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Varietal difference in the response of rice chalkiness to temperature during ripening phase across different sowing dates
Field Crops Research 151 (2013) 85–91
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Varietal difference in the response of rice chalkiness to temperature during ripening phase across different sowing dates Chang Chen a , Jianliang Huang a , Liyang Zhu a , Farooq Shah b , Lixiao Nie a , Kehui Cui a , Shaobing Peng a,∗ a National Key Laboratory of Crop Genetic Improvement, MOA Key Laboratory of Crop Ecophysiology and Farming System in the Middle Reaches of the Yangtze River, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, Hubei 430070, China b Department of Agriculture, Abdul Wali Khan University, Mardan, 23200 Pakhtunkhwa, Pakistan
a r t i c l e
i n f o
Article history: Received 6 May 2013 Received in revised form 18 July 2013 Accepted 18 July 2013 Keywords: Chalkiness Grain quality Heading date Rice variety Temperature
a b s t r a c t Chalkiness, which is highly influenced by high temperature during ripening phase, is one of key factors in determining rice quality and commercial value. This study was conducted to determine varietal differences in chalkiness and in the response of chalkiness to temperature during ripening phase. We evaluated the chalkiness of 42 and 7 varieties with a wide range of genetic background across different sowing dates under field conditions in 2009 and 2010, respectively. Image analysis was used to measure chalky grains and chalkiness was calculated as the percentage of chalky area to projected grain area. A wide range in chalkiness was observed among the tested varieties. These varieties also demonstrated large difference in the response of chalkiness to temperature during ripening phase. Overall, chalkiness was positively correlated with temperature during ripening phase and temperature during second week after heading had the closest correlation with chalkiness. In some varieties such as Dongtingwanxian, Chengnongshuijing, and IR64, their chalkiness was sensitive to temperature and minimum chalkiness could be achieved through optimum sowing date. For these varieties, crop management practice is effective for improving appearance quality. Other varieties such as Yangdao6, Gu154, and Huanghuazhan had low level of chalkiness regardless of sowing dates. These varieties with low and stable chalkiness could be considered as parents in the breeding program for developing new rice varieties with improved appearance quality especially for the future warming environment. © 2013 Elsevier B.V. All rights reserved.
1. Introduction Rice is the staple food for more than half of the world’s population (Maclean et al., 2002). Increasing grain yield and improving grain quality are equally important for meeting the demands of rice consumers. However, projected increase in global temperature will reduce not only grain yield but also grain quality (Peng et al., 2004; IPCC, 2007; Fitzgerald and Resurreccion, 2009). Rice quality includes appearance, milling, cooking, eating, and nutritional properties (Koutroubas et al., 2004). Chalkiness of the grains is one of key factors in determining rice quality and commercial value (Yoshioka et al., 2007). Although the preference of rice grain characteristics varies with consumer groups in different countries, translucent kernels without chalkiness are preferred by the majority of rice consumers worldwide (Juliano and Villareal, 1993). Chalkiness is defined as the opaque parts in the endosperm and can be categorized into white-cored, white-belly, milky-white,
∗ Corresponding author. Tel.: +86 27 8728 8668; fax: +86 27 8728 8380. E-mail address: [email protected] (S. Peng). 0378-4290/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.fcr.2013.07.016
white-back, and white-based types depending on the site of the chalky part in the grain (Tashiro and Wardlaw, 1991). Appearance quality is largely determined by chalkiness (Lisle et al., 2000). Chalkiness also affects milling quality by reducing grain resistance to forces applied during the milling process, causing grain breakage and consequently a decrease in head rice percentage (Lisle et al., 2000; Counce et al., 2005). This is because chalky endosperms are filled with loosely packed, round and large compound starch granules, while translucent endosperms have tightly packed, polyhedral and small single starch granules (Singh et al., 2006). Wang et al. (2012) reported that the varietal difference in chalkiness explained the difference in head rice percentage among varieties. Furthermore, palatability of the cooked products is reduced by chalkiness because cracks develop readily when chalky grains is steamed or boiled (Cheng et al., 2005). Chalkiness is directly associated with inferior cooking and eating qualities and is a major cause of processing and financial losses (Fitzgerald and Resurreccion, 2009). The physiological causes of the chalkiness are hypothesized to be an insufficient substrate supply to the developing endosperm, reduced ability to synthesize starch in the endosperm, the degradation of starch by ␣-amylase during ripening, slower growth
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of starch granules, or different structures of starch that interfere with granular organization (Sato and Inaba, 1976a,b; Yamakawa et al., 2007; Tsukaguchi and Iida, 2008; Fitzgerald and Resurreccion, 2009). Chalkiness is influenced by varieties, environmental conditions, and crop management practices (Tan et al., 2000; Fitzgerald et al., 2009). Rice chalkiness is a complex quantitative trait controlled by polygenes and readily influenced by environment (Tan et al., 2000). Several QTLs have been found to control the chalkiness of rice grains (Tan et al., 2000; Guo et al., 2011). Varietal differences in chalkiness were reported in several studies (Wang et al., 2006; Yamakawa et al., 2007; Ambardekar et al., 2011). Among environmental factors, temperature has the largest influence on chalkiness (Cheng and Zhong, 2001). Formation of chalky grains is greatly enhanced by high temperature during ripening phase (Tashiro and Wardlaw, 1991; Yamakawa et al., 2007), which is recently occurring more frequently due to global warming (Wakamatsu et al., 2007). Therefore, grain chalkiness caused by high temperature stress will become a global problem for rice production in the near future (Ishimaru et al., 2009). Recent research has shown that elevated nighttime temperature increased chalkiness (Fitzgerald and Resurreccion, 2009; Ambardekar et al., 2011). Unfavorably warm weather during the grain filling period results in reduced enzymatic activity related to grain filling, increased respiratory consumption of assimilation products, disturbed water balance, decreased sink activity of glumous flowers, and increased loosely-packed starch granules (Inaba and Sato, 1976; Sato and Inaba, 1976a,b; Tashiro and Wardlaw, 1991). Chalkiness is also affected by crop management practices such as nitrogen fertilization (Qiao et al., 2011) and water management (Hayashi et al., 2011). Many studies have been conducted about the chalkiness of rice grains. However, most of them were carried out for understanding the physiological and genetic mechanism underlying the chalky formation under normal or high temperature (Tan et al., 2000; Yamakawa et al., 2007; Fitzgerald and Resurreccion, 2009; Zhang et al., 2009; Zhou et al., 2009). These studies were often conducted under controlled-environment conditions with a few varieties. In this study, we evaluated the chalkiness of 42 and 7 varieties with a wide range of genetic background across different sowing dates under field conditions in 2009 and 2010, respectively. The objectives were to determine varietal differences in chalkiness and in the response of chalkiness to temperature during ripening phase and to determine which stage of grain filling was most sensitive to temperature for chalky formation.
