Male Parent Plays More Important Role in Heat Tolerance in Three-Line Hybrid Rice

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1 Rice Science, 2015, 22(3): Copyright 2015, China National Rice Research Institute Hosting by Elsevier B.V. All rights reserved DOI: /S (14) Male Parent Plays More Important Role in Heat Tolerance in Three-Line Hybrid Rice FU Guan-fu 1, #, ZHANG Cai-xia 1, #, YANG Yong-jie 1, XIONG Jie 2, YANG Xue-qin 1, ZHANG Xiu-fu 1, JIN Qian-yu 1, TAO Long-xing 1 ( 1 National Key Laboratory of Rice Biology, China National Rice Research Institute, Hangzhou , China; 2 Zhejiang Science & Technology University; # These authors contributed equally to this work) Abstract: Ten F 1 combinations with their male and female parents were employed to evaluate their heat tolerance during the flowering and early grain filling stages. The rice plants were subjected to heat stress (39 C 43 C) for 1 15 d during flowering. Based on the heat stress index, heat tolerance was only observed in the F 1 combinations H2 (K22A R207), H3 (Bobai A R207) and H4 (Bobai A Minghui 63), whereas the others received above of heat stress index. Both parents of the tolerant combination (heat-tolerant heat-tolerant) possessed heat tolerance, whereas the susceptible combinations were crossed by heat-tolerant (sterile lines) heat-susceptible (restorer lines), heat-susceptible heat-tolerant, or heat-susceptible heat-susceptible parents. This result indicated that heat tolerance in rice was controlled by recessive genes. Thus, both parents should possess high temperature tolerance to develop heat-tolerant F 1 combinations. Furthermore, the heat stress index of F 1 combinations was significantly correlated with the heat stress index of restorer lines but not with the heat stress index of maintainer lines. This result suggested that male parents play a more important role in heat-tolerant combinations than female parents. Therefore, the heat susceptibility of the hybrid rice in China is mainly due to the wide application of low-heat-tolerant restorer lines with high yield in three-line hybrid rice breeding. Key words: hybrid rice; genetic correlation analysis; heat stress; heat tolerance The global climate is predicted to warm by an average of 2.5 C 5.8 C by the end of the 21 st century (IPCC, 2014) because of increased emissions of CO 2 and other heat-trapping greenhouse gases, such as methane, nitrous oxide, ozone and water vapor (Maraseni et al, 2009; Smith and Olesen, 2010). Recent climatic conditions wherein extreme high temperatures with a daily average of above 38 C and a daily maximum of 41 C frequently last for over 15 d have exposed most crops worldwide to heat stress at some stages of their life cycles. Heat stress has become a primary abiotic factor that limits the productivity of plants, especially summer-sown crops such as rice (Oryza sativa L.), which is grown in subtropical and tropical regions. Rice is an important cereal cultivated worldwide. Nearly half of the global population depends on rice, and a 0.6% 0.9% annual increase in rice production is needed until 2050 to support the demand of the growing population (Carriger and Vallee, 2007). Received: 8 August 2014; Accepted: 29 December 2014 Corresponding author: TAO Long-xing (lxtao@mail.hz.zj.cn) Therefore, breeding high-yielding rice varieties remains a priority to ensure food security. In this case, hybrid rice breeding may be a great option because of its heterosis. Compared with conventional inbred rice, modern hybrid rice exhibit higher seedling vigor, tillering rate, growth rate, and yield potential (Ling et al, 1994; Xie et al, 1996). In 2012, the super hybrid rice Yongyou 12 grown in Zhejiang Province, China attained a record grain yield of 15.4 t/hm 2 (Pan et al, 2013). Given the higher spikelet number, hybrids possess a large yield advantage over conventional cultivars (IR64) at 29 C and 35 C, however, this advantage disappears at 38 C (Madan et al, 2012). Temperature significantly influences seed-setting rate in all genotypes. In specific, the seed-setting rate of the hybrid decreases from 75% 80% at 29 C to below 20% at 38 C, whereas the conventional variety N22 can achieve 57% seed-setting rate at 38 C (Madan et al, 2012). Over 80% of hybrid rice is heat-susceptible (Zhou et al, 2009; Hu et al, 2012). Previous studies indicated that heat stress occurred at the flowering stage can significantly increase the

