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CROP PHYSIOLOGY & METABOLISM

Grain and Dry Matter Yields and Partitioning of Assimilates in Japonica/Indica Hybrid Rice

^a College of Agriculture, Yangzhou Univ., Yangzhou, Jiangsu 225009, China
^b Crop, Soil and Water Sciences Division, International Rice Research Institute (IRRI), DAPO Box 7777, Metro Manila, The Philippines

* Corresponding author (s.peng{at}cgiar.org)

	ABSTRACT

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Poor grain filling is a major constraint in utilizing the heterosis of japonica/indica hybrid rice (Oryza sativa L.). The objective of this study was to investigate potential causes of poor grain filling of japonica/indica hybrids (J/IHs) by examining the source-sink relations in 36 J/IHs. Thirty-six J/IHs and their parents and two intervarietal hybrids (IVHs) were grown at the Yangzhou University farm during the 1998, 1999, and 2000 rice growing seasons. Growth analyses were performed at heading and during grain filling period, and yield and yield components were determined at maturity. Results showed that J/IHs had 18.9% greater spikelet number per square meter than the two IVHs because of the difference in spikelet number per panicle, but grain yields of the two kinds of hybrids did not differ significantly as a result of low spikelet filling percentage in J/IHs. Above-ground dry matter accumulation of J/IHs was 73.8% greater than that of IVHs during the grain filling period. The above-ground dry matter per spikelet of the J/IHs was 12.7 and 4.1% higher than that of their parents and IVHs, respectively, indicating that source limitation was not the cause of poor grain filling of J/IHs. Translocation of assimilates and remobilization of stored assimilates from the straw to the grains during the grain filling period in J/IHs was about 64%, which was significantly less than that of IVHs. At maturity, only 44.1% of ¹⁴C fed to the flag leaves of J/IHs was partitioned into grains and the rest remained in stems and leaves. Poor translocation and partitioning of assimilates to the grain of J/IHs resulted in low harvest index. The results suggest that poor transport of assimilates to grains account for poor grain filling of J/IHs.

Abbreviations: IVHs, intervarietal hybrids • J/IHs, japonica/indica hybrids • LAI, leaf area index • NSC, nonstructural carbohydrate

	INTRODUCTION

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JAPONICA/INDICA HYBRIDS of rice possess greater heterosis in biomass production than other rice hybrid combinations (Yuan, 1994; Peng et al., 1999). Four major barriers, however, have hindered the exploitation of the J/IHs: sterility, tall plant stature, long growth duration, and poor grain filling (Yuan, 1994, 1998). So far, the first three of the four problems have been solved by the discovery and utilization of wide compatibility genes and other breeding strategies (Ikehashi, 1984; Lu et al., 1994; Yuan, 1998). The last problem to solve is poor filling of fertilized grains (Yuan, 1994, 1998).

Possible genetic, physiological, and ecological causes of the poor grain filling of J/IHs have been recently investigated (Zhu et al., 1997; Wang et al., 1998; Yang et al., 1999), but the causes of the poor grain filling are still unclear. There are two controversial hypotheses for the poor grain filling of J/IHs. Some investigators reported that limited dry matter production caused by low photosynthetic rate and early senescence of leaves during grain filling period, or relatively low ratio of source to sink (Lu et al., 1994; Yuan, 1994), resulted in poor grain filling of J/IHs. Our recent work, however, showed that J/IHs had high dry matter accumulation during grain filling, and their above-ground dry matter per spikelet was greater than that of IVHs (Wang et al., 1998; Yang et al., 1999), indicating that poor grain filling of J/IHs was not a result of source limitation. We hypothesized that poor grain filling might be related to poor partitioning of assimilates to the grain in J/IHs.

The objective of this study was to investigate the potential causes of poor grain filling of J/IHs by examining the source-sink relations in 36 J/IHs.