2. Materials and methods Field experiments were conducted in Dajin Township (29◦ 51 N, 115◦ 53 E), Wuxue County, Hubei Province, China, during the ricegrowing season from May to October in 2009 and 2010. Soil in the field for 2009 experiment has the following properties: pH 5.01, 30.1 g kg−1 organic matter, 1.39 g kg−1 total N, 5.92 mg kg−1 available P, and 46.3 mg kg−1 available K. Soil in the field for 2010 experiment has the following properties: pH 5.70, 21.9 g kg−1 organic matter, 1.77 g kg−1 total N, 8.75 mg kg−1 available P, and 66.1 mg kg−1 available K. Monthly mean temperature from May to October were 22.5, 28.5, 30.0, 29.5, 25.8, 21.0 ◦ C in 2009, and were 22.2, 25.2, 29.3, 30.1, 25.0, 17.7 ◦ C in 2010, respectively. In 2009, four sowing dates were used and 42 varieties were arranged in three replications within each sowing date. In 2010, six sowing dates were used and seven varieties were arranged in three replications within each sowing date. Sowing dates were May 5, May 16, May 26, and June 4 in 2009, and April 27, May 7, May 15, May 26, June 6, and June 15 in 2010. Forty-two varieties used in 2009 were from rice core collection. Among the 42 varieties, 12 varieties were japonica and the rest were indica. Most varieties
were from China except for IR64, IR661-1, and Gu154 (from IRRI with original name of IR837-36-1), IRAT109 (from IITA), and Gui630 (from Gunaya). Based on the varietal difference in the response of chalkiness to temperature in 2009, seven varieties were selected for the 2010 experiment. Another selection criterion was the similarity in growth duration among the varieties. The seven varieties were indica, and five of them were from China and two from IRRI. Seedlings were raised in wet seedbed in both years. Seedlings were transplanted with a hill spacing of 0.133 m × 0.267 m and with 2–3 seedlings per hill. Seedling age was 20–25 days in 2009 and 25–33 days in 2010. Seedling age was variable across the sowing dates in order to reduce the differences in seedling size at transplanting. Phosphorus in the form of calcium superphosphate (40 kg P ha−1 ) and zinc in the form of zinc sulfate heptahydrate (5 kg Zn ha−1 ) were applied and incorporated in the field 1 day before transplanting. Potassium in the form of potassium chloride (100 kg K ha−1 ) was split equally at basal and panicle initiation. Nitrogen in the form of urea (150 kg N ha−1 ) was split-applied: 40% at basal, 30% at mid-tillering, and 30% at panicle initiation in 2009. Total N rate was 135 kg ha−1 with the split application of 50% at basal, 20% at mid-tillering, and 30% at panicle initiation in 2010. The field was kept 5–10 cm water depth from 3 days after transplanting to 7 days before maturity. Pests, diseases, birds, and weeds were intensively controlled for avoiding yield losses. Other crop management practices followed the local recommendation to achieve high grain yield. Plant samples were taken from each plot at crop maturity for the measurements of various traits. Grains were threshed and filled grains were separated from unfilled grains and debris using an air blower. Two subsamples of air-dried and filled grain each at 26 g were taken from each plot for the measurement of chalkiness. Rough rice was de-husked using a husker (SY88-TH, BRIC, Korea). From each subsample, 10 g brown rice was taken for milling using a Miller (Pearlest, Kett, Japan), and then head rice was divided from broken rice using a separator (JFQS-13*20, China). Chalkiness was evaluated following the method of Yoshioka et al. (2007) with some modification. A digital image was created by placing all head rice of each subsample on the scanner (Epson Expression 1680 Professional, Epson, America) with a white fraction back board, which increased the contrast between chalky and translucent parts in the images. Digital images were analyzed using an image analyzing software (Image J, the National Institutes of Health, USA). With the tool of “Threshold Color” in the software, we determined two threshold values of brightness pass in hue-saturation-brightness color model to separate chalky, translucent and background parts. Then the areas of pixel in chalky and translucent parts were measured, and chalkiness was calculated as the percentage of chalky area to projected grain area. Air temperature was obtained from the temperature data loggers (HOBO H08-032-08, Onset Computer Corp., USA). Daily mean temperature was calculated as the average of daily minimum and maximum temperature. Correlation analysis was done to determine the relationship between chalkiness and average daily mean temperature during different periods of ripening phase.
3. Results Air temperature during rice growing seasons in 2009 and 2010 followed normal pattern which increased from May to June, reached a peak in July and August, and declined from September to October (Fig. 1). Monthly mean temperature in June and October was greater in 2009 than in 2010. The difference in temperature between the two years was relatively small in May, July, August, and September. In general, 2010 was cooler than 2009. Heading dates
C. Chen et al. / Field Crops Research 151 (2013) 85–91
87
100
40
Chengnongshuijing IR64 Zhenxian232
Dongtingwanxian
2009 2010
80
30
Chalkiness (%)
Daily mean temperature (ºC )
35
25
Yangdao2 Xiangwanxian1 Huangsiguizhan
60
40
20 20
15
10 May 1
Jun 1
Jul 1
Aug 1
Sep 1
Oct 1
0 Jul 10
Oct 31
Jul 20
Jul 30
Aug 29
Sep 8
Fig. 2. Response of chalkiness to heading dates in seven varieties grown in Wuxue, Hubei, China, in 2009. The chalkiness of these seven varieties was sensitive to heading dates and reached low level (less than 15%) when heading occurred after August 20.
Chengnongshuijing, IR64, and Zhenxian232. Nanjing11 and Aimi belonged to Group 2 while Gu154 and Yangdao6 were in Group 3. Nanjing11 changed from Group 3 in 2009 to Group 2 in 2010, and the rest six varieties remained the same grouping across the two years. Chalkiness of varieties in Groups 1 and 2 was sensitive to heading dates, and minimum chalkiness was observed when heading occurred between August 10 and 25 (Fig. 5). However, the minimum chalkiness was less than 10% in Group 1 while it was greater than 30% in Group 2. Chalkiness of varieties in Group 3 was relatively insensitive to heading dates, especially when heading was after August 9. Correlation between chalkiness and average daily mean temperature during the ripening phase from heading to maturity was analyzed for each variety in 2009 (Table 1). Among the 42 varieties, the correlation coefficients of 13 varieties between chalkiness
100
80
Chalkiness (%)
spreaded over two months from July 12 to September 12 due to a wide range in sowing dates. There was substantial variation in temperature over this two-month period and subsequent one month so that tested varieties could experience different temperature during their ripening phase. Variation in chalkiness across four sowing dates was listed in Table 1 for the 42 varieties in 2009. Large variation in chalkiness was observed among varieties and across sowing dates. Average chalkiness ranged from 1.3% for Huanghuazhan to 78.4% for Sankecun. The difference between maximum and minimum chalkiness across the four sowing dates ranged from 2.0% for Huanghuazhan to 52.8% for Dongtingwanxian. Based on the response of chalkiness to sowing dates and minimum chalkiness, 42 varieties were divided into three groups. In Groups 1 and 2, the difference between maximum and minimum chalkiness across the four sowing dates was greater than 15%, while it was below 15% in Group 3. The minimum chalkiness of Groups 1 and 2 was smaller and greater than 15%, respectively. Using these criteria, 7, 19, and 16 varieties were classified into Groups 1, 2, and 3, respectively. The chalkiness response of varieties in Group 1 to heading dates was depicted in Fig. 2. In general, the chalkiness of these seven varieties was sensitive to heading dates and chalkiness decreased with delayed heading dates for this group. Chalkiness reached low level (less than 15%) when heading occurred after August 20. Chalkiness of varieties in Group 2 was also sensitive to heading dates (Fig. 3). In this group, three varieties (Guangluai4, JinghuB, and Aijiaonante) had short growth duration. In these three varieties, minimum chalkiness was observed with heading date around July 20. For the rest varieties, minimum chalkiness generally occurred with the latest heading dates. Furthermore, the 19 varieties in Group 2 had a minimum chalkiness greater than 15% across the four heading dates. Chalkiness of varieties in Group 3 was relatively insensitive to heading dates (Fig. 4). Among this group, nine varieties had chalkiness greater than 35% and seven varieties had chalkiness below 20% across the four heading dates. Huanghuazhan demonstrated most stable and the lowest chalkiness among the 42 varieties. Variation in chalkiness among varieties and across sowing dates was also observed in 2010 (Table 2). Based on criteria used in 2009, the seven varieties were divided into the three groups, which had different responses of chalkiness to heading dates and minimum chalkiness. Group 1 included three varieties, which were
Aug 19
Heading date
Date Fig. 1. Daily mean air temperature from May to October in 2009 and 2010.