2 FU Guan-fu, et al. Heat Tolerance in Three-Line Hybrid Rice 117 spikelet sterility of rice due to the inhibition of anther dehiscence (Matsui et al, 2000, 2005), pollen germination (Song et al, 2001; Wassmann and Dobermann, 2007), and pollen tube elongation (Tang et al, 2008), especially for the heat-susceptible varieties. Heat tolerance in rice is quantitatively controlled by multiple genes and/or major genes, and several quantitative trait loci (QTLs) controlling heat tolerance have been detected in rice (Zhang et al, 2009; Jagadish et al, 2010; Cheng et al, 2012; Ye et al, 2012). In addition, heat shock proteins reportedly impart thermo-tolerance in rice (Yamanouchi et al, 2002; Wang et al, 2004; Hu et al, 2009; Shah et al, 2011). However, the heat susceptibility widely found in three-line hybrid rice combinations remains unexplained to date. Heat tolerance in three-line hybrid rice significantly correlates with their parents (Gong et al, 2008). Kuang et al (2002) reported that the three-line hybrid rice IIyou 7 exhibits a higher heat tolerance than Shanyou 63 because the male parent of the former displays higher heat tolerance than that of the latter. Similar results were observed by Li et al (2004), who suggested that heat tolerance in three-line hybrid rice mainly depends on the male parent. The female parent is also considered to influence the heat tolerance of three-line hybrid rice (Gong et al, 2008). However, the relationship in heat tolerance between the hybrid rice and their parents remains unclear, and none of the hybrid rice widely planted in China has been reported to have high and stable grain yield under heat stress during the flowering stage. Thus, in this study, four sterile lines and four restorer lines differing in heat tolerance (Fu et al, 2012) were selected to cross each other to clarify the relationships in heat tolerance between the hybrid rice and their parents, and to explain the heat susceptibility generally found in hybrid rice in China. Rice materials MATERIALS AND METHODS Four pairs of maintainer lines and their corresponding sterile lines K22B/K22A (heat-tolerant), Bobai B/ Bobai A (heat-tolerant), Neixiang 85B/Neixiang 85A (heat-susceptible), and Zhong 9B/Zhong 9A (heatsusceptible), and four restorer lines Minghui 63 (heat-tolerant), R207 (heat-tolerant), Chuannong 527 (heat-susceptible), and Milyang 46 (heat-susceptible) were selected. The rice maintainer lines were used to evaluate their heat tolerance, whereas their sterile lines were used to cross with the rice restorer lines to generate F 1 combinations. The following 10 F 1 combinations were obtained: H1 (Zhong 9A Minghui 63), H2 (Bobai A Minghui 63), H3 (K22A R207), H4 (Bobai A R207), H5 (K22A Chuannong 527), H6 (Neixiang 85A Chuannong 527), H7 (Zhong 9A Chuannong 527), H8 (K22A Milyang 46), H9 (Zhong 9A Milyang 46), and H10 (Bobai A Milyang 46). Plant cultivation and treatments This study was conducted at the experimental fields of China National Rice Research Institute, Hangzhou, during In 2009, four sterile lines and four restorer lines were crossed to generate F 1 seeds. These seeds were divided into two groups: one was planted in 2010, and the other was planted in The seeds were incubated in 0.01% methylene dithiocyanate at 30 C for 2 d, germinated in an incubator at 37 C for 1 d, and then directly sown in pots (30 cm 30 cm) each filled with 15 kg (dry weight) paddy soil. Each pot was fertilized with 15 g rapeseed cake. Rice plants were grown until the main stem flowering under natural condition in the net house. Then, the plants were subjected to heat stress for 15 d in the greenhouse with an automatic temperature control system to regulate the temperature at 39 C 43 C from 9:00 AM to 15:00 PM. After the respective temperature treatments, the plants were returned to the net house (natural condition) with daily mean temperatures of 28.8 C and 30.4 C, relative humidities of 70.5% and 66.7%, and illumination intensities of 5.51 and 6.12 klux as measured with a meteorological automatic recorder (ZDR-34, Hangzhou, China) until maturity in 2010 and 2011, respectively. The plants were sampled to determine the number of panicle per plant, number of grains per panicle, 1000-grain weight, and seed-setting rate. Then, the heat stress index (HSI) was calculated as (seed-setting rate of control seed-setting rate of heat stress) / seed-setting rate of control (Tao et al, 2008; Fu et al, 2012). Statistical analysis Data were presented as the means of three replicates (if not stated otherwise) and analyzed by one-way analysis of variance (ANOVA) using SPSS version Least significant differences were conducted to compare significant effects at the 5% level. The