	MATERIALS AND METHODS

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Plant Materials and Field Design
Thirty-six J/IHs (F₁) were grown in the field of Yangzhou University farm, Jiangsu Province, China (32°30'N, 119°25'E), during the rice growing season (May–October) of 1998, and the experiment was repeated in 1999 and 2000. All J/IHs were made from six japonica lines with wide compatibility genes (female parents—PC311, Lunhui 422, Jw-8, Ce01, 02428, and Ce03) crossed with six indica lines (male parents—Miyang 23, 3037, Zaoxian-dang 18, IR36, Minghui 63, and Yangdao 4). The female and male parents and two IVHs, Shanyou 63 (indica/indica) and Liuyou 1 (japonica/japonica) were planted as the controls. The two IVHs were chosen because they have been planted in large areas in China. Seedlings were raised in the field with sowing date on 10 or 11 May and transplanted on 10 or 11 June at a hill spacing of 0.20 by 0.16 m with one seedling per hill. The plot dimensions were in 4.0 by 2.4 m. A completely randomized block design with three replications was used in the study. The soil of the field was sandy loam [Typic fluvaquents, Etisols (U.S. taxonomy)] with 24.5 g kg^-1 organic matter and available N-P-K at 105, 33.5 and 66.0 mg kg^-1, respectively. N (60 kg ha^-1 as urea), P (30 kg ha^-1 as single superphosphate), and K (40 kg ha^-1 as KCl) were applied and incorporated before transplanting. Nitrogen as urea was also applied at midtillering (40 kg ha^-1) and at panicle initiation (25 kg ha^-1). All the hybrids and lines headed on 15 to 19 August, and harvested on 4 to 8 October. Mean air temperatures for 10-d periods from heading to harvest were 26.7, 26.4, 25.1, 24.1, and 22.8°C, respectively.

Radioactive Labeling
Six genotypes (Ce03/Yangdao 4, Ce01/Miyang 23, PC311/Zaoxian-dang 18, PC311, Yangdao 4, and Shanyou 63) were chosen for radioactive labeling in 1999 and 2000. The three J/IHs were chosen because they showed great biomass production and great number of spikelets per square meter. Flag leaves of 10 main stems per plot were labeled with ¹⁴CO₂ at heading. Labeling was done between 0900 to 1100 h on a clear day with photosynthetically active radiation at the top of the canopy between 1000 to 1100 µmol m^-2 s^-1. The whole flag leaf was enclosed in a polyethylene chamber (25 cm in length and 4 cm in diameter) and sealed with tape to form a gas tight seal. Six milliliters of air in the chamber was drawn out and the same volume of gas was injected into the chamber, which contained 0.01 mol L^-1 CO₂ with specific radioactivity of ¹⁴C at 1.48 MBq L^-1. The chamber was removed after 0.5 h.

The labeled plants were sampled at maturity. Each plant was divided into leaf blades, stems (culms plus sheaths), and panicles (grains + rachis). Samples were dried at 70°C to constant weight, ground into powder, and then extracted by shaking in 632 g L^-1 boiling ethanol. The residue was extracted in 2:1 of 14.3 M HClO₄ to 10.6 M H₂O₂ for 4 h at 60°C. The radioactivity of ¹⁴C in both the extracted aliquots was measured by a liquid scintillation counter (Beckman Instruments Inc., Fullerton, CA). Radioactivity distribution in each part of the plant was expressed as a percentage of total radioactivity remaining in the aboveground portion of the plant.

Measurement of Photosynthetic Rate
The six genotypes chosen for radioactive labeling were also used for measuring net photosynthetic rate (P_n) of flag leaves on 9 to 10, 23 to 24, and 34 to 35 d after heading in 1999 and 2000. A gas analyzer (CID-PS CO₂ Analyzer System, CID, Vancouver, WA) was used to measure P_n of six leaves per genotype. Measurements were made during 0900 to 1100 h when photosynthetically active radiation above the canopy was 1000 to 1100 µmol m^-2 s^-1.

Sampling and Harvest
Plants were sampled from a 0.19-m² area (6 hills) at 6-d intervals from heading (80% panicles emerged) to maturity. Hills were sampled starting from the third row and two rows were left between the two samplings in order to minimize border effect. All plant samples were separated into green leaf blades (leaf), culm and sheath (stem), and panicles. The leaf area was measured with a leaf area meter (CID-203 Area Meter, CID) and expressed as leaf area index (LAI). Dry matter of each component was determined after drying at 70°C to constant weight.