Aug 9
Guihuahuang Bawangbian1 Aituogu151 Guangluai4 HR5 Chengdouai3 PeiC122
Aimi Geshandao Guichao2 Gui630 Xugunuo Qingsiai16B
Zhenshan97B IRAT109 Teqing JinghuB Aijiaonante Zaoshunonghu6
Aug 9
Aug 29
60
40
20
0 Jul 10
Jul 20
Jul 30
Aug 19
Sep 8
Heading date Fig. 3. Response of chalkiness to heading dates in 19 varieties grown in Wuxue, Hubei, China, in 2009. The chalkiness of these 19 varieties was sensitive to heading dates but remained at high level (greater than 15%).
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Table 1 Maximum, minimum, mean, and range of chalkiness (%) for 42 varieties across four sowing dates in Wuxue, Hubei, China, in 2009. Groupa
Variety
Typeb
Maximum
Minimum
Mean
Range
1
Dongtingwanxian Yangdao2 Xiangwanxian1 Huangsiguizhan Chengnongshuijing IR64 Zhenxian232
I I I I I I I
57.8 47.1 43.1 41.2 32.1 26.4 22.6
5.0 8.9 12.4 6.3 4.2 7.1 3.1
27.4 24.2 23.3 29.2 18.3 16.3 13.8
52.8 38.3 30.7 34.9 27.9 19.3 19.5
0.90 0.76 0.85 0.93 0.86 0.96* 0.97*
2
Guihuahuang Bawangbian1 Aituogu151 Guangluai4 HR5 Chengdouai3 PeiC122 Aimi Geshandao Guichao2 Gui630 Xugunuo Qingsiai16B Zhenshan97B IRAT109 Teqing JinghuB Aijiaonante Zaoshunonghu6
I J I I I I J I J I I J I I J I J I J
71.3 66.8 65.8 65.6 62.9 62.8 62.7 60.6 59.8 59.7 59.6 58.9 58.7 57.0 55.3 53.8 51.2 50.1 37.5
50.4 33.0 35.2 39.1 47.6 35.9 31.2 34.8 37.7 38.2 44.4 36.9 39.6 32.7 31.7 23.0 24.6 18.4 17.4
60.4 50.8 51.3 58.0 54.4 49.2 45.5 49.6 50.8 48.4 52.1 47.5 49.4 46.6 42.4 39.7 37.5 39.4 31.2
20.9 33.8 30.6 26.5 15.3 26.9 31.5 25.8 22.0 21.5 15.2 22.1 19.0 24.3 23.5 30.8 26.6 31.7 20.0
0.95* 0.97* 0.96* −0.22 0.88 −0.07 0.90 0.94 0.98* 0.90 0.17 0.95* 0.87 0.20 0.31 0.93 0.96* −0.35 0.76
3
Sankecun Taishannuo 88B Huke3 Aimakang Gongju73 IR661-1 Nanjing11 Liusha1 LimingB Dangyu5 JWR221 Zhonghua8 Yangdao6 Gu154 Huanghuazhan
I I I I I J I I I J J J J I I I
80.0 79.3 77.6 76.9 70.0 64.8 59.0 55.6 46.6 18.3 17.5 16.9 14.3 12.6 11.5 2.3
77.5 75.3 73.7 63.6 61.2 56.8 48.6 45.0 37.8 15.4 5.3 4.2 2.9 3.5 1.1 0.3
78.4 77.7 75.5 69.9 66.7 60.6 53.6 49.8 42.5 16.7 11.6 8.8 7.8 7.0 6.0 1.3
2.6 4.0 3.9 13.2 8.8 8.1 10.4 10.7 8.8 2.8 12.2 12.8 11.4 9.1 10.4 2.0
−0.04 0.99** 0.82 0.95* 0.76 0.63 0.29 0.77 0.25 −0.89 0.97* 0.83 0.95* 0.94 0.99* 0.67 0.50**
All a b c * **
rc
Groups 1 and 2 had larger ranges in chalkiness across sowing dates than Group 3. Group 2 had higher minimum chalkiness than Group 1. I = indica, J = japonica. Correlation coefficients between chalkiness and average daily mean temperature from heading to maturity. P < 0.05. P < 0.01.
and temperature were statistically significant. Eighteen varieties had correlation coefficients between 0.70 and 0.94, which were not statistically significant due to small sample size (n = 4). When pooled data of the 42 varieties were used, statistically significant correlation was found between chalkiness and temperature (r = 0.50, p < 0.01). Similar correlation between chalkiness and
temperature was observed in 2010 when the correlation analysis was done across the seven varieties (Table 3). The relationship between chalkiness and temperature was further analyzed using average daily mean temperature during different periods of ripening phase in 2010 because more data points were available (i.e. six sowing dates in 2010 vs. four in 2009). For individual varieties,
Table 2 Maximum, minimum, mean, and range of chalkiness (%) for seven varieties across six sowing dates in Wuxue, Hubei, China, in 2010. Groupa
Variety
Typeb
Maximum
Mean
Range
1
Chengnongshuijing IR64 Zhenxian232
I I I
51.8 40.2 27.4
5.6 4.1 4.3
19.1 16.9 10.4
46.2 36.1 23.1
2
Nanjing11 Aimi
I I
71.4 65.8
34.6 34.5
55.7 47.7
36.8 31.4
3
Gu154 Yangdao6
I I
17.8 14.7
2.8 5.5
7.3 8.3
15.0 9.2
a b
Minimum
Groups 1 and 2 had larger ranges in chalkiness across sowing dates than Group 3. Group 2 had higher minimum chalkiness than Group 1. I = indica.
C. Chen et al. / Field Crops Research 151 (2013) 85–91
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Table 3 Correlation coefficients (r) between chalkiness and average daily mean temperature during different periods of ripening phase in Wuxue, Hubei, China, in 2010. Group
1 WAHa
Variety
2 WAH *
3 WAH
4 WAH
Ripeningb
0.17 0.32 −0.15
0.63 0.50 0.27
1
Chengnongshuijing IR64 Zhenxian232
0.66 0.52 0.20
0.84 0.78 0.68
0.44 0.34 0.03
2
Nanjing11 Aimi
0.73 0.73
0.95** 0.96**
0.89* 0.74
3
Gu154 Yangdao6
0.19 0.07
0.36 0.51
0.23 0.30
0.32*
0.56**
0.48**
All a b * **
0.19 0.05 −0.09 −0.12 0.30
0.93** 0.63 0.16 0.22 0.48**
Weeks after heading. From heading to maturity. P < 0.05. P < 0.01.
100
Sankecun Taishannuo 88B Huke3 Aimakang Gongju73 IR661-1 Nanjing11
Chalkiness (%)
80
Liushan1 LimingB Dangyu5 JWR221
4. Discussion
Zhonghua8 Yangdao6 Gu154 Huanghuazhan
60
40
20
0
Heading date Fig. 4. Response of chalkiness to heading dates in 16 varieties grown in Wuxue, Hubei, China, in 2009. The chalkiness of these 16 varieties was insensitive to heading dates.
correlation coefficient between chalkiness and average daily mean temperature during second week after heading was the largest compared with other periods in ripening phase. When data from all seven varieties were pooled, the second week after heading had the closest correlation between chalkiness and temperature, followed by third week, first week, and fourth week after heading.
