat resistance. For example, Meng et al (2012) used Chaoyou 1 as a recurrent parent to obtain a high yield and heat-resistant polymerization lines, and Zhang et al (2004) obtained pure lines with heat tolerance during the early grain filling stage, which can provide a reference for rice breeding at the flowering stage.

Prevention and management of heat stress during flowering stage

The selection of heat-resistant varieties can effectively reduce yield loss caused by heat stress. However, because of the instability of temperature, heat-resistant varieties still face heat stress risks if temperatures exceed the range of their tolerance. In addition, planting rice varieties with long growth duration to fit the rice flowering stage at late August can reduce the heat injury loss, especially in Anhui Province, where presents the most severe heat injury in rice production.

Rice heat stress monitor and warnings include weather prediction and model construction of rice spikelet fertilization in heat stress. Current rice heat stress warning is mainly based on meteorological temperature prediction, which is not closely related to the actual flowering stage of rice. Therefore, high temperature monitor and warning platforms should be based on the rice flowering stage and heat resistance characters of different rice production regions. This should then be combined with meteorological temperature forecasts for 7–10 d to provide real-time monitoring and early warning for heat damage.

The rice cropping system can be adjusted in two main ways to avoid high temperatures during the flowering stage. The first is to alter the sowing date of single- season rice, while the second is to convert single- season rice into double-season rice. In the southwest region of China, earlier rice sowing increases spikelet fertility by 5% (Xiong et al, 2016). In the middle and lower reaches of the Yangtze River, postponing the sowing date of single-season rice could avoid high temperatures by enabling rice to flowering during late August. However, in present, the growing area of direct seeding rice and machine transplanting rice has a great influence on the rice growth period. The frequency of high temperature at rice flowering stage gradually changes, therefore the sowing date of single- season rice should be adjusted according to the actual conditions, and at the same time, the effect of sowing date postponing of rice on the later crop growth should be considered.

Some single-season planting areas are gradually becoming suitable for double-season rice production under global warming conditions. Therefore, in the context of rising global temperatures, yield loss can be reduced by changing from single-season to double- season rice in suitable areas by reducing damage on spikelet fertilization of single-season rice. Although double-season rice production is threatened by high temperature and chilling injury at the ripening stage in early and late rice, respectively. Generally, the yield of double-season rice is relative higher.

Irrigation is the most effective real-time measure to reduce canopy temperature in rice field population (Zhang et al, 2008). However, timely irrigation is difficult in some regions due to high temperature weather usually accompanied with drought and irrigation infrastructure deficiency. Therefore, in the early stages of rice growth, it is important to maintain adequate field moisture.

Adjusting the rice plant population and microclimate in the field can also alleviate heat damage, and increasing row spacing between rice plants is beneficial for air circulation in paddy fields to reduce the canopy temperature during the flowering stage (Yan et al, 2007).

Spraying micronutrient fertilizers containing silicon, KH2PO4, ZnSO4, Na2SeO3or natural abscisic acid can increase the capacity of spikelet fertilization under high temperature conditions (Wu et al, 2013; Wang Q et al, 2015). The application of exogenous regulators also improves the pollination performance of anthers under high temperatures (Fahad et al, 2016). In rice production, exogenous regulation should combine the prevention and control of diseases and pests to improve production efficiency due to the higher cost of growth regulator spraying.

Prospects

The most effective way to solve the heat stress problem in rice production is to breed heat-resistant varieties. The genetic characteristics of heat-resistant rice varieties grown in China are not well studied because of various effects of high temperature on floral organ and spikelet fertilization progress. For further study, suitable varieties should be selected for growth in major regions of heat stress, and study should be conducted on exploring the genetic background and characteristics of heat-resistant varieties to accelerate the breeding progress.

Cultivation measures should be taken to prevent and avoid high temperatures during the rice flowering stage. High temperature warning systems should combine meteorological early warnings and breeding growth periods to predict catastrophic processes with rice cropping systems greatly changing. It is necessary to adjust the sowing date to avoid heat stress, and take account of other environmental factors at the same time to establish a cultivation system combining regional environment, cultivar selection, disaster warning and cultivation technology.

Acknowledgements

This study was financially supported by the National Key Research and Development Program of China (Grant No. 2017YFD0300409), the National Natural Science Foundation of China (Grant No. 31701374), the Special Fund for China Agricultural Research System (Grant Nos. CARS-01-22 and CARS-01-65), and the Basic Research Foundation of National Commonweal Research Institute of China (Grant No. 2017RG004-4).

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25 May 2018;

25 June 2018

Shi Qinghua (qinghua.shi@163.com); Zhu Defeng (cnrice@qq.com); Zhang Yuping (cnrrizyp@163.com)

Copyright ? 2019, China National Rice Research Institute. Hosting by Elsevier B V

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/)

Peer review under responsibility of China National Rice Research Institute

http://dx.doi.org/10.1016/j.rsci.2018.06.009

(Managing Editor: Li Guan)