The method for extraction of nonstructural carbohydrate (NSC) was modified according to the method described by Yoshida et al. (1976). The sample was dried in an oven and ground into fine powder. In a 15-mL centrifuge tube, 10 mL of 632 g L^-1 ethanol was added to 100 mg of ground sample and kept in a water bath at 80°C for 30 min. The tube was then centrifuged at 365.9 g for 20 min after cooling. The supernatant was collected and the extraction was repeated three times. The alcohol in the supernatant was evaporated on a water bath at 80°C until most of the alcohol was removed and the volume was reduced to about 3 mL. The sugar extract was then diluted into 25 mL with distilled water. The concentration of sugars in the extract was then analyzed as described by Somogyi (1945).

The residue left in the centrifuge tube was dried at 80°C for starch extraction. Two milliliters of distilled water was added to the tube containing the dried residue. The tube was then shaken in a boiling water bath for 30 min. Two milliliters of 9.36 M HClO₄ was added to the tube after cooling. The solution was shaken for 15 min. The extract was then made up to about 10 mL and centrifuged at 365.9 g for 20 min. The supernatant was collected and 2 mL of 4.68 M HClO₄ was added to the residue. The extraction was repeated as above. The supernatants were combined and made up to 50 mL with distilled water. The starch was analyzed by the method of Pucher et al. (1948).

Plants from a 2.5-m² area in each plot were harvested at maturity for the determination of grain yield. Yield components: panicles per square meter, spikelets per panicle, spikelet filling percentage, and grain weight were determined from the plants of 10 hills. Spikelet filling percentage was defined as the number of grains that sank to the bottom of a beaker filled with salt solution with specific gravity of 1.06 as a percentage of total spikelets. Grain plumpness was calculated using the following formula (Zhu et al., 1995):

[1]

In this study, the efficiency of translocation of assimilates and remobilization of stored assimilates in the straw to grains during grain filling period was expressed as transfer ratio of total assimilates. The percentage of remobilized carbon reserve and transfer ratio of total assimilates were calculated using the following equations (Yang et al., 2000):

[2]

Transfer ratio of total assimilates = (panicle dry matter at maturity - panicle dry matter at heading)/[NSC in stems at heading + (plant dry matter at maturity - plant dry matter at heading)].

The results were analyzed for variance by ANOVA. An analysis of variance was completed first for each group of genotypes (J/IHs, female parents, male parents and IVHs). The error variance for each group of genotypes was examined for variance heterogeneity by calculating the ratio of the large error variance to the small variance (Petersen, 1994). The error variances of the four groups of genotypes were homogenous in all parameters. Therefore, the average error mean square of the four groups of rice genotypes was used to test the significance of the among-groups variation. Data from each sampling date were analyzed separately. Means were tested by least significant difference at the 0.05 probability level (LSD0.05).

	RESULTS

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Grain Yield and Yield Components
The grain yield of J/IHs was 9.2 Mg ha^-1, which was 18.2% greater than that of their parents, but 2.6% less than that of the IVHs (Table 1). The three hybrids 02428/Yangdao 4, PC311/IR36, and PC311/Minghui 63 had the greatest grain yield (12.6–12.9 Mg ha^-1, respectively) among the 36 J/IHs, which was associated with a high number of spikelets (62 000–64 000 spikelets m^-2) and high spikelet filling percentage (80–84%). The average spikelet number per square meter of 36 J/IHs was 52 000, which was 30.8, 24.5, and 18.9% greater than that of japonica lines (female parents), indica lines (male parents) and the two IVHs, respectively. The greater number of spikelets per square meter of J/IHs was associated with larger panicles (Table 1). The average spikelet filling percentage of J/IHs was 69.4%, which was significantly less than that of their female and male parents and the IVHs. The grain weight of J/IHs was not significantly different from that of IVHs, but significantly greater than those of their parents. The results indicate that, in general, a greater number of spikelets per square meter did not translate into greater grain yield for J/IHs because of their low spikelet filling percentage.

View larger version (24K): [in this window] [in a new window]   Fig. 1. Changes in stem dry weight of japonica/indica hybrids of Ce03/Yangdao 4 (J/I-1), Ce01/Miyang 23 (J/I-2) and PC311/Zaoxiang-dang 18 (J/I-3) and intervarietal hybrid of Shanyou 63(SY) during ripening period. Measurements were taken in 1998, 1999, and 2000. Vertical bars represent ±SE of the mean of three replications.