Wide range in chalkiness was observed among tested varieties. Varietal difference in chalkiness was fairly stable across the two years since the average chalkiness of the seven varieties in 2010 was similar to that in 2009 (Tables 1 and 2). Yangdao6 and Gu154 had low chalkiness, whereas Aimi and Nanjing 11 had high chalkiness in the two years. The data from this experiment and our previous studies suggest that Huanghuazhan has minimum chalkiness across a wide range of growing conditions although it was tested only in 2009 in this study. Varietal differences in chalkiness were reported previously. American variety Lemont and IRRI-bred variety IR22 had no chalky grains while Chinese variety Guangluai4 was opposite across a wide range of environmental conditions (Wang et al., 2006). Among japonica varieties from Japan, Koshiibuki and Tentakaku had less chalky grains even when they were exposed to high temperature, whereas Hatsuboshi and Sasanishiki produced severely chalky grains (Yamakawa et al., 2007). In general, japonica rice varieties have less chalkiness than indica rice varieties (Juliano, 1992; Fitzgerald et al., 2009; Ishimaru et al., 2009). However, our study did not show clear difference in chalkiness between japonica and indica rice varieties. This could be due to large genotype by environment interaction on chalkiness because chalkiness is under genetic control, but its extent can be affected by weather conditions experienced during the grain filling period (Yamakawa et al., 2007). The varietal difference in the response of chalkiness to temperature was evaluated by changing sowing dates so that a variety reached heading at different dates and experienced different temperature during grain filling. The advantage of this method over controlled environment such as growth chambers is that it represents actual field growing conditions (Ambardekar et al., 2011).
100
Chalkiness (%)
80
Chengnongshuijing IR64 Zhengxian232
Nanjing11 Aimi
Gu154 Yangdao6
60
40
20
0 Jul 20 Jul 30 Aug 9 Aug 19 Aug 29 Sep 8 Jul 20 Jul 30
Aug 9 Aug 19 Aug 29 Sep 8 Jul 20 Jul 30
Aug 9 Aug 19 Aug 29 Sep 8 Sep 18
Heading date Fig. 5. Response of chalkiness to heading dates in seven varieties grown in Wuxue, Hubei, China, in 2010.
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Furthermore, this method allows the evaluation of large number of varieties at the same time. The shortcoming of this system for studying temperature response is the potential confounding factors such as solar radiation and relative humidity. However, temperature during grain filling period is the most important environmental factor that influences rice chalkiness (Cheng and Zhong, 2001). The 42 varieties demonstrated large difference in their response to temperature during ripening phase for chalky grain formation. Three groups of varieties were formed based on the response of chalkiness to temperature and minimum chalkiness. Groups 1 and 2 were sensitive to temperature, whereas Group 3 was insensitive to temperature. Group 1 had lower minimum chalkiness than Group 2 across sowing dates. The grouping was fairly stable across the two years for the seven varieties tested in both years, except for Nanjing 11, which belonged to Group 3 in 2009 and Group 2 in 2010. Dongtingwanxian, Chengnongshuijing, and IR64 were representatives of Group 1. Interestingly, Group 1 had no japonica varieties. For varieties in Group 1, minimum chalkiness could be achieved through optimum sowing date. Bawangbian1, Aimi, Guichao2 and Zhenshan97B were the typical varieties of Group 2. Changing sowing date might result in a reduction in chalkiness for varieties in Group 2, but they never reached the minimum chalkiness that is desirable for rice consumers. Crop management practice could be more effective for improving appearance quality for varieties in Group 1 than these in Group 2. Some varieties in Group 3 such as Sankecun and Taishannuo maintained a high level of chalkiness, whereas others such as Yangdao6, Gu154, and Huanghuazhan had a low level of chalkiness regardless of sowing dates. Both indica and japonica varieties existed in Groups 2 and 3. These varieties with low and stable chalkiness in Group 3 could be considered as parents in the breeding program for developing new rice varieties with improved appearance quality especially for the future warming environment. Correlation between chalkiness and average daily temperature during ripening phase was observed in majority of tested varieties, although correlation coefficients in some varieties were not statistically significant due to small sample size (n = 4). When polled data from all varieties were used, statistically significant correlation was observed between chalkiness and temperature during ripening phase in both years. There was no clear difference among the three groups in the relationship between chalkiness and temperature. Close correlation between chalkiness and temperature was found even for some varieties in Group 3 with low and stable chalkiness across different heading dates. Various studies have shown that high temperature during specific stages of grain development tends to increase the occurrence of chalk in rice grains more than other stages (Lisle et al., 2000). Chalkiness is frequently found when the average temperature during the 20 days after heading exceeds 27 ◦ C (Wakamatsu et al., 2007). The chalky grains were most evident when the high temperature commenced four days after heading (Tashiro and Wardlaw, 1991). Tashiro and Wardlaw (1991) also stated that the time when the rice plant is exposed to high temperature stress during ripening determines the part with chalkiness in the grain. Eight-day exposure of rice plants to high temperature starting 12 days after heading induced mostly the milky-white grains while exposure for 8 days starting 16 days after heading formed more white-back grains. Ambardekar et al. (2011) reported that the effects of elevated nighttime temperature on chalkiness were incurred during certain stages of grain filling period and were variety-specific. In general, R6 and R7 grain-filling stages, which correspond to milk and soft dough stages, were most sensitive to warm nights for chalky grain formation. Chalkiness of medium-grain varieties (Bengal and Jupiter) was less sensitive to high night temperature than long-grain varieties (LaGrue, XL723, and Wells). In our study, we found that second week after heading had the closest correlation
between chalkiness and temperature, followed by third week, first week, and fourth week after heading. It is fairly consistent between our study and previous studies in the finding of the specific stage of grain development that is more sensitive to temperature for chalky grain formation. Identification of sensitive stage of grain filling provides important information in determining optimal sowing and heading dates for reducing chalkiness of rice varieties through crop management practice. Acknowledgements This work was supported by the Program for Changjiang Scholars and Innovative Research Team in University of China (IRT1247), the Special Fund for Agro-scientific Research in the Public Interest of China from the Ministry of Agriculture (No. 201203096), and the Key Technology Program R&D of Chinese Ministry of Science and Technology (No. 2012BAD04B12). References Ambardekar, A.A., Siebenmorgen, T.J., Counce, P.A., Lanning, S.B., Mauromoustakos, A., 2011. 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Guo, T., Liu, X., Wan, X., Weng, J., Liu, S., Liu, X., Chen, M., Li, J., Su, N., Wu, F., Cheng, Z., Guo, X., Lei, C., Wang, J., Jiang, L., Wan, J., 2011. Identification of a stable quantitative trait locus for percentage grains with white chalkiness in rice (Oryza sativa L). J. Integr. Plant Biol. 53, 598–607. Hayashi, M., Sugiura, K., Kuno, C., Endo, I., Tanaka, Y., Yamauchi, A., 2011. Reduction of rice chalky grain by deep and permanent irrigation method. Effect on growth and grain quality of rice. Plant Prod. Sci. 14, 282–290. Inaba, K., Sato, K., 1976. High temperature injury of ripening in rice plant. VI. Enzyme activities of kernel as influenced by high temperature. Jpn. J. Crop Sci. 45, 162–167. IPCC, 2007. Climate change 2007: synthesis report. In: Summary for Policymakers. http://www.ipcc.ch/pdf/assessment–report/ar4/syr/ar4 syr spm.pdf Ishimaru, T., Horigane, A.K., Ida, M., Iwasawa, N., San-oh, Y.A., Nakazono, M., Nishizawa, N.K., Masumura, T., Kondo, M., Yoshida, M., 2009. Formation of grain chalkiness and changes in water distribution in developing rice caryopses grown under high-temperature stress. J. Cereal Sci. 50, 166–174. Juliano, B.O., 1992. Structure, chemistry, and function of the rice grain and its fractions. Cereal Foods World 37, 772–774. Juliano, B.O., Villareal, C.P., 1993. Grain Quality Evaluation of World Rices. IRRI, International Rice Research Institute, pp. 1–205. Koutroubas, S.D., Mazzini, F., Pons, B., Ntanos, D.A., 2004. Grain quality variation and relationships with morpho-physiological traits in rice (Oryza sativa L) genetic resources in Europe. Field Crops Res. 86, 115–130. Lisle, A.J., Martin, M., Fitzgerald, M.A., 2000. Chalky and translucent rice grains differ in starch composition and structure and cooking properties. Cereal Chem. 77, 627–632. Maclean, J.L., Dawe, D.C., Hardy, B., Hettel, G.P., 2002. Rice Almanac, 3rd ed. Interna˜ Philippines, pp. 1–253. tional Rice Research Institute (IRRI), Los Banos, Peng, S., Huang, J., Sheehy, J., Laza, R.C., Visperas, R.M., Zhong, X., Centeno, G.S., Khush, G.S., Cassman, K.G., 2004. Rice yields decline with higher night temperature from global warming. Proc. Natl. Acad. Sci. USA 101, 9971–9975. Qiao, J., Liu, Z., Deng, S., Ning, H., Yang, X., Lin, Z., Li, G., Wang, Q., Wang, S., Ding, Y., 2011. Occurrence of perfect and imperfect grains of six japonica rice cultivars as affected by nitrogen fertilization. Plant Soil 349, 191–202. Sato, K., Inaba, K., 1976a. High temperature injury of ripening in rice plant. IV. Effect of high temperature on 14 C-assimilation and translocation at an early ripening period. Jpn. J. Crop Sci. 45, 151–155. Sato, K., Inaba, K., 1976b. High temperature injury of ripening in rice plant. V. On the early decline of assimilate storing ability of grains at high temperature. Jpn. J. Crop Sci. 45, 156–161. 