3 118 Rice Science, Vol. 22, No. 3, 2015 Table 1. Effects of heat stress on grain yield components of maintainer and restorer lines at flowering. Line Variety No. of panicle per plant No. of grains per panicle Seed-setting rate (%) 1000-grain weight Control Heat stress Control Heat stress Control Heat stress Control Heat stress HSI Maintainer line K22B 11.7 a 9.4 b a b a b a b Bobai B 15.7 a 12.2 b a b a b a a Neixiang 85B 13.0 a 8.2 b a b a b a b Zhong 9B 12.3 a 13.1 a a a a 7.43 b a b Restorer line Minghui a 13.7 a a b a b a b R a 8.0 b a b a b a 9.79 b Chuannong a 14.7 b a b a 0.38 b a b Milyang a 15.7 b a a a 5.82 b a b HSI, Heat stress index. Different letters indicate statistically significant differences between control and heat stress in the same variety (P < 0.05). correlation between variables was analyzed by linear regression. RESULTS Heat stress at the flowering stage decreased the number of panicle per plant, number of grains per panicle, 1000-grain weight, and seed setting rate in both maintainer and restorer lines compared with the respective control (Table 1). However, the panicle number slightly increased under heat stress (Table 1). Heat stress decreased the seed-setting rates by 53.89% and 74.95% in the maintainer and restorer lines compared with the control, respectively. This result indicated that the rice maintainer lines had higher heat tolerance than the restorer lines. The HSI values of the rice maintainer lines K22B and Bobai B were and , respectively, whereas those of the heat-tolerant restorer lines Minghui 63 and R207 were and , respectively. Heat stress decreased the average number of panicle per plant, number of grains per panicle, 1000-grain weight, and seed-setting rate of the F 1 hybrid rice combinations at the flowering stage compared with the control, in particular, heat stress decreased the seed-setting rate by 48.06% (Table 2). The lowest HSI values of , , and were observed in H2, H3 and H4, respectively, whereas the other F 1 combinations had HSI values above The highest HSI was recorded in H7, followed by H5. Genetic correlation analysis in heat tolerance was conducted between the F 1 combinations and their parents. Results indicated significant relationships between the HSI of F 1 combinations and the seed-setting rate of restorer lines under control and heat stress, with correlation coefficients of * and *, respectively; however, such significant relationships were not observed in the maintainer lines (Fig. 1). A highly significant relationship was observed between the HSI of the F 1 combinations and the seed-setting Table 2. Effects of heat stress on grain yield components of F 1 combinations at flowering. Combination No. of panicle per plant No. of grains per panicle 1000-grain weight (g) Seed-setting rate (%) Control Heat stress Control Heat stress Control Heat stress Control Heat stress HSI H a 14.5 a a a a b 75.1 a 37.4 b H b 16.3 a a a a a 83.8 a 74.9 b H a 18.1 b a b a b 74.7 a 67.8 b H a 14.6 a b a a b 71.8 a 59.9 b H a 15.8 a a b a b 58.4 a 14.9 b H a 11.3 a a b a a 66.1 a 26.2 b H a 9.3 b a b a a 76.4 a 14.8 b H a 13.1 a a a a a 62.1 a 21.9 b H a 6.6 b a a a a 65.0 a 26.4 b H a 8.1 b a a a b 52.2 a 18.0 b H1, Zhong 9A Minghui 63; H2, Bobai A Minghui 63; H3, K22A R207; H4, Bobai A R207; H5, K22A Chuannong 527; H6, Neixiang 85A Chuannong 527; H7, Zhong 9A Chuannong 527; H8, K22A Milyang 46; H9, Zhong 9A Milyang 46; H10, Bobai A Milyang 46; HSI, Heat stress index. Data in this table were showed as means of six replications within two years during Different letters above columns indicate statistically significant differences between control and heat stress in the same cultivar (P < 0.05).