	DISCUSSION

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Lu et al. (1994) reported that low spikelet filling percentage of J/IHs mainly resulted from the number of sterile spikelets. Our results showed that both sterile spikelets and poor filling of fertilized grains (expressed as grain plumpness) contributed to low spikelet filling percentage of J/IHs. However, poor filling of fertilized grains was a major factor (Table 2). The discrepancy between their data and that reported here might be due to the limited number of J/IHs used in their study. We did find two combinations among the 36 J/IHs which had high percentage of sterile spikelets (data not shown), which may be caused by poor compatibility between japonica and indica parents (Ikehashi and Wan, 1998).

Both IVHs and J/IHs had greater biomass production than inbred cultivars (Table 3). But the biomass attained at each growth stage was different between the two kinds of hybrids. For IVHs, only 30.8% of biomass was produced after heading. This is consistent with the report that the great biomass production of IVHs occurs in vegetative and reproductive stages, but not during the grain filling period, in contrast to inbred cultivars (Yan, 1981). For J/IHs, 43.2% of biomass was produced from heading to maturity, and the dry matter accumulation was 73.8% greater than that of IVHs during this period (Table 3). Increased dry matter accumulation after heading would be greatly beneficial to attain higher grain yield because 60 to 100% of the yield comes from assimilates produced during the grain filling period (Yoshida, 1981). It is notable that J/IHs had a large LAI and a high photosynthetic rate during the grain filling period compared to their parents and IVHs (Table 4 and 5). The greater biomass production in J/IHs may be attributable, in part, to the greater LAI and leaf photosynthetic rates and results also indicated that the rate of leaf senescence during the grain filling period was less in J/IHs than in their parents and IVHs (Table 4).

Cao et al. (1992) classified rice varieties into sink-limiting, source-limiting, and intermediate types according to their source-sink relationships. Most indica/indica or japonica/japonica hybrid rice belong to source-limiting type, with a high ratio of spikelet number to leaf area at heading and low spikelet filling percentage. Some researchers attributed poor grain filling of J/IHs to source limitation because of the large number of spikelets (Lu et al., 1994; Yuan, 1997). We found, however, J/IHs had both a greater number of spikelets and greater biomass production (Table 1 and 3), and the aboveground dry matter per spikelet was more than their parents and IVHs (Table 6). Since little C reserve was remobilized, and much NSC remained in the stems at maturity (Table 7 and Fig. 1), and less ¹⁴C fed to the flag leaves was partitioned into panicles (Table 8), we conclude that poor grain filling of J/IHs was a result of poor translocation and partitioning of assimilates into grains, rather than limited biomass production or source limitation.

Many factors, such as phloem structure (Cronshaw, 1981) and phloem loading (Delrot, 1989) and unloading (Eschrich, 1989; Patrick, 1997), affect translocation and partitioning of assimilates. Our earlier work has shown that J/IHs were superior to IVHs, in terms of the number and cross sectional area of vascular bundles, vessels and phloem of elongated internodes, the peduncle and rachis, and primary and secondary branches (Wang et al., 1998). This indicated that the phloem structure of J/IHs is not a barrier of assimilate transport. We found, however, that J/IHs had low sink strength (sink size x sink activity) because of low sink activity (the contents of adenosine triphosphate, polyamines and indole-3-acetic acid, and activities of the enzymes related to starch synthesis in grains) during grain filling (Yang et al., 1999, 2001). It is generally accepted that sink strength controls the direction and rate of transport and partitioning of assimilates in plants (Venkateswarlu and Visperas, 1987; Delrot, 1989; Eschrich, 1989; Patrick, 1997). Thereby we argue that low sink activity in J/IHs may result in poor translocation and partitioning of assimilates into grains, leading to more resources for vegetative growth. Understanding the mechanism of poor translocation and partitioning of assimilates into grains in J/IHs may help to improve the grain filling of J/IHs.

	ACKNOWLEDGMENTS

 
The work was financed by the National Natural Science Foundation of China (Project No. 39970424) and the International Rice Research Institute (IRRI). The authors thank Lijun Liu and Youzhong Lang for their assistance in some laboratory work.

Received for publication July 16, 2001.

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