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Varietal difference in the response of rice chalkiness to temperature during ripening phase across different sowing dates Chang Chen a , Jianliang Huang a , Liyang Zhu a , Farooq Shah b , Lixiao Nie a , Kehui Cui a , Shaobing Peng a,∗ a National Key Laboratory of Crop Genetic Improvement, MOA Key Laboratory of Crop Ecophysiology and Farming System in the Middle Reaches of the Yangtze River, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, Hubei 430070, China b Department of Agriculture, Abdul Wali Khan University, Mardan, 23200 Pakhtunkhwa, Pakistan
a r t i c l e
i n f o
Article history: Received 6 May 2013 Received in revised form 18 July 2013 Accepted 18 July 2013 Keywords: Chalkiness Grain quality Heading date Rice variety Temperature
a b s t r a c t Chalkiness, which is highly influenced by high temperature during ripening phase, is one of key factors in determining rice quality and commercial value. This study was conducted to determine varietal differences in chalkiness and in the response of chalkiness to temperature during ripening phase. We evaluated the chalkiness of 42 and 7 varieties with a wide range of genetic background across different sowing dates under field conditions in 2009 and 2010, respectively. Image analysis was used to measure chalky grains and chalkiness was calculated as the percentage of chalky area to projected grain area. A wide range in chalkiness was observed among the tested varieties. These varieties also demonstrated large difference in the response of chalkiness to temperature during ripening phase. Overall, chalkiness was positively correlated with temperature during ripening phase and temperature during second week after heading had the closest correlation with chalkiness. In some varieties such as Dongtingwanxian, Chengnongshuijing, and IR64, their chalkiness was sensitive to temperature and minimum chalkiness could be achieved through optimum sowing date. For these varieties, crop management practice is effective for improving appearance quality. Other varieties such as Yangdao6, Gu154, and Huanghuazhan had low level of chalkiness regardless of sowing dates. These varieties with low and stable chalkiness could be considered as parents in the breeding program for developing new rice varieties with improved appearance quality especially for the future warming environment. © 2013 Elsevier B.V. All rights reserved.
1. Introduction Rice is the staple food for more than half of the world’s population (Maclean et al., 2002). Increasing grain yield and improving grain quality are equally important for meeting the demands of rice consumers. However, projected increase in global temperature will reduce not only grain yield but also grain quality (Peng et al., 2004; IPCC, 2007; Fitzgerald and Resurreccion, 2009). Rice quality includes appearance, milling, cooking, eating, and nutritional properties (Koutroubas et al., 2004). Chalkiness of the grains is one of key factors in determining rice quality and commercial value (Yoshioka et al., 2007). Although the preference of rice grain characteristics varies with consumer groups in different countries, translucent kernels without chalkiness are preferred by the majority of rice consumers worldwide (Juliano and Villareal, 1993). Chalkiness is defined as the opaque parts in the endosperm and can be categorized into white-cored, white-belly, milky-white,
∗ Corresponding author. Tel.: +86 27 8728 8668; fax: +86 27 8728 8380. E-mail address: [email protected] (S. Peng). 0378-4290/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.fcr.2013.07.016
white-back, and white-based types depending on the site of the chalky part in the grain (Tashiro and Wardlaw, 1991). Appearance quality is largely determined by chalkiness (Lisle et al., 2000). Chalkiness also affects milling quality by reducing grain resistance to forces applied during the milling process, causing grain breakage and consequently a decrease in head rice percentage (Lisle et al., 2000; Counce et al., 2005). This is because chalky endosperms are filled with loosely packed, round and large compound starch granules, while translucent endosperms have tightly packed, polyhedral and small single starch granules (Singh et al., 2006). Wang et al. (2012) reported that the varietal difference in chalkiness explained the difference in head rice percentage among varieties. Furthermore, palatability of the cooked products is reduced by chalkiness because cracks develop readily when chalky grains is steamed or boiled (Cheng et al., 2005). Chalkiness is directly associated with inferior cooking and eating qualities and is a major cause of processing and financial losses (Fitzgerald and Resurreccion, 2009). The physiological causes of the chalkiness are hypothesized to be an insufficient substrate supply to the developing endosperm, reduced ability to synthesize starch in the endosperm, the degradation of starch by ␣-amylase during ripening, slower growth
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of starch granules, or different structures of starch that interfere with granular organization (Sato and Inaba, 1976a,b; Yamakawa et al., 2007; Tsukaguchi and Iida, 2008; Fitzgerald and Resurreccion, 2009). Chalkiness is influenced by varieties, environmental conditions, and crop management practices (Tan et al., 2000; Fitzgerald et al., 2009). Rice chalkiness is a complex quantitative trait controlled by polygenes and readily influenced by environment (Tan et al., 2000). Several QTLs have been found to control the chalkiness of rice grains (Tan et al., 2000; Guo et al., 2011). Varietal differences in chalkiness were reported in several studies (Wang et al., 2006; Yamakawa et al., 2007; Ambardekar et al., 2011). Among environmental factors, temperature has the largest influence on chalkiness (Cheng and Zhong, 2001). Formation of chalky grains is greatly enhanced by high temperature during ripening phase (Tashiro and Wardlaw, 1991; Yamakawa et al., 2007), which is recently occurring more frequently due to global warming (Wakamatsu et al., 2007). Therefore, grain chalkiness caused by high temperature stress will become a global problem for rice production in the near future (Ishimaru et al., 2009). Recent research has shown that elevated nighttime temperature increased chalkiness (Fitzgerald and Resurreccion, 2009; Ambardekar et al., 2011). Unfavorably warm weather during the grain filling period results in reduced enzymatic activity related to grain filling, increased respiratory consumption of assimilation products, disturbed water balance, decreased sink activity of glumous flowers, and increased loosely-packed starch granules (Inaba and Sato, 1976; Sato and Inaba, 1976a,b; Tashiro and Wardlaw, 1991). Chalkiness is also affected by crop management practices such as nitrogen fertilization (Qiao et al., 2011) and water management (Hayashi et al., 2011). Many studies have been conducted about the chalkiness of rice grains. However, most of them were carried out for understanding the physiological and genetic mechanism underlying the chalky formation under normal or high temperature (Tan et al., 2000; Yamakawa et al., 2007; Fitzgerald and Resurreccion, 2009; Zhang et al., 2009; Zhou et al., 2009). These studies were often conducted under controlled-environment conditions with a few varieties. In this study, we evaluated the chalkiness of 42 and 7 varieties with a wide range of genetic background across different sowing dates under field conditions in 2009 and 2010, respectively. The objectives were to determine varietal differences in chalkiness and in the response of chalkiness to temperature during ripening phase and to determine which stage of grain filling was most sensitive to temperature for chalky formation.