4 FU Guan-fu, et al. Heat Tolerance in Three-Line Hybrid Rice 119 Fig. 1. Relationships between heat stress indices of F 1 combinations with seed-setting rates of maintainer lines, restorer lines and F 1 combinations under control and heat stress, respectively. A and B, Relationships between F 1 combination and maintainer lines under control and heat stress, respectively; C and D, Relationships between F 1 combinations and restorer lines under control and heat stress, respectively; E and F, Relationships between the heat stress index and seed-setting rates of F 1 combinations under control and heat stress, respectively. * indicates the relationships are significant. rates under heat stress but not under the control. Unexpectedly, the HSI values of the F 1 combinations significantly correlated with those of the restorer lines but not with those of the maintainer lines (Fig. 2). DISCUSSION Heterosis or hybrid vigor refers to the superior performance of hybrids relative to their parents. Utilization of heterosis has tremendously increased the global productivity of many crops because of the success in breeding elite hybrids. It often exhibits wider adaptability that enhances resistance to both biotic and abiotic stress (e.g., heat) relative to inbreds (Goff and Zhang, 2013). Heat-tolerant rice varieties can be attained through three-line hybrid breeding, but both parents (i.e., male and female) should possess heat tolerance. In the Heat stress index Seed-setting rate (%) Fig. 2. Relationships in heat stress index between the F 1 combinations and their parents. A, Relationship between F 1 combinations and maintainer lines; B, Relationship between F 1 combinations and restorer lines. * indicated the relationship was remarkable.

5 120 Rice Science, Vol. 22, No. 3, 2015 present study, heat tolerance was only observed in the F 1 combinations H2, H3 and H4, with below 20% decrease in seed-setting rate under heat stress; by contrast, the other combinations were susceptible to heat stress during flowering, with above 50% decrease in seed-setting rate (Table 1). These tolerant combinations and their parents possessed heat tolerance (heat-tolerant heat-tolerant), whereas the sensitive hybrid rice combinations were derived from crosses of heat-tolerant (sterile lines) heat-susceptible (restorer lines), heat-susceptible heat-tolerant, or heat-susceptible heat-susceptible parents. This result suggests that the heat tolerance of rice is controlled by recessive genes. Similar findings were previously reported (Hall, 1993; Ye et al, 2012). The former considered that recessive gene provides tolerance to the heat-induced suppression of floral bud development, whereas the latter identified one heat-tolerant allele of qhtsf4.1 that is controlled by a recessive gene. The HSI values of the combinations H6, H7 and H9 crossed by heat-susceptible heat-susceptible parents were , and , respectively, whereas those of the combinations H8 and H10 crossed by heat-susceptible heat-tolerant parents were and , respectively (Table 2). This result further indicates that recessive genes confer heat tolerance in rice. Many QTLs and major genes confer heat tolerance in crops (Cao et al, 2003; Chen et al, 2008; Zhang et al, 2008; Zhang et al, 2009; Jagadish et al, 2010; Mason et al, 2010; Xiao et al, 2011; Chauhan et al, 2012; Wu and Jinn, 2012), but only a few of these genes are recessive. Heat tolerance in both cowpea varieties (Prima and TVu4552) is reportedly controlled by a single dominant gene (Marfo and Hall, 1992), and heat sensitivity in snap bean is purportedly to be conferred by a single recessive gene derived from a susceptible variety (Rainey and Griffiths, 2005). However, many recessive genes have been reported to confer resistance to other abiotic and biotic stress, such as frost (Galiba et al, 1995), stripe rust (Milus and Line, 1986), spring black stem (Kamphuis et al, 2008), rice blast (Fukuoka and Okuno, 2001) and Magnaporthe oryzae (He et al, 2012; Wang et al, 2014). Heat tolerance in three-line hybrid rice is significantly related to their both parents, but which parent plays the dominant role remains controversial. Hu et al (2012) analyzed the origin of combinations conferring heat tolerance and found that most hybrid combinations derived from the same female parent showed similar heat resistance, they, therefore, concluded