2. Materials and methods Field experiments were conducted in Dajin Township (29◦ 51 N, 115◦ 53 E), Wuxue County, Hubei Province, China, during the ricegrowing season from May to October in 2009 and 2010. Soil in the field for 2009 experiment has the following properties: pH 5.01, 30.1 g kg−1 organic matter, 1.39 g kg−1 total N, 5.92 mg kg−1 available P, and 46.3 mg kg−1 available K. Soil in the field for 2010 experiment has the following properties: pH 5.70, 21.9 g kg−1 organic matter, 1.77 g kg−1 total N, 8.75 mg kg−1 available P, and 66.1 mg kg−1 available K. Monthly mean temperature from May to October were 22.5, 28.5, 30.0, 29.5, 25.8, 21.0 ◦ C in 2009, and were 22.2, 25.2, 29.3, 30.1, 25.0, 17.7 ◦ C in 2010, respectively. In 2009, four sowing dates were used and 42 varieties were arranged in three replications within each sowing date. In 2010, six sowing dates were used and seven varieties were arranged in three replications within each sowing date. Sowing dates were May 5, May 16, May 26, and June 4 in 2009, and April 27, May 7, May 15, May 26, June 6, and June 15 in 2010. Forty-two varieties used in 2009 were from rice core collection. Among the 42 varieties, 12 varieties were japonica and the rest were indica. Most varieties
were from China except for IR64, IR661-1, and Gu154 (from IRRI with original name of IR837-36-1), IRAT109 (from IITA), and Gui630 (from Gunaya). Based on the varietal difference in the response of chalkiness to temperature in 2009, seven varieties were selected for the 2010 experiment. Another selection criterion was the similarity in growth duration among the varieties. The seven varieties were indica, and five of them were from China and two from IRRI. Seedlings were raised in wet seedbed in both years. Seedlings were transplanted with a hill spacing of 0.133 m × 0.267 m and with 2–3 seedlings per hill. Seedling age was 20–25 days in 2009 and 25–33 days in 2010. Seedling age was variable across the sowing dates in order to reduce the differences in seedling size at transplanting. Phosphorus in the form of calcium superphosphate (40 kg P ha−1 ) and zinc in the form of zinc sulfate heptahydrate (5 kg Zn ha−1 ) were applied and incorporated in the field 1 day before transplanting. Potassium in the form of potassium chloride (100 kg K ha−1 ) was split equally at basal and panicle initiation. Nitrogen in the form of urea (150 kg N ha−1 ) was split-applied: 40% at basal, 30% at mid-tillering, and 30% at panicle initiation in 2009. Total N rate was 135 kg ha−1 with the split application of 50% at basal, 20% at mid-tillering, and 30% at panicle initiation in 2010. The field was kept 5–10 cm water depth from 3 days after transplanting to 7 days before maturity. Pests, diseases, birds, and weeds were intensively controlled for avoiding yield losses. Other crop management practices followed the local recommendation to achieve high grain yield. Plant samples were taken from each plot at crop maturity for the measurements of various traits. Grains were threshed and filled grains were separated from unfilled grains and debris using an air blower. Two subsamples of air-dried and filled grain each at 26 g were taken from each plot for the measurement of chalkiness. Rough rice was de-husked using a husker (SY88-TH, BRIC, Korea). From each subsample, 10 g brown rice was taken for milling using a Miller (Pearlest, Kett, Japan), and then head rice was divided from broken rice using a separator (JFQS-13*20, China). Chalkiness was evaluated following the method of Yoshioka et al. (2007) with some modification. A digital image was created by placing all head rice of each subsample on the scanner (Epson Expression 1680 Professional, Epson, America) with a white fraction back board, which increased the contrast between chalky and translucent parts in the images. Digital images were analyzed using an image analyzing software (Image J, the National Institutes of Health, USA). With the tool of “Threshold Color” in the software, we determined two threshold values of brightness pass in hue-saturation-brightness color model to separate chalky, translucent and background parts. Then the areas of pixel in chalky and translucent parts were measured, and chalkiness was calculated as the percentage of chalky area to projected grain area. Air temperature was obtained from the temperature data loggers (HOBO H08-032-08, Onset Computer Corp., USA). Daily mean temperature was calculated as the average of daily minimum and maximum temperature. Correlation analysis was done to determine the relationship between chalkiness and average daily mean temperature during different periods of ripening phase.
3. Results Air temperature during rice growing seasons in 2009 and 2010 followed normal pattern which increased from May to June, reached a peak in July and August, and declined from September to October (Fig. 1). Monthly mean temperature in June and October was greater in 2009 than in 2010. The difference in temperature between the two years was relatively small in May, July, August, and September. In general, 2010 was cooler than 2009. Heading dates
C. Chen et al. / Field Crops Research 151 (2013) 85–91
87
100
40
Chengnongshuijing IR64 Zhenxian232
Dongtingwanxian
2009 2010
80
30
Chalkiness (%)
Daily mean temperature (ºC )
35
25
Yangdao2 Xiangwanxian1 Huangsiguizhan
60
40
20 20
15
10 May 1
Jun 1
Jul 1
Aug 1
Sep 1
Oct 1
0 Jul 10
Oct 31
Jul 20
Jul 30
Aug 29
Sep 8
Fig. 2. Response of chalkiness to heading dates in seven varieties grown in Wuxue, Hubei, China, in 2009. The chalkiness of these seven varieties was sensitive to heading dates and reached low level (less than 15%) when heading occurred after August 20.
Chengnongshuijing, IR64, and Zhenxian232. Nanjing11 and Aimi belonged to Group 2 while Gu154 and Yangdao6 were in Group 3. Nanjing11 changed from Group 3 in 2009 to Group 2 in 2010, and the rest six varieties remained the same grouping across the two years. Chalkiness of varieties in Groups 1 and 2 was sensitive to heading dates, and minimum chalkiness was observed when heading occurred between August 10 and 25 (Fig. 5). However, the minimum chalkiness was less than 10% in Group 1 while it was greater than 30% in Group 2. Chalkiness of varieties in Group 3 was relatively insensitive to heading dates, especially when heading was after August 9. Correlation between chalkiness and average daily mean temperature during the ripening phase from heading to maturity was analyzed for each variety in 2009 (Table 1). Among the 42 varieties, the correlation coefficients of 13 varieties between chalkiness
100
80
Chalkiness (%)
spreaded over two months from July 12 to September 12 due to a wide range in sowing dates. There was substantial variation in temperature over this two-month period and subsequent one month so that tested varieties could experience different temperature during their ripening phase. Variation in chalkiness across four sowing dates was listed in Table 1 for the 42 varieties in 2009. Large variation in chalkiness was observed among varieties and across sowing dates. Average chalkiness ranged from 1.3% for Huanghuazhan to 78.4% for Sankecun. The difference between maximum and minimum chalkiness across the four sowing dates ranged from 2.0% for Huanghuazhan to 52.8% for Dongtingwanxian. Based on the response of chalkiness to sowing dates and minimum chalkiness, 42 varieties were divided into three groups. In Groups 1 and 2, the difference between maximum and minimum chalkiness across the four sowing dates was greater than 15%, while it was below 15% in Group 3. The minimum chalkiness of Groups 1 and 2 was smaller and greater than 15%, respectively. Using these criteria, 7, 19, and 16 varieties were classified into Groups 1, 2, and 3, respectively. The chalkiness response of varieties in Group 1 to heading dates was depicted in Fig. 2. In general, the chalkiness of these seven varieties was sensitive to heading dates and chalkiness decreased with delayed heading dates for this group. Chalkiness reached low level (less than 15%) when heading occurred after August 20. Chalkiness of varieties in Group 2 was also sensitive to heading dates (Fig. 3). In this group, three varieties (Guangluai4, JinghuB, and Aijiaonante) had short growth duration. In these three varieties, minimum chalkiness was observed with heading date around July 20. For the rest varieties, minimum chalkiness generally occurred with the latest heading dates. Furthermore, the 19 varieties in Group 2 had a minimum chalkiness greater than 15% across the four heading dates. Chalkiness of varieties in Group 3 was relatively insensitive to heading dates (Fig. 4). Among this group, nine varieties had chalkiness greater than 35% and seven varieties had chalkiness below 20% across the four heading dates. Huanghuazhan demonstrated most stable and the lowest chalkiness among the 42 varieties. Variation in chalkiness among varieties and across sowing dates was also observed in 2010 (Table 2). Based on criteria used in 2009, the seven varieties were divided into the three groups, which had different responses of chalkiness to heading dates and minimum chalkiness. Group 1 included three varieties, which were
Aug 19
Heading date
Date Fig. 1. Daily mean air temperature from May to October in 2009 and 2010.
Aug 9
Guihuahuang Bawangbian1 Aituogu151 Guangluai4 HR5 Chengdouai3 PeiC122
Aimi Geshandao Guichao2 Gui630 Xugunuo Qingsiai16B
Zhenshan97B IRAT109 Teqing JinghuB Aijiaonante Zaoshunonghu6
Aug 9
Aug 29
60
40
20
0 Jul 10
Jul 20
Jul 30
Aug 19
Sep 8
Heading date Fig. 3. Response of chalkiness to heading dates in 19 varieties grown in Wuxue, Hubei, China, in 2009. The chalkiness of these 19 varieties was sensitive to heading dates but remained at high level (greater than 15%).
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Table 1 Maximum, minimum, mean, and range of chalkiness (%) for 42 varieties across four sowing dates in Wuxue, Hubei, China, in 2009. Groupa
Variety
Typeb
Maximum
Minimum
Mean
Range
1
Dongtingwanxian Yangdao2 Xiangwanxian1 Huangsiguizhan Chengnongshuijing IR64 Zhenxian232
I I I I I I I
57.8 47.1 43.1 41.2 32.1 26.4 22.6
5.0 8.9 12.4 6.3 4.2 7.1 3.1
27.4 24.2 23.3 29.2 18.3 16.3 13.8
52.8 38.3 30.7 34.9 27.9 19.3 19.5
0.90 0.76 0.85 0.93 0.86 0.96* 0.97*
2
Guihuahuang Bawangbian1 Aituogu151 Guangluai4 HR5 Chengdouai3 PeiC122 Aimi Geshandao Guichao2 Gui630 Xugunuo Qingsiai16B Zhenshan97B IRAT109 Teqing JinghuB Aijiaonante Zaoshunonghu6
I J I I I I J I J I I J I I J I J I J
71.3 66.8 65.8 65.6 62.9 62.8 62.7 60.6 59.8 59.7 59.6 58.9 58.7 57.0 55.3 53.8 51.2 50.1 37.5
50.4 33.0 35.2 39.1 47.6 35.9 31.2 34.8 37.7 38.2 44.4 36.9 39.6 32.7 31.7 23.0 24.6 18.4 17.4
60.4 50.8 51.3 58.0 54.4 49.2 45.5 49.6 50.8 48.4 52.1 47.5 49.4 46.6 42.4 39.7 37.5 39.4 31.2
20.9 33.8 30.6 26.5 15.3 26.9 31.5 25.8 22.0 21.5 15.2 22.1 19.0 24.3 23.5 30.8 26.6 31.7 20.0
0.95* 0.97* 0.96* −0.22 0.88 −0.07 0.90 0.94 0.98* 0.90 0.17 0.95* 0.87 0.20 0.31 0.93 0.96* −0.35 0.76
3
Sankecun Taishannuo 88B Huke3 Aimakang Gongju73 IR661-1 Nanjing11 Liusha1 LimingB Dangyu5 JWR221 Zhonghua8 Yangdao6 Gu154 Huanghuazhan
I I I I I J I I I J J J J I I I
80.0 79.3 77.6 76.9 70.0 64.8 59.0 55.6 46.6 18.3 17.5 16.9 14.3 12.6 11.5 2.3
77.5 75.3 73.7 63.6 61.2 56.8 48.6 45.0 37.8 15.4 5.3 4.2 2.9 3.5 1.1 0.3
78.4 77.7 75.5 69.9 66.7 60.6 53.6 49.8 42.5 16.7 11.6 8.8 7.8 7.0 6.0 1.3
2.6 4.0 3.9 13.2 8.8 8.1 10.4 10.7 8.8 2.8 12.2 12.8 11.4 9.1 10.4 2.0
−0.04 0.99** 0.82 0.95* 0.76 0.63 0.29 0.77 0.25 −0.89 0.97* 0.83 0.95* 0.94 0.99* 0.67 0.50**
All a b c * **
rc
Groups 1 and 2 had larger ranges in chalkiness across sowing dates than Group 3. Group 2 had higher minimum chalkiness than Group 1. I = indica, J = japonica. Correlation coefficients between chalkiness and average daily mean temperature from heading to maturity. P < 0.05. P < 0.01.
and temperature were statistically significant. Eighteen varieties had correlation coefficients between 0.70 and 0.94, which were not statistically significant due to small sample size (n = 4). When pooled data of the 42 varieties were used, statistically significant correlation was found between chalkiness and temperature (r = 0.50, p < 0.01). Similar correlation between chalkiness and
temperature was observed in 2010 when the correlation analysis was done across the seven varieties (Table 3). The relationship between chalkiness and temperature was further analyzed using average daily mean temperature during different periods of ripening phase in 2010 because more data points were available (i.e. six sowing dates in 2010 vs. four in 2009). For individual varieties,
Table 2 Maximum, minimum, mean, and range of chalkiness (%) for seven varieties across six sowing dates in Wuxue, Hubei, China, in 2010. Groupa
Variety
Typeb
Maximum
Mean
Range
1
Chengnongshuijing IR64 Zhenxian232
I I I
51.8 40.2 27.4
5.6 4.1 4.3
19.1 16.9 10.4
46.2 36.1 23.1
2
Nanjing11 Aimi
I I
71.4 65.8
34.6 34.5
55.7 47.7
36.8 31.4
3
Gu154 Yangdao6
I I
17.8 14.7
2.8 5.5
7.3 8.3
15.0 9.2
a b
Minimum
Groups 1 and 2 had larger ranges in chalkiness across sowing dates than Group 3. Group 2 had higher minimum chalkiness than Group 1. I = indica.