that the female parent plays a more important role than the male parent in the heat tolerance of hybrid rice. By contrast, the present results demonstrated that the male parent may play a more important role than the female parent in the heat tolerance of hybrid rice. The HSI values of the F 1 combinations were significantly correlated with the seed-setting rate and HSI of the restorer lines but not with those of the maintainer lines (Figs. 1 and 2). Furthermore, the HSI values of the F 1 combinations with the male parent conferring heat tolerance were lower than those with the female parent possessing heat tolerance; in specific, the HSI of H1 crossed by Zhong 9A and Minghui 63 (heat-susceptible heat-tolerant) was , whereas those of H5, H8 and H10 crossed by heat-tolerant female and heat-susceptible male were , and , respectively (Tables 1 3). Similar observations were previously reported (Li et al, 2004; Tao et al, 2008, 2009). Thus, rice restorer lines with low heat tolerance may be responsible for the thermal sensitivity generally showed in three-line hybrid rice in China. This deduction agrees with our previous results that most rice maintainer lines are thermal tolerant and semi-thermal tolerant, whereas 25 rice restorer lines have HSI values above across 26 varieties (Fu et al, 2012). Only one of the 15 rice maintainer lines was heat-susceptible, whereas 19 restorer lines were susceptible, with more than 90% decrease in seed-setting rate at flowering under heat stress. This result suggests that the rice maintainer lines have higher heat tolerance than the restorer lines (Fu et al, 2012). These rice restorer lines with high yields have been widely applied in three-line hybrid rice breeding in China and their low heat tolerance would limit the success in heat tolerant rice breeding. The heat susceptibility widely shown in three-line hybrid rice may be related to heterosis. Breeding super-high-yielding rice variety by utilizing the strong heterosis between indica and japonica is imperative to support the demand of the growing population. Hybrid rice combinations could attain high grain yields. For example, the super hybrid rice Yongyou 12 received a grain yield of 15.4 t/hm 2 in 2012 (Pan et al, 2013). However, these combinations exhibit low resistance to abiotic and biotic stress. Zhou et al (2009) reported that the indica hybrid rice combinations with pure

6 FU Guan-fu, et al. Heat Tolerance in Three-Line Hybrid Rice 121 indica male parent show higher heat tolerance than those with permeability japonica male parent. In conclusion, thermo-tolerance is a complex cellular feature that depends on the function of many biochemical pathways and on the current physiological status of cells and the whole plant. This feature involves numerous genes/proteins, but the functions and interactions of these genes/proteins in conferring stress tolerance have not yet to be investigated. Nevertheless, the present study indicated that breeding heat-resistant varieties required both parents rather than single parent to possess heat tolerance. In heat tolerance breeding, significantly improving heat tolerance via better parent heterosis through the simple utilization of heterosis is impractical. Therefore, emphasis should be given to the directional selection of heat-tolerant parents. ACKNOWLEDGEMENTS This work was funded by the National Natural Science Foundation of China (Grant Nos and ), the Research Grant of China National Rice Research Institute (Grant No. 2012RG004-3), the Special Fund for Agro-Scientific Research in the Public Interest (Grant No ), and the National System of Rice Industry (Grant No. CARS-01-27). We thank to Prof. WANG Xi for his useful suggestion on this paper. The authors are grateful to Prof. ZHU Xudong for his assistance in rice hybridization. REFERENCES Cao L Y, Zhao J G, Zhan X D, Li D L, He L B, Cheng S H Mapping QTLs for heat tolerance and correlation between heat tolerance and photosynthetic rate in rice. Chin J Rice Sci, 17(3): (in Chinese with English abstract) Carriger S, Vallee D More crop per drop. Rice Today, 6(2): Chauhan H, Khurana N, Nijhavan A, Khurana J P, Khurana P The wheat chloroplastic small heat shock protein (shsp26) is involved in seed maturation and germination and imparts tolerance to heat stress. 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