C. Chen et al. / Field Crops Research 151 (2013) 85–91
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Table 3 Correlation coefficients (r) between chalkiness and average daily mean temperature during different periods of ripening phase in Wuxue, Hubei, China, in 2010. Group
1 WAHa
Variety
2 WAH *
3 WAH
4 WAH
Ripeningb
0.17 0.32 −0.15
0.63 0.50 0.27
1
Chengnongshuijing IR64 Zhenxian232
0.66 0.52 0.20
0.84 0.78 0.68
0.44 0.34 0.03
2
Nanjing11 Aimi
0.73 0.73
0.95** 0.96**
0.89* 0.74
3
Gu154 Yangdao6
0.19 0.07
0.36 0.51
0.23 0.30
0.32*
0.56**
0.48**
All a b * **
0.19 0.05 −0.09 −0.12 0.30
0.93** 0.63 0.16 0.22 0.48**
Weeks after heading. From heading to maturity. P < 0.05. P < 0.01.
100
Sankecun Taishannuo 88B Huke3 Aimakang Gongju73 IR661-1 Nanjing11
Chalkiness (%)
80
Liushan1 LimingB Dangyu5 JWR221
4. Discussion
Zhonghua8 Yangdao6 Gu154 Huanghuazhan
60
40
20
0
Heading date Fig. 4. Response of chalkiness to heading dates in 16 varieties grown in Wuxue, Hubei, China, in 2009. The chalkiness of these 16 varieties was insensitive to heading dates.
correlation coefficient between chalkiness and average daily mean temperature during second week after heading was the largest compared with other periods in ripening phase. When data from all seven varieties were pooled, the second week after heading had the closest correlation between chalkiness and temperature, followed by third week, first week, and fourth week after heading.
Wide range in chalkiness was observed among tested varieties. Varietal difference in chalkiness was fairly stable across the two years since the average chalkiness of the seven varieties in 2010 was similar to that in 2009 (Tables 1 and 2). Yangdao6 and Gu154 had low chalkiness, whereas Aimi and Nanjing 11 had high chalkiness in the two years. The data from this experiment and our previous studies suggest that Huanghuazhan has minimum chalkiness across a wide range of growing conditions although it was tested only in 2009 in this study. Varietal differences in chalkiness were reported previously. American variety Lemont and IRRI-bred variety IR22 had no chalky grains while Chinese variety Guangluai4 was opposite across a wide range of environmental conditions (Wang et al., 2006). Among japonica varieties from Japan, Koshiibuki and Tentakaku had less chalky grains even when they were exposed to high temperature, whereas Hatsuboshi and Sasanishiki produced severely chalky grains (Yamakawa et al., 2007). In general, japonica rice varieties have less chalkiness than indica rice varieties (Juliano, 1992; Fitzgerald et al., 2009; Ishimaru et al., 2009). However, our study did not show clear difference in chalkiness between japonica and indica rice varieties. This could be due to large genotype by environment interaction on chalkiness because chalkiness is under genetic control, but its extent can be affected by weather conditions experienced during the grain filling period (Yamakawa et al., 2007). The varietal difference in the response of chalkiness to temperature was evaluated by changing sowing dates so that a variety reached heading at different dates and experienced different temperature during grain filling. The advantage of this method over controlled environment such as growth chambers is that it represents actual field growing conditions (Ambardekar et al., 2011).
100
Chalkiness (%)
80
Chengnongshuijing IR64 Zhengxian232
Nanjing11 Aimi
Gu154 Yangdao6
60
40
20
0 Jul 20 Jul 30 Aug 9 Aug 19 Aug 29 Sep 8 Jul 20 Jul 30
Aug 9 Aug 19 Aug 29 Sep 8 Jul 20 Jul 30
Aug 9 Aug 19 Aug 29 Sep 8 Sep 18
Heading date Fig. 5. Response of chalkiness to heading dates in seven varieties grown in Wuxue, Hubei, China, in 2010.
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Furthermore, this method allows the evaluation of large number of varieties at the same time. The shortcoming of this system for studying temperature response is the potential confounding factors such as solar radiation and relative humidity. However, temperature during grain filling period is the most important environmental factor that influences rice chalkiness (Cheng and Zhong, 2001). The 42 varieties demonstrated large difference in their response to temperature during ripening phase for chalky grain formation. Three groups of varieties were formed based on the response of chalkiness to temperature and minimum chalkiness. Groups 1 and 2 were sensitive to temperature, whereas Group 3 was insensitive to temperature. Group 1 had lower minimum chalkiness than Group 2 across sowing dates. The grouping was fairly stable across the two years for the seven varieties tested in both years, except for Nanjing 11, which belonged to Group 3 in 2009 and Group 2 in 2010. Dongtingwanxian, Chengnongshuijing, and IR64 were representatives of Group 1. Interestingly, Group 1 had no japonica varieties. For varieties in Group 1, minimum chalkiness could be achieved through optimum sowing date. Bawangbian1, Aimi, Guichao2 and Zhenshan97B were the typical varieties of Group 2. Changing sowing date might result in a reduction in chalkiness for varieties in Group 2, but they never reached the minimum chalkiness that is desirable for rice consumers. Crop management practice could be more effective for improving appearance quality for varieties in Group 1 than these in Group 2. Some varieties in Group 3 such as Sankecun and Taishannuo maintained a high level of chalkiness, whereas others such as Yangdao6, Gu154, and Huanghuazhan had a low level of chalkiness regardless of sowing dates. Both indica and japonica varieties existed in Groups 2 and 3. These varieties with low and stable chalkiness in Group 3 could be considered as parents in the breeding program for developing new rice varieties with improved appearance quality especially for the future warming environment. Correlation between chalkiness and average daily temperature during ripening phase was observed in majority of tested varieties, although correlation coefficients in some varieties were not statistically significant due to small sample size (n = 4). When polled data from all varieties were used, statistically significant correlation was observed between chalkiness and temperature during ripening phase in both years. There was no clear difference among the three groups in the relationship between chalkiness and temperature. Close correlation between chalkiness and temperature was found even for some varieties in Group 3 with low and stable chalkiness across different heading dates. Various studies have shown that high temperature during specific stages of grain development tends to increase the occurrence of chalk in rice grains more than other stages (Lisle et al., 2000). Chalkiness is frequently found when the average temperature during the 20 days after heading exceeds 27 ◦ C (Wakamatsu et al., 2007). The chalky grains were most evident when the high temperature commenced four days after heading (Tashiro and Wardlaw, 1991). Tashiro and Wardlaw (1991) also stated that the time when the rice plant is exposed to high temperature stress during ripening determines the part with chalkiness in the grain. Eight-day exposure of rice plants to high temperature starting 12 days after heading induced mostly the milky-white grains while exposure for 8 days starting 16 days after heading formed more white-back grains. Ambardekar et al. (2011) reported that the effects of elevated nighttime temperature on chalkiness were incurred during certain stages of grain filling period and were variety-specific. In general, R6 and R7 grain-filling stages, which correspond to milk and soft dough stages, were most sensitive to warm nights for chalky grain formation. Chalkiness of medium-grain varieties (Bengal and Jupiter) was less sensitive to high night temperature than long-grain varieties (LaGrue, XL723, and Wells). In our study, we found that second week after heading had the closest